T
Tabanidae
A family of flies (order Diptera). They commonly
are known as horse flies or deer flies, and some are
called yellow flies or greenheads.
 Flies
Tachinidae
A family of flies (order Diptera). They commonly
are known as tachinid flies.
 Flies
 Tachinid Flies
Tachinid Flies (Diptera:
Tachinidae)
James E. O’Hara
Agriculture and Agri-Food Canada, Ottawa, ON,
Canada
There are well over 100 families in the order Dip-
tera, or true flies, and most of them are comprised
entirely of species with free-living larvae. There
are, however, about 20 families with at least some
species classed as parasitoids, species that live
within other animals as larvae and kill their hosts
before progressing on to the adult stage. It is esti-
mated that this type of parasitic life style evolved
over 100 times in the Diptera and multiple times
within certain families. About 16,000 of the
approximately 120,000 described species of
­ iptera are parasitoids, and about 10,000 of them
D
belong to a single family, the Tachinidae. All
tachinid flies are parasitoids in their larval stage
and their hosts all belong to the Arthropoda,
almost exclusively the Insecta. The true diversity
of the Tachinidae is likely many thousands of spe-
cies higher than the 10,000 currently described,
making this family a good candidate for the most
speciose family of Diptera and without question
the most successful with a parasitic way of life.
Most tachinid flies are larger than a house fly
and noticeably more bristly, but they range in size
from 2–20 mm and across the family there is a tre-
mendous variety of shapes, colors and degree of
bristling. The features upon which the family is
founded and that support its monophyly (descent
from a common ancestor) are rather subtle. In
addition to features shared with other families of
the Oestroidea (Rhinophoridae, Sarcophagidae,
Calliphoridae, and Oestridae), adult tachinids pos-
sess a well developed postscutellum (a rounded
bulge below the hind part of the thoracic dorsum)
and the labrum (or mouth hook) of the first instar
larva is fused with the cephalopharyngeal skele-
ton. The family is cosmopolitan in distribution
and most diverse in the subtropics and tropics.
Classification
The Tachinidae are currently divided into four
subfamilies, the Phasiinae, Dexiinae, Exoristinae
and Tachininae (see Fig. 1 for representatives of
each). The smallest of these in terms of species,
3676
T Tachinid Flies (Diptera: Tachinidae)

Tachinid Flies (Diptera: Tachinidae), Figure 1  Representative Tachinidae. Row 1 (top), left to right:
Exoristinae, Gonia porca, Belvosia bifasciata, Calolydella lathami, Chrysoexorista ochracea, Cyzenis browni,
Leschenaultia fusca, Trigonospila sp., Lespesia stonei, Winthemia vesiculata; Tachininae, Microtropesa sp.
Row 2: Tachininae, Chrysotachina sp., Siphona (Siphona) lutea, Genea sp., Euscopolia dacotensis,
Xanthoepalpus bicolor, Siphona (Baeomyia) xanthogaster, Ormia reinhardi, Vanderwulpia sequens,
Paradejeania rutilioides, Oestrophasia sp., Neximyia sp. Row 3: Phasiinae, Penthosia satanica, Gymnosoma
par, Besseria brevipennis, Cylindromyia (Cylindromyia) euchenor, Phasia aldrichi, Trichopoda sp.;
Dexiinae, Zelia vertebrata, Billaea sp., Periscepsia (Ramonda) clesides, Uramya halisidotae. Row 4: Dexiinae,
Amphitropesa sp., Euthera tentatrix, Euchaetogyne roederi, Voria aurifrons, Rutilia (Donovanius) regalis,
Euantha litturata, Cordyligaster septentrianalis, Trixodes obesus.

the ­Phasiinae, is possibly but not demonstrably a
monophyletic lineage in which all species are
parasitoids of Hemiptera-Heteroptera, or true
bugs. The Phasiinae are morphologically diverse
and include most of the tachinid species that lack
strong bristling. The Dexiinae are the next largest
subfamily and the only one widely regarded as
monophyletic, a belief based on shared derived
features of the male ­terminalia. In particular,
male dexiines possess a hinged connection
between the basiphallus and distiphallus of the
phallus (or aedeagus) that is not found in other
tachinids. Some of the most visually stunning
tachinids belong to the dexiine tribe Rutiliini, an
Oriental and Australasian group of mostly large
and metallic-colored flies. The Exoristinae and
Tachininae are the most speciose subfamilies.
The former is more homogeneous in appearance,
with many species grayish black in color and
moderately bristly. Given this combination of
homogeneity and diversity, the Exoristinae are, as
a group, the most taxonomically difficult of all
Tachinidae. The Tachininae are more morpho-
logically diverse and include some of the largest,

most colorful, and most bristly of tachinids. The
subfamily also includes some of the smallest and
least conspicuous tachinids.
The phylogenetic relationships within the
Tachinidae are unclear at the higher levels. There
are currently about 40 tribes recognized, but not
all are monophyletic and the relationships within
and between them are poorly known. Many of the
main characters used to distinguish tachinid spe-
cies are not unique to particular lineages, thus
inhibiting attempts to infer relationships through
parsimony analysis of external morphological
traits. It is possible that more detailed study of
male and female terminalia and immature stages
will provide better, less homoplastic, characters
for phylogenetic analysis. Molecular systematics
is beginning to show promise in the elucidation
of tachinid relationships but there have been few
studies to date.
The classification at the generic level is rela-
tively stable in the Nearctic and Palearctic
regions where the tachinid faunas are fairly well
known. There are literally thousands of unde-
scribed species in the other regions, and until
those species have been better studied the gen-
era of those regions will remain poorly charac-
terized. Certain authors in the first half of the
1900s had a tendency to oversplit the Tachinidae
to the extent that each genus would often com-
prise only one or two species, and this legacy is
still in evidence today in less studied parts of the
world. For example, the Neotropical Region has
nearly 30% of all described tachinid species but
over 50% of all genera.
Life Stages
Adult
The variation in size and shape of adult tachin-
ids has been mentioned above and is evident
in  the specimens shown in Figure 1. Tachinids
range in color from pale yellow to jet black, with
some species shiny metallic blue or purple (e.g.,
Tachinid Flies (Diptera: Tachinidae)
T 3677
­ ymno che ta), or brilliantly metallic and multi-
G
colored (many Rutiliini). Wings are usually clear
but are darkened or patterned in some species,
or even bicolored. Despite the huge range in
size, shape and color within the family, the
majority of tachinids are grayish black and
5–10  mm in length. Many species have four
black longitudinal stripes on the thorax, in con-
trast to members of the closely related family
Sarcophagidae that usually have three stripes.
The head is about the width of the thorax,
with compound eyes that vary in size from about
half head height to almost head height. Eyes are
only rarely holoptic (meeting above) and range
from bare to densely haired. Antennae range
from tiny to enlarged and in certain species
(males only) are bifid, trifid, or elaborately
branched (Fig.  2). Mouthparts are present and
functional, apically padlike for feeding on liq-
uids (e.g., nectar and honey dew), and occasion-
ally greatly elongated (up to length of body)
(Fig.  3). Chaetotaxy (arrangement of setae) on
the head is greatly varied and very useful for
the identification of species.
Tachinid Flies (Diptera: Tachinidae), Figure 2 
Head of male Borgmeiermyia sp.,
illustrating elaborately branched antenna.
3678
T Tachinid Flies (Diptera: Tachinidae)
Tachinid Flies (Diptera: Tachinidae), Figure 3 
Siphona pisinnia, illustrating unusually
long proboscis.
The thorax is slender to broad, typically ­setose
but almost bare dorsally in many Phasiinae. The
prosternum between the fore legs is typically
haired in Exoristinae, bare in Phasiinae and Dexii-
nae, and varied in Tachininae. Legs are setose and
in some groups elongated, without elaborate mod-
ifications except for the flattened, feather-like setae
on the hind tibia of Trichopoda. Wings are well
developed, haired along several veins in a few spe-
cies, and show some variation in venation. Vein M
in the center of the wing has a bend near the wing
margin (bend rarely absent, e.g., Cinochira) and
the vein may terminate in vein R4 + 5 or the wing
margin. Very rarely, vein M fades out at about the
usual location of the bend. Chaetotaxy of the tho-
rax, especially the arrangement of setae on the
upper surface (i.e., scutum and scutellum), is taxo-
nomically and diagnostically very important.
The abdomen is greatly varied from narrow
and long to short and round, and from nearly bare
to thickly setose. A few species are very good wasp
mimics (e.g., Cylindromyia (Ichneumonops) mira­
bilis) with a wasp-like abdomen. Males of some
Uramya species have the tip of tergite 5 con-
stricted and lengthened posteriorly into an almost
cone-like appendage that can be nearly as long as
the rest of the abdomen (slightly developed in
Uramya halisidotae, see Fig. 1). Segments 6–11
comprise the terminalia and are highly varied
morphologically in both sexes. The female termi-
nalia show obvious modifications related to ovi-
position: short unspecialized ovipositors in most
species that lay eggs on foliage, tubular telescopic
ovipositors in some species that lay eggs with great
precision on their hosts, and piercers of varied
shapes and sizes derived from different sternites in
different lineages. The terminalia, particularly
those of the male, provide some of the best charac-
ters for interpreting the phylogenetic relationships
within the Tachinidae and are helpful for identifi-
cations at the species and genus levels.
Egg
Modifications to the female reproductive system,
egg, and ovipositor permit tachinids to parasitize
hosts in a wide variety of ways. In the primitive
condition, an unembryonated egg is deposited
directly on a host by means of an extensible
­ovipositor. The egg is typically thick and convex
on its upper surface and thinner and flatter on its
under surface, and is attached to a host with a
glue-like substance. Tachinids employing this
mode of attack are termed oviparous because the
egg is undeveloped when laid and the first instar is
not fully formed for several days. The first instar
may then burrow directly through the underside
of the egg and through the host’s integument, or
may exit the egg through an operculum and then
burrow into the host. Certain oviparous tachinids,
including most Phasiinae, inject an egg directly
into a host by means of a piercing ovipositor.
Oviparous tachinids comprise the Phasiinae and
some Exoristinae (Exoristiini, Winthemiini, and
a  few species of Blondeliini and Eryciini). The
female reproductive system of an oviparous
tachinid is shown in Fig. 4.
The majority of tachinids are ovolarviparous,
depositing eggs that contain fully d­ eveloped first

Tachinid Flies (Diptera: Tachinidae),
­Figure 4 ­Female reproductive system of an
oviparous tachinid, Smidtia fumiferanae. Not more
than one fertilized egg is retained in the common
oviduct at a time. Abbreviations: ac gl, accessory
gland; c ov, common oviduct.
instars. The female reproductive system of these
flies is modified to retain fertilized eggs in an
ovisac or uterus until they are ready to hatch.
The ovisac stretches and forms a coil as hundreds
to thousands of fertilized eggs are added to it
(Fig.  5). The females of numerous ovolarvipa-
rous species still deposit eggs directly on a host,
but other strategies, some quite ingenious, are
used as well. In most cases the eggs have a thin
chorion and hatch almost immediately after
deposition. The eggs of many species are laid
near a host or are broadcast on its food plant and
the motile first instar either crawls to a host or
waits for one to pass by. The eggs of Dexiini and
most Rutiliini (Dexiinae) are deposited on the
ground and the first instar burrows into the soil
in search of a beetle host. A few ovolarviparous
species have the unusual habit of ovipositing an
egg into the mouth of a host. Members of the
Goniini (Exoristinae) have tiny “microtype” eggs
that they scatter on the food plant of a host, usu-
ally in the vicinity of feeding damage, and these
eggs hatch only after being ingested by a host.
Various types of piercers have evolved in ­different
Tachinid Flies (Diptera: Tachinidae)
T 3679
Tachinid Flies (Diptera: Tachinidae), Figure 5 ­
Female reproductive system of an ovolarviparous
tachinid, Lypha fumipennis. Fertilized eggs form
tightly packed rows within a coiled ovisac.
lineages of ovolarviparous tachinids to inject an
egg into a host.
The number of eggs produced by a tachinid is
roughly proportional to the likelihood of a first
instar infecting a host. Species that oviposit directly
on or in a host have a high success rate and low
fecundity, generally less than a few hundred eggs.
Species that oviposit in the vicinity of a host often
produce many hundreds of eggs, and species with
microtype eggs or that oviposit rather indiscrimi-
nately on a host’s food plant have the highest
fecundity of all, with the number of eggs produced
numbering into the thousands.
Some tachinids are cited in the literature as
larviparous, meaning in the strict sense of the term
that their eggs hatch internally and first instars are
oviposited instead of eggs. However, the term lar-
viparous has also been used in a looser sense to
describe tachinids that deposit fully developed
eggs that hatch immediately after deposition (i.e.,
ovolarviparous tachinids). The eggs are frequently
so thin and membranous as to be almost invisible.
In some cases, first instars inside a freshly killed
female will break free of their thin-walled eggs
and escape through the ovipositor, giving the
impression that the species is normally larvipa-
rous. Dissections of killed females may also reveal
first instars free in the ovisac that would, under
3680
T Tachinid Flies (Diptera: Tachinidae)
normal circumstances, remain in the egg until
after oviposition. Although there may be species
that are truly larviparous, they have yet to be reli-
ably documented.
The eggs of tachinid flies are not intended to
provide long term protection for a first instar.
Tachinids do not overwinter in the egg stage or as
free-living first instars.
Larval instars
Tachinids, like other cyclorrhaphan flies, have three
larval instars. The first instar is remarkably varied
externally, adapted to cope with the different cir-
cumstances under which eggs are placed in the
environment. First instars that must search for
hosts on their own have evolved a number of spe-
cializations to aid movement and avoid desicca-
tion. Their bodies are often adorned with bands of
small spines or sclerotized plates, in some instances
displaying more morphological variation between
species than the bodies of their adults. First instars
of ovolarviparous species can be removed from
pinned adult females in museum collections and
rehydrated for morphological study. Research into
the diversity of first instars is expected to contrib-
ute valuable characters for tachinid taxonomy and
for phylogenetic analyses of tachinid relationships.
First instars that enter a host on their own do
so with the cutting action of a sharp labrum that is
varied apically from pointed to axe-like. The labrum
is scraped against the host’s integument with a
­back-and-forth motion until a hole is created, likely
aided by an enzymatic substance in the saliva. Once
inside the host, the first instar may attach itself pos-
teriorly to its entrance hole or to the host’s tracheal
system, or it may remain free in the host’s body.
First instars that remain free usually attach them-
selves to the tracheal system when they become
second instars to provide an adequate supply of
oxygen for developmental needs. A first instar may
start to feed immediately and can pass through all
three instars in as little as a few days, but in most
species the ­larval stage lasts a few weeks. Not
uncommonly, the  first instar delays development
until the host reaches a particular stage. It might
migrate to specific places within the host during its
period of inactivity, such as the salivary glands, ganglia
or muscles, where it is able to evade the host’s immune
system. It is generally hormonal signals within the
host that trigger the first instar to relocate and
­continue development. Some tachinid species over-
winter as first instars within their hosts.
A first instar feeds on host hemolymph and
carefully avoids damaging any vital organs, living
more like a parasite than a host-killing parasitoid.
This changes during the second instar when rapid
feeding and growth begin. If a larva did not form a
connection to tracheal or outside air during its first
instar, then it typically does so as an early second
instar. At the same time as the tachinid larva is
attempting to feed and obtain oxygen, the host
is attempting to kill it through an immune response
termed encapsulation. In the early stages of encap-
sulation, a thin membrane forms around the larva.
A first instar can be almost completely encased, but
if this happens then it can usually still feed on
hemolymph that filters through to it. The larger sec-
ond instar frees itself anteriorly and begins to feed
more aggressively on non-vital tissues, at the same
time continuing to stay attached to an air supply
posteriorly. The capsule that forms around the larva
is termed a respiratory funnel and it becomes larger
and thicker as time passes. The ability of the Tachin-
idae to thwart the encapsulation process is one of
the keys to their success. This ability does not afford
total protection and some larvae are killed by encap-
sulation even in suitable hosts. Other potential hosts
that are seldom successfully parasitized may have
immune systems that are more effective at combat-
ing tachinid invaders or there may be other incom-
patibilities between parasitoid and host.
The primary cutting structure in the first
instar, the labrum, is replaced in later instars by
paired mandibles. The second instar is a voracious
feeder that selectively consumes non-vital tissues,
especially fat stores. The host may appear normal
or somewhat lethargic, or may display atypical
behavior induced in some way by the parasitoid.
 Tachinid Flies (Diptera: Tachinidae)
T 3681

The third instar leaves the respiratory funnel and

feeds less discriminately. Except in rare cases, the
host is killed and the third instar continues to feed
until fully grown or until the food supply is
exhausted. The latter situation is not uncommon
among tachinids that develop gregariously within
a single host and the tachinid adults that develop
from under-fed third instars can be half or less the
size of typical adults.

Puparium

Pupation in tachinid flies takes place within a

puparium, the hardened shell of the third instar.
Most commonly the third instar crawls away from
the host and pupariates in the soil or ground litter,
but in some species pupariation takes place within
the host. A few species that pupariate within adult
beetles strategically cut openings in the host’s
integument to facilitate respiration and the even-
tual exit of the adult (Fig. 6). Quite a few tachinids
Tachinid Flies (Diptera: Tachinidae), Figure 6 
overwinter in the pupal stage.
Puparium of Myiopharus neilli within remains of
The puparium is roughly cylindrical with two
its host, an adult sunflower beetle (Zygogramma
small anterior spiracles and generally two conspic-
exclamationis). Anterior and posterior ends of
uous and darkened posterior spiracular discs, for
puparium are visible. The beetle is typically
respiration. The posterior spiracular discs can be
decapitated between the prothorax and
flush with the surface of the puparium or raised
mesothorax. Underside of beetle is shown with
above it, and directly level with the midline or
legs removed. Abbreviations: a spr, anterior
above or below it. In a few species the spiracular
spiracle; p spr ds, posterior spiracular disc.
discs are fused into one. Quite often there are three
or four spiracular slits on the upper surface of each
spiracular disc. The morphology of the spiracular although poorly represented on smaller islands
discs is highly varied and provides useful charac- that are distant from larger land masses (e.g.,
ters for the identification of species. An adult Hawaiian Islands, Galapagos Islands). The total
tachinid emerges from its puparium by inflating a number of described species is about 10,000, but
balloon-like ptilinum from behind its face to force this number is misleading because only the Nearc-
open the anterior end of the puparium along a cir- tic and Palearctic faunas are relatively well known.
cular line of weakness. The Neotropical Region has the largest number of
described species at about 3,000, almost twice that
of any other region and representing 30% of the
Distribution and Evolution world’s fauna, yet there are so many undescribed
species and the region is so vast and under-­collected
The Tachinidae are well distributed throughout all that the actual number is probably well over
zoogeographic regions of the world (see Table 1), 5,000.  Similarly, Australia has a described fauna
3682
T Tachinid Flies (Diptera: Tachinidae)
Tachinid Flies (Diptera: Tachinidae), Table 1  The sister group to the Tachinidae has not
Number of tachinid species and genera in each
biogeographic region and the world
Biogeographic Genera Described species
region
Neotropical 822 2,864
Nearctic 304 1,345
Palearctic 405 >1,600
Afrotropical 213 1,006
Oriental 264 725
Australasian 230 808
World 1,523 about 10,000
Numbers for genera follow O’Hara (2007) and for
described species follow the most recent regional
­catalogues. Actual number of tachinid species
(described + undescribed) in the world is likely greater
than 15,000. Some species and many genera are found in
more than one region so the values for the world are not
the sums of the regional numbers.
numbering about 500 species but the actual fauna
has been  estimated at 3,500–4,000 species. The
tachinid faunas of the Afrotropical and Oriental
regions have not been well studied and also con-
tain many undescribed species. Given these cir-
cumstances, it is likely that the total number of
tachinid species in the world is in excess of 15,000.
Some older insect groups show an interesting
pattern of distribution that links the faunal ele-
ments in South America, Australia and sometimes
southern Africa. These relationships are thought
to date back to Gondwanaland when the southern
continents were fused into a single land mass. By
the end of the Cretaceous Period about 65 million
years ago, Africa was drifting northward and the
connection between South America and Australia
(via Antarctica) was becoming cooler and more
tenuous. If the Tachinidae began their radiation in
the Cretaceous then evidence of this might be
sought in the fossil record and modern distribu-
tion patterns. However, no fossil Tachinidae are
known from the Cretaceous and there is no clear
evidence of southern relationships, so the family is
assumed to be of Tertiary origin.
been determined but is to be found among the
families Sarcophagidae, Calliphoridae, Rhino-
phoridae and Oestridae. These five families are
united by their possession of a row of setae on the
meron (a sclerite above the hind leg) and together
comprise the superfamily Oestroidea.
Hosts
The evolutionary success of the Tachinidae is
closely tied to their exploitation of arthropods as a
source of hosts. The family is a difficult one taxo-
nomically and a relatively young one, suggesting
that it is still undergoing rapid radiation within its
specialized niche. The life of an endoparasitoid is a
complex one with strong selective pressures cen-
tered around finding and parasitizing a host. In
some cases selection has produced generalists that
attack many species of hosts, in others selection
has produced specialists that attack only one or a
very few host species.
Hosts of Tachinidae are all arthropods, almost
exclusively insects. For many tachinid species the
hosts are unknown. The non-insect hosts com-
prise only a few species in the Chilopoda (centi-
pedes), Scorpiones (scorpions), and Araneae (a
single record from a spider). These hosts are
attacked by a few species of Tachininae, mostly
within the Polideini.
The majority of hosts of tachinids are Lepi-
doptera, mostly caterpillars that feed on foliage in
exposed situations but also others that are con-
cealed, such as leafrollers and stem borers. Lepi-
doptera represent the main hosts of the two largest
tachinid subfamilies, Exoristinae and Tachininae,
and are also significantly attacked by the third
largest subfamily, the Dexiinae. The smallest sub-
family, the Phasiinae, attacks only Heteroptera and
there is only one genus outside the Phasiinae
(Euthera in the Dexiinae) that also attacks het-
eropteran bugs.
Larval and adult Coleoptera of about 20 fami-
lies are attacked by a small number of species in

the Exoristinae and Tachininae and by the major-
ity of species in the Dexiinae. The greatest number
of beetle hosts belong to the Scarabaeidae, larvae
of which are parasitized by nearly all members of
the sizable dexiine tribes Dexiini and Rutillini;
adult scarabs are parasitized by members of the
small dexiine tribe Palpostomatini.
Hymenopteran hosts are chiefly larval Sym-
phyta, many of which are exposed defoliators like
larval Lepidoptera. A small number of wasps
(Vespoidea) and ants (Formicidae) also serve as
hosts. Hymenopteran parasitoids belong to the
Exoristinae and Tachininae. The remaining hosts
of tachinids are also parasitized by members of
these two tachinid subfamilies and include the
Orthoptera (crickets, grasshoppers, katydids), Blat-
taria (cockroaches), Mantodea (mantids), Phasma-
todea (leaf and stick insects), Dermaptera (earwigs),
Diptera (flies), and Embioptera (webspinners).
Some tachinids are solitary endoparasitoids
and will fight one another within a host until a sin-
gle larva remains alive. Other species, especially
those that parasitize larger hosts, are not aggressive
toward one another and numerous individuals can
successfully develop into adults. If conditions are
crowded, then some maggots may die and the rest
may produce stunted adults. Multiparasitism, the
development of more than one larva within a host,
also can result in more than one tachinid species
successfully parasitizing a single host.
There are a variety of factors that determine
how many host species a tachinid species will par-
asitize. The adult female plays a large role in host
range by deciding where to oviposit. If eggs are
laid on or near a host or injected into it, then the
host range is determined by the specificity of the
ovipositing female and the ability of the larva to
develop in the selected host. Females of some spe-
cies search for a particular microhabitat and once
in it (e.g., a particular plant species) will oviposit
on different potential host species encountered
there. One tachinid species, Compsilura concin­
nata, has become well known because it is highly
indiscriminate in its selection of hosts and its lar-
vae are capable of developing in many different
Tachinid Flies (Diptera: Tachinidae)
T 3683
species. The female fly injects an incubated egg
into a host and the larva escapes the defenses of its
varied hosts by living and feeding in the midgut
between the peritrophic membrane and gut wall.
Compsilura concinnata has almost 200 recorded
hosts in numerous families of Lepidoptera and
also parasitizes sawflies and a species of weevil.
Host Location
The ancestral mode of host finding in Tachinidae
likely involved a series of cues, olfactory and
visual, that guided a searching female to the right
microhabitat and host plant and then to an
exposed host, where perhaps tactile stimuli initi-
ated oviposition behavior. This method of host
location is still common, but there are many
sophisticated behaviors that have evolved to aid
the searching tachinid. For example, oviposition
in numerous tachinids does not involve the visual
sighting of a host. In the case of Goniini, micro-
type eggs are deposited on the food plant of a
host, usually in response to plant volatiles released
at the site of feeding damage, and the eggs do not
hatch until ingested by a host. Many other tachin-
ids also oviposit on the food plant of a host or in
a specific microhabitat (e.g., those that parasitize
litter insects like cockroaches and earwigs), not
necessarily within sight of a host, and the first
instar locates a host on its own or lies in wait for
one to pass by. Certain tachinids (e.g., Lixophaga
diatraeae) are stimulated to oviposit near the bur-
row of a concealed host by the odor of the frass
that has accumulated at the entrance. Members of
the Dexiini oviposit on the ground, leaving the
task of finding a soil-dwelling scarab host to their
first instars.
The importance of visual cues varies in differ-
ent tachinids. Those that search for hosts at night
must rely mostly on other sensory cues to find an
acceptable place to oviposit. Some tachinids that
lay eggs on exposed caterpillars not only select
hosts of a particular size, presumably by sight, but
may also place the eggs near the front of the host
3684
T Tachinid Flies (Diptera: Tachinidae)
where they cannot be reached by the host’s man-
dibles. A few species that parasitize adult beetles
assist their first instars by ovipositing near natural
openings such as the mouth, anus and spiracles.
Not uncommonly, females that oviposit on a spe-
cific part of a moving host have a telescopic ovi-
positor that can be brought forward under the
body and in front of the head to permit egg place-
ment to be visually guided. Some tachinids attack
their hosts on the wing, requiring acute vision as
well as maneuverable flight.
In most instances where olfaction is involved,
the chemical cues that attract a female tachinid to
an oviposition site are the standard odors of a host
or host plant, or odors (volatiles) given off by a
damaged plant that is being fed upon. More
unusual are the cues that attract certain Phasiinae
to their hosts; these species use the pheromones of
their heteropteran hosts as host-finding kai-
romones. The antennae of these tachinids are up
to 10 times more sensitive to the bug pheromones
than are those of the bugs.
The vast majority of Tachinidae are incapable
of hearing, but members of the tribe Ormiini
have evolved an inflated prosternum between the
front legs that functions as a tympanal organ. This
structure allows these tachinids to locate their
orthopteran hosts at night by homing in on their
mating calls. So effective are these parasitoids in
finding their calling hosts that some hosts have
evolved strategies to reduce their susceptibility.
The tympanal organs are different in male and
female ormiines, with those of the female very
receptive to the low frequency calls of hosts and to
sounds in the ultrasonic range, whereas males are
only sensitive to ultrasonic sound. It has been sug-
gested that the sensitivity of these nocturnally
active flies to high frequency sound helps them
avoid predators such as insectivorous bats.
Mate Finding
Male and female tachinids that are commonly
found in meadows and along roadways, particularly
on wildflowers, probably mate in those places,
e.g.,  Phasiinae, larger Tachinini, most Siphonini.
There are other tachinids that go to species-specific
aggregation sites to find a mate. The most notewor-
thy of all aggregation phenomena is “hilltopping,”
where males of certain tachinid species fly to the
tops of hills or mountains to await the arrival of
females. Each species has its own predetermined
time of day during which it will hilltop, with some
species preferring the morning, others the after-
noon, and the night-active Ormia hilltopping at
dusk. On hot days the activity begins earlier than
on cool days, and on cloudy days there are fewer
flies. A good hilltop on a hot and sunny day is a
frantic place, with anywhere from a few tachinid
species to 75 or more (in exceptional habitats) vis-
iting the hilltop by mid afternoon, after which fly
activity drops off considerably. Virtually all the
observable individuals are males, presumably
because they remain on the hilltop for some time
whereas females stay only long enough to find a
mate. Males of each species are guided by instinct
to a particular place on a hilltop and successive
generations will return to the same spot year after
year. One species may prefer a sunlit spot on the
ground at the base of a bush, another will alight on
tree trunks, and others will sit on foliage to one side
of the hilltop or buzz around the topmost branches
of a bush at the hilltop’s center, etc. Males of some
species spend most of their time perched at pre-
ferred locations, darting out frequently to inspect
passing insects. Males of other species are in almost
constant motion as they fly from point to point but
seldom alight.
Aggregation sites for male tachinids are not
always on hilltops. The branches of an isolated
tree, or shrubs alongside a stream, or a patch of
ground below a bush, are a few of the places where
males of one or more species may congregate to
await a potential mate, nearly always in sunlit situ-
ations. Tree trunks also serve as aggregation sites
for a number of species. Often several males will
occupy the same tree trunk, but the males of some
species (e.g., Trixodes obesus) are always found
singly. Generally only one or a few trees in an area

are attractive to aggregating males and these trees
will be frequented by the same species year after
year. Some species do not alight on a tree but
instead fly in a zig-zag pattern up the trunk for a
few moments before flying to another tree to
repeat the behavior.
It is not uncommon for the antennae of male
tachinids to be larger than those of females, but
usually this difference is slight. Rarely, the differ-
ence is dramatic with the first flagellomere greatly
enlarged over that in its conspecific female, or even
bifid or multi-branched. Since antennae serve a
mostly olfactory function, it is presumed that such
antennae help in the location and/or courtship of
females. Very little is known about courtship and
mating in tachinids, especially under natural
conditions.
Ecology
The vast majority of hosts of tachinid flies are
plant-feeding insects. As a result, parasitism by
tachinids has two major effects at the community
level: a reduction of host populations, and an indi-
rect reduction in feeding damage to plants used by
hosts. The level of parasitism can vary greatly, from
less than 1% to approaching 100%, depending on
such factors as the size of a host population, size of
the parasitoid population, and environmental con-
ditions. Parasitism levels usually vary locally from
one portion of a host’s range to another. Parasitism
rates are quite dynamic and rise and fall through
the generations and from area to area in cycles
that both influence, and are influenced by, host
populations. The net effect is generally low rates of
parasitism (under 5%) with occasional genera-
tions where parasitism is significantly higher. Most
of the studies into parasitism rates by tachinid flies
have involved pest insects, some of which cause
damage to crops or forests on an annual basis and
some of which are only of economic concern dur-
ing outbreaks. How quickly a tachinid population
can take advantage of an increase in host numbers
is dependent on a number of factors but is
Tachinid Flies (Diptera: Tachinidae)
T 3685
i­ nfluenced in part by the oviposition strategy and
fecundity of the tachinid species involved.
Tachinid species can be broadly divided into
two types, specialists and generalists. As the names
imply, specialists attack one or a few host species
and generalists attack multiple hosts. On the whole,
tachinids tend to be less host specific than
hymenopteran parasitoids. Factors affecting
tachinid host range include, but are not limited to,
habitat choice, host searching strategy, oviposition
strategy, method for coping with physiological
defenses of host, and developmental synchrony.
There is recent evidence from large scale, long term
rearings of Tachinidae from Lepidoptera in Costa
Rica that some supposedly generalist tachinid spe-
cies actually comprise a group of specialist cryptic
species (species that are difficult to separate mor-
phologically). Although it is likely true that cryptic
species are more common in the Tachinidae than
previously thought and these species may have
narrow host ranges, there are still many tachinid
species that are clearly generalists. Most generalists
have fewer than 20 recorded hosts, but some have
over 50 and a very few have over 100. The hosts of
many tachinid species are either unknown or
poorly known and are not completely known for
the vast majority of species.
Tachinid flies and other parasitoids exert
selection pressures on their hosts to evolve ways
in which to minimize parasitism. The more obvi-
ous may involve the evolution of cryptic color-
ation, specialized feeding strategies such as
concealed feeding or feeding at night, or evasive
maneuvers that are evoked when a host is
attacked. Less obvious, but quite important at the
community level, are the effects of tachinid para-
sitism on host and host-plant interactions (i.e.,
tritrophic interactions). Insect herbivores do not
always feed preferentially on plant species that
provide the highest nutrition. Certain insect her-
bivores will feed on less preferred host plants if
such feeding reduces their level of mortality due
to parasitism. The investigation of enemy-free
space as an important component of tritrophic
interactions is an active area of research.
3686
T Tachiniscidae
Biological Control
Potential insect pests are kept largely in check by
their natural enemies in their native habitats, but
the spread of agriculture and the introduction of
insects into new areas has resulted in a steady
increase in the number of economically important
insect pests attacking crops and forests. Control
measures continue to be largely chemical-based,
but the benefits of biological control or integrated
pest control (control by chemical, biological and
other means) have long been recognized. By the
early 1900s there was an increasing realization that
some insects unwittingly transported to new
places by sea vessels were causing considerable
damage in their new locations. An early example
concerns the gypsy moth (Lymantria dispar) and
browntail moth (Euproctis chrysorrhoea), two for-
est pests introduced into eastern North America
from Europe prior to 1900. In one of the earliest
cases of a classical biological control program, sev-
eral tachinid parasitoids of these pests were
imported into eastern USA from Europe in huge
numbers in the early 1900s. Although the program
was not a complete success, it laid the groundwork
for future studies of tachinids as biological control
agents. In recent years, one of the tachinid species
introduced against those forest pests, Compsilura
concinnata, has been implicated in the decline of
giant silk moths (Saturniidae) in northeastern
United States.
Some of the best known success stories of
tachinid biological control programs have been
reviewed many times. They include: the release of
Cyzenis albicans from Europe against the winter
moth (Operophtera brumata) in Canada; release of
Lixophaga diatraeae from Cuba and elsewhere and
Lydella minense from Brazil against sugarcane
borers (Diatraea spp.) in the Caribbean; release of
Bessa remota from Malaysia against the coconut
moth (Levuana iridescens) in Fiji; and release of
Ceromasia sphenophori from Papua New Guinea
against the New Guinea sugarcane weevil (Rhab­
doscelus obscurus). More recently, Ormia depleta
from Brazil has been implicated in the control of
pest mole crickets (Scapteriscus spp.) in Florida,
USA. Similarly, several species of Trichopoda from
the southern United States and South America
have been introduced recently into Hawaii,
­Australia, Italy (accidentally), South Africa, and
other places for control of the southern green stink
bug (Nezara viridula), with mixed results.
Some tachinid species have been successfully
mass-produced for biological control programs
whereas others have proved difficult or expensive
to rear under laboratory conditions. The in vitro
propagation of tachinids on artificial diets has
been achieved for a very few species in laboratory
experiments but has yet to be employed in a bio-
logical control program.
 Flies
 Natural Enemies Important in Biological
Control
References
Belshaw R (1994) Life history characteristics of Tachinidae
(Diptera) and their effect on polyphagy. In: Hawkins BA,
Sheehan W (eds) Parasitoid community ecology. Oxford,
Oxford University Press, pp 145–162
Grenier S (1988) Applied biological control with tachinid flies
(Diptera, Tachinidae): a review. Anz Schadlingskd Pfl
61:49–56
O’Hara JE (2007) World genera of the Tachinidae (Diptera)
and their regional occurrence. Version 3. 71 pp. http://
www.nadsdiptera.org/Tach/Genera/Gentach ver3.pdf
Stireman JO, O’Hara JE, Wood DM (2006) Tachinidae:
evolution, behavior, and ecology. Annu Rev Entomol
51:525–555
Tschorsnig H-P, Richter VA (1998). Family Tachinidae. In:
Papp L, Darvas B (eds) Contributions to a manual of
Palaearctic Diptera (with special reference to flies of
economic importance). Higher Brachycera, vol. 3.
Science Herald, Budapest, Hungary, pp 691–827
Wood DM (1987) Tachinidae. In: McAlpine JF, Peterson BV,
Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds)
Manual of Nearctic Diptera, vol. 2. Agriculture Canada
Monograph 28: i–vi, 675–1332, pp 1193–1269
Tachiniscidae
A family of flies (order Diptera).
 Flies
 Taiga Tick, Ixodes persulcatus Schulze (Acari: Ixodida: Ixodidae)
Taenidium (pl., Taenidia)
Cuticular ridges that strengthen and support the
walls of the trachae.
Taeniopterygidae
A family of stoneflies (order Plecoptera). They
sometimes are called winter stoneflies.
 Stoneflies
Tagma (pl., Tagmata)
One of the major body regions. In insects, this is
the head, thorax and abdomen. In many other
arthropods it is the cephalothorax and abdomen.
Taiga Tick, Ixodes persulcatus
Schulze (Acari: Ixodida: Ixodidae)
Igor UsUpensky
The Hebrew University of Jerusalem, Jerusalem,
Israel
This is one of the most well-studied species among
hard ticks. Intensive study of Ixodes persulcatus was
initiated in the late 1930s when this tick was found
to be the main vector and reservoir of a virus caus-
ing a severe human disease, tick-borne encephalitis
(Russian spring-summer encephalitis, Far Eastern
encephalitis), that occurs throughout the range of
the tick. Two other viruses responsible for human
pathogenicity were isolated from the taiga tick:
Powassan virus in the southern Russian Far East,
and Kemerovo virus in Western Siberia and the
European part of Russia. Later, I. persulcatus was
found to be the main vector of Lyme borrelioses,
caused by Borrelia garinii and B. afzelii, over the
entire range of the tick. Recently, I. persulcatus was
found to be a vector of a number of agents of
human and animal diseases: babesiosis (Babesia
microti), human monocytic ehrlichiosis (Ehrlichia
T 3687
muris) and human granulocytic anaplasmosis
(Anaplasma phagocytophilum). Also, two new
agents were isolated from I. persulcatus in Siberia:
Bartonella henselae responsible for cat-scratch dis-
ease, and a new rickettsia of unclear pathogenicity
(Rickettsia tarasevichiae). This tick plays some role
in mechanical or biological transmission and
maintenance of agents of some other human dis-
eases (salmonellosis, tularemia, Omsk hemorrhagic
fever, Q-fever). Transovarial and/or transstadial
passage of many pathogens has been proved. Thus,
this tick is one of the most important vectors and
reservoirs of human pathogens from various
groups. Mixed infections in the same populations
of ticks, as well as in the same individuals, were
documented. A double infection of humans was
recorded, and this event may dramatically change
the clinical course of human illness.
The range of I. persulcatus covers a huge terri-
tory of boreal coniferous (taiga) forests, from the
Baltic Sea to the Pacific Ocean, extending as a large
strip through Estonia, Latvia and the entire ­Russian
Federation. In the west, the tick range includes
the eastern parts of Lithuania and some spots in
Finland, Poland, Belorussia and in Ukrainian and
Hungarian parts of the Carpathians. In the east,
the range includes the northern part of Mongolia,
the northwestern and northeastern parts of China,
North and partly South Korea, as well as a part of
Hokkaido Island and several smaller nearby
islands in Japan. In the south, there are findings of
the taiga tick in limited areas of Kazakhstan,
Uzbekistan and Kyrgyzstan. The spread of I. per­
sulcatus to the north of its reproductive range is
limited by low temperature, and to the south by
low humidity. The single findings of the tick to the
north of its reproductive range are explained by its
introduction by birds during spring migrations
from their overwintering areas to the breeding
sites. Thus, cases of tick findings on humans and
animals even within the Arctic Circle have been
documented. The routes of bird migrations are
influenced by various geomorphological forma-
tions including the valleys of large rivers. Evolu-
tionarily, the taiga tick is one of the youngest
3688
T Taiga Tick, Ixodes persulcatus Schulze (Acari: Ixodida: Ixodidae)

representatives of the closely related species in the

subgenus Ixodes that are united in the I. persulca­
tus group or I. ricinus complex, but its range is the
largest one among all ticks of this group.
As is the case with most species of ticks living
in the temperate zone, I. persulcatus has a well-
defined seasonality. The unfed ticks search for
hosts (questing or host seeking) during the spring-
summer season of the year. They use a so-called
“ambush strategy” for seeking hosts: unfed ticks
are positioned on the vegetation, from the litter
layer to the tips of stems or branches, scanning
nearby spaces with their chemoreceptors (part of
Haller’s organs, located on the dorsal surface of
tarsus I). They spend from several hours to several
days in questing position (Fig.  7) depending on
particular environmental conditions. Adult ticks
sense the host stimuli from a distance of 5 to 10 m.
They can also detect paths of regular host migra-
tion, which explains their high concentration
nearby. Questing ticks either catch onto a passing
host or, sensing it from a distance, move in its
direction. Ticks cannot constantly be in a questing Taiga Tick, Ixodes persulcatus Schulze (Acari:
position because their water reserves would Ixodida: Ixodidae), Figure 7  Unfed adult female of
become depleted. To maintain their water balance, the taiga tick on foliage, seeking a host (after B. I.
ticks must regularly migrate down to the litter and Pomerantsev and G. V. Serdyukova 1947).
soil where the ­temperature is lower and humidity
higher. During the day, unfed adults have two t­ emperatures. The taiga tick has no eyes, though it
peaks of activity: in the morning (8–10 a.m.) and can distinguish between more or less illuminated
in the late afternoon (after 4 p.m.). Nymphal activ- areas, preferring the latter. Photosensitive cells
ity is maximal at dusk and the beginning of the were found approximately in the same area where
night. Cloudy weather, rain or warm nights may eyes might be, and their response to light is no
significantly change this pattern. However, if a less pronounced than in some species of ticks
host appears close to an unfed tick, it may be having eyes.
attacked at any time. The season of adult activity lasts for
The capacity of I. persulcatus for active migra- 3–6 months, from the time of snow melt (April–
tion is limited. The questing larvae usually can May) until July-September, depending on the
move up to 20 cm, nymphs up to 40–50 cm, and ­conditions of a particular region. The season of
adults up to 1.0 m. The height of vertical movement activity for unfed subadults (larvae and nymphs)
is directly correlated with the air humidity. Ticks principally corresponds to that for adult ticks,
also are unable to carry out long horizontal migra- though it may be longer. The activity period does
tions: mean 5 m (up to 10 m) for adults and 0.5 m not correspond to the life span of individual ticks.
(up to 1.5  m) for larvae. The rate of adult move- After hatching or molting, unfed subadults live
ment may be as high as 30  cm/min at 23°C but about 14–15 months and unfed adults live about
generally is lower, decreasing with decreasing 12 months, including post-molting development
 Taiga Tick, Ixodes persulcatus Schulze (Acari: Ixodida: Ixodidae)
and behavioral diapause during hibernation, when
ticks do not seek hosts. The life of active (host-
seeking) ticks is much shorter, from 1 day to about
75  days for unfed adults. The unfed ticks do not
become active immediately after post-molting
development or diapause but gradually, during the
main part of the activity season. Most adults
become active during the first 15–30 days of the
season. The adults that become active earlier in the
season live longer than ticks that become active
later. The abundance of active adults sharply
increases during the first third of the season (often
during a shorter period) and then gradually
diminishes until the end of the season. Unfed ticks
that do not find a host and cannot feed during the
activity period die due to complete expenditure of
their nutritional reserves.
The taiga tick is a typical exophilic three-host
tick. Each parasitic stage feeds on a vertebrate host
only once: the larva feeds for 3–5 days, the nymph
for 3–6 days and an adult female for 6–10 days. The
duration of feeding strongly depends on the host
species. Males feed several times during their active
life for 15–30 min each time, and even these brief
periods are sufficient for infection of hosts with
viruses. The obligatory condition for normal female
engorgement is its insemination. The female I. per­
sulcatus can be inseminated not only on a host, but
also in nature before finding a host. In some popu-
lations, about 50% of unfed females collected from
vegetation are inseminated. The larvae and nymphs
increase their weight during feeding 15- to 30-fold,
while engorged females are heavier than unfed
females 100- to 150-fold. The mass of an unfed
larva is 0.03–0.045 mg, whereas the mass of fully
engorged females reaches 250–470 mg. Females lay
from 2,000 to 4,000 eggs. The minimal weight of
engorgement, after which females are capable of
laying single eggs, is about 20–35 mg. The heavier
the engorged female becomes, the greater the ratio
of the number of laid eggs/mg of the female’s
weight, until the female weight reaches 140–200 mg,
after which the dependence of egg number/mg of
engorged female becomes linear and equals
approximately 8.5–9.5 eggs/mg of the female
T 3689
weight. Values of all these parameters differ for tick
populations from different parts of the range of
I. persulcatus.
The engorged ticks drop off the host into the
litter where they develop before molting, or where
the females oviposit and the eggs develop. The
engorged subadults feeding in the late summer
have no time to undergo the necessary metamor-
phosis by the autumn; they enter the morphoge-
netic diapause and molt into the next stage only in
the second part of the summer of the following
year. The possibility of nymphal diapause during
2  years is rather questionable and needs further
study. The molted unfed individuals hibernate,
being in behavioral diapause, and become active
next season. Only eggs and engorged adults can-
not hibernate. The general duration of the entire
life cycle (from eggs to eggs) may fluctuate from
2  years under most favorable conditions (the
southern part of the Russian Far East) to 5 years.
In most cases, the tick populations consist of ticks
of different cohorts (having life cycles of different
durations). These two factors make I. persulcatus a
unique reservoir for pathogenic agents.
The taiga tick is one of the most opportunis-
tic (generalist) tick species, using as hosts nearly
300 species of different vertebrates (about 100
species of mammals, more than 175 species of
birds and a few species of reptiles). Larvae princi-
pally feed on small mammals (rodents and insec-
tivores), nymphs on medium-sized mammals
(rodents, lagomorphs, some carnivores) and birds,
and adults on large mammals. The questing height
of ticks of each stage coincides with the size and
location of their main hosts. In years of depres-
sion of the abundance of small mammals, or
under specific environmental conditions, sub-
adults may change their hosts for larger ones or
for hosts less typical for them under normal con-
ditions. Adults actively attack people and are the
main source of human infection by different
pathogens; nymphal attacks toward humans have
been recorded extremely rarely. Ixodes persulcatus
adults are more aggressive than adults of the clos-
est relative, the sheep tick I. ricinus. Their efficient
3690
T Tally Threshold
attachment to the host body is enhanced by a long
hypostome covered with numerous recurved
teeth, preventing tick removal.
A number of parasites and predators of the
taiga tick are known. However, the prospects of
their use for tick control are rather slim. The taiga
tick is a member of some rather complicated forest
communities formed long ago, and there is little
chance of destroying a well developed balance of
such communities by introducing new agents. The
high stability of adult tick abundance from year to
year (the difference is not more than one order of
magnitude) indicates the extreme fitness of this
species. This stability is provided for by a number
of factors, such as a complicated life cycle, exis-
tence of different types of diapause, numerous
hosts from various groups, and a high level of
aggressiveness of adults toward potential hosts.
The simplest mode of human protection from
taiga tick attacks and bites is proper clothing when
in forested areas, and regular self- and cross-
inspections followed by tick removal. A wide-scale
educational program (lectures, leaflets, articles in
newspapers, etc.) just before and during the sea-
son of tick activity may increase public awareness
of tick attacks and personal motivation for self-
protection. There are data on the protective effect
of some repellents which can be used on clothing
or applied directly to the skin to reduce tick infes-
tation. Large-scale treatment of tick-populated
forest areas by persistent acaricides, which were
used in the 1950s to 1970s, is now banned. The
only target for treatment with non-persistent aca-
ricides might be the popular sites of human relax-
ation during the summer months.
 Ticks
References
Filippova NA (ed) (1985) The taiga tick, Ixodes persulcatus
Schulze (Acarina, Ixodidae). Nauka, Leningrad, 416 pp
(in Russian)
Goodman JL, Dennis DT, Sonenshine DE (eds) (2005) Tick-
borne diseases of humans. American Society for Micro-
biology, Washington, DC, 402 pp
Korenberg EI (2000) Seasonal population dynamics of Ixodes
ticks and tick-borne encephalitis virus. Exp Appl Acarol
24:665–681
Uspensky I (1993) Ability of successful attack in two species
of ixodid ticks (Acari: Ixodidae) as a manifestation of
their aggressiveness. Exp Appl Acarol 17:673–683
Uspensky I (1995) Physiological age of ixodid ticks: aspects of
its determination and application. J Med Entomol
32:651–664
Uspensky I (1996) Tick-borne encephalitis prevention
through vector control in Russia: an historical review.
Rev Med Vet Entomol 84:679–689
Uspensky I, Ioffe-Uspensky I (1999) The relationship between
engorged female weight and egg number in ixodid ticks:
a biological interpretation of linear regression parame-
ters. Acarologia 40:9–17
Uspensky I, Garuto RM, Goldfarb L (2003) The taiga tick
Ixodes persulcatus (Acari: Ixodidae) in the Sakha Repub-
lic (Yakutia): distributional and reproductive ranges.
J Med Entomol 40:119–122
Tally Threshold
In binomial sampling, the number of individuals
required to be present per sample unit to consider
the sample unit infested. Proper selection of the
tally threshold can improve the accuracy of clas-
sification sampling.
 Sampling Arthropods
Tanaostigmatidae
A family of wasps (order Hymenoptera).
 Wasps, Ants, Bees, and Sawflies
Tandem Running
A from of communication among some ants,
wherein ants trail one another, with each ant main-
taining contact with the preceding individual by
means of its antennae.
Tangle-Veined Flies
Members of the family Nemestrinidae (order
Diptera).
 Flies
 Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)
Tanning
The process of sclerotization (hardening) of the
cuticle after an insect molts; tanning involves the
cross-linking of proteins, aided by quinones. Dark-
ening may accompany tanning. Transparent cuti-
cle can be tanned (hardened), as occurs over the
compound eye, though in the absence of
darkening.
Tanoceridae
A family of grasshoppers (order Orthoptera). They
commonly are known as desert longhorned
grasshoppers.
 Grasshoppers, Katydids and Crickets
Tanyderidae
A family of flies (order Diptera). They commonly
are known as primitive crane flies.
 Flies
Tanypezid Flies
Members of the family Tanypezidae (order
Diptera).
 Flies
Tanypezidae
A family of flies (order Diptera). They commonly
are known as tanypezid flies.
 Flies
Tanzaniophasmatidae
A family of gladiators (order Manto­phas­
matodea).
 Gladiators (Mantophasmatodea)
T 3691
Tarnished Plant Bug, Lygus
lineolaris Palisot De Beauvois
(Hemiptera: Miridae)
N. J. Bostanian
Agriculture and Agri-Food Canada, Horticultural
Research and Development Center, St. Jean-sur-
Richelieu, QC, Canada
The tarnished plant bug, Lygus lineolaris (Pal-
isot de Beauvois) is a widely distributed mirid,
known from Alaska to southern Mexico. It is a
pest of a wide range of seed, vegetable, fruit,
fiber and ­forage crops. More than 600 different
plant ­species have been reported as potential
hosts for this insect. Its ability to cause eco-
nomic losses is often related to the migratory
behavior of the adult and the phenology of the
host plant. Depending on the host plant spe-
cies, feeding may cause any of the following
injuries: ­malformation of fruit, abnormal
growth habits, necrosis, abscission of fruiting
structures, or production of shriveled or embry-
oless seeds.
Life Stages
Egg
A freshly laid egg is translucent. Later it is
­yellowish. It is oval and slightly curved on one
side. One end is obtuse and broadly rounded,
whereas the other end is almost squarely trun-
cated. The hardened egg shell (chorium) is
smooth. Each is 0.85–1.6  mm long and
0.22–0.28 mm wide.
Nymphs
The five instars (Fig.  8) are very similar in form
and all are yellowish-green. They walk rapidly and
drop readily when disturbed.
3692
T Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)

Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae), Figure 8  Tarnished
plant bug, Lygus lineolaris: upper left, eggs; upper right, third-instar nymph. Note the black spot of
the abdominal gland; second row left, fifth-instar nymph. Note the four black spots on the ­thorax.
The wing pads are ­yellowish with irregularly marked brown lines and extend to the fifth and sixth
­abdominal segments; second row right, the adult, dark brownish; lower left, a berry injured by
­tarnished plant bug nymphs. Note the closeness of the achenes where the bug has fed; lower right,
a pear injured by tarnished plant bug. Note the “pit.”

First Instar Second Instar

The yellowish-green body has a pale orange spot
in the middle of the caudal margin of the third
abdominal segment. The body length is
0.85–1.10  mm and the body width is around
0.40  mm. The width of the head at the eyes is
0.34–0.36 mm.
The body is yellowish to yellowish pea-green. The
third abdominal segment exhibits a bright orange-
yellow spot with a slightly smaller spot at the pos-
terior margin. The body length is 1.30–1.65 mm
and the body width is about 0.60 mm. The width
of the head at the eyes is 0.45–0.52 mm.
 Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)
Third Instar
The body is green. The abdominal gland is
­indicated by a black spot. Toward the end of this
stage, four dark thoracic spots begin to appear.
Wing pads also appear and extend on to the
second abdominal segment. The body length is
1.7–2.2  mm and the body width is about
1  mm. The width of the head at the eyes is
0.58–0.60 mm.
Fourth Instar
A great variation of color exists and green, red,
white and black predominate. The four black
thoracic spots are more prominent. The caudal
margin of the third abdominal segment bears a
large black spot. Two prominent reddish bands
appear on each femur. The wing pads extend to
the third abdominal segment. The body length
is 2.1–2.7  mm and the body width is about
1.5  mm. The width of the head at the eyes is
0.78–0.80 mm.
Fifth Instar
The color is variable, but greenish in general. The
yellowish head has five longitudinal brownish
stripes converging behind, but not attaining, the
posterior margin of the vertex. The thorax and
wing pads are yellowish with irregularly marked
brown lines. The abdomen is yellowish or green-
ish yellow. The wing pads extend onto the fifth or
sixth abdominal segment. The veins begin to
appear in the pads. Four black spots are con­
spicuous on the thorax. The dorsal abdominal
gland is indicated by a conspicuous black spot
on  the caudal margin of the third abdominal
­segment. The legs are variable in color. The body
length is 3.2–4.2 mm and the body width is about
2  mm. The width of the head at the eyes is
0.94–0.96 mm.
T 3693
Adult
The color is variable, usually greenish or brownish,
with reddish brown markings on the wings. The
thorax has five longitudinal dark stripes. The scutel-
lum has two medium and two lateral black or red-
dish lines. Eleven segments comprise the abdomen,
although some of these are considerably modified.
The first ventral segment is reduced to an elastic
membrane that joins the abdomen to the thorax. In
the female, the seventh segment is named the sub-
genital plate, as it extends posteriorly in the mid-
ventral region to cover the base of the ovipositor.
The body length is 4.9–5.7  mm for males and
5.2–6.0  mm for females. The body width is
2.4–2.8 mm for males and 2.4–3.0 mm for females.
Moreover, around the base of the ovipositor on the
ventral surface of the abdomen, there is usually a
dark brown patch that may extend to the thorax.
Life Cycle
Tarnished plant bugs overwinter as diapausing
adults either beneath plant litter or duff ground
cover, or between the leaves of plants and long dry
grasses. In piled leaves and rubbish, winter sur-
vival is about 29%, whereas in orchard sod it is
only 6%. Overwintering adults start emerging in
mid-April at temperatures as low as 8°C. These
adults feed first on the opening buds of trees such
as apple, peach and shrubs. A little later they
migrate to early appearing annual plants. The
favorite spring food plants include black current
(Ribes nigrum L.), wild currents (Ribes spp.), com-
mon mullein (Verbascum thapsus L.), sheep sorrel
(Rumex acetosella L.), yellow rocket (Barbarea
­vulgaris R.Br.), and strawberries (Fragaria spp.)
(Table 2).
Overwintering adults gradually disperse on
these spring plants as the temperature increases
and then migrate to other favorable emerging
weeds or cultivated plants. The bugs usually feed
on the sap of growing tips or the reproductive
parts of a plant, such as the buds of flowers, or the
3694
T Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)

Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae), Table 2  Annotated list of
crop plants attacked by the tarnished plant bug
Forest trees (nurseries)
Bare-root pine and container Conifers Douglas-fir Larch
nurseries
Fruit trees
Apple Cherry Prune Grape
Peach Pear Pecan Plum
Quince      
Small fruits
Blackberry Currant Grape Raspberry
Strawberry
Commercially Grown Flowers
Aster Bachelor‘s button Bleeding heart Calendula
Carnation Chrysanthemum Cosmos Dahlia
Garden balsam Geranium Gladiolus Golden glow
Hollyhock Impatiens Iris Marigold
Nasturtium Peony Poppy Rose
Sage Salvia Shasta daisy Snapdragon
Stock Strawflower Sunflower Sweet pea
Verbena Zinnia    
Garden crops
Asparagus Beet Broccoli Cabbage
Carrot Celery Cucumber Eggplant
Endive Escarole Horseradish Lettuce
Lima beans Mustard Onion Pea
Pepper Potato Radish Snap beans
Spinach Squash Swiss chard Tomato
Turnip      
Forage crops
Alfalfa Birdsfoot trefoil Clover Soybeans
Other crops
Oilseed rape Tobacco Sunflower Sweet corn
Seed heads of wheat and other grasses

rapidly growing meristematic tissue of such plants growth stage. There is a seasonal succession of
as asparagus, alfalfa and other forage crops. hosts as the bugs feed on different plants from
Tarnished plant bugs generally migrate to a spring to fall (Table 3). Nymphs can disperse long
host only when the plant enters its reproductive distances (15–20 m) within a short time and adults
 Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)
T 3695

Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae), Table 3  Annotated list of
weeds attacked by the tarnished plant bug
Spring
Annual fleabane Erigeron annuus (L.) Pers.
Common mullein Verbascum thapsus L.
Common ragweed Ambrosia artemisiifolia L.
Garden sorrel Rumex acetosa L.
Wild strawberries Fragaria spp.
Yellow rocket Barbarea vulgaris R. Br.
Summer
Black mustard Brassica nigra (L.) Koch
Boneset Eupatorium perfoliatum L.
Brown knapweed Centaurea jacea L.
Lamb‘s-quarters Chenopodium album L.
Narrow-leaved hawk‘s beard Crepis tectorum L.
Ox-eye daisy Chrysanthemum leucanthemum L.
Pineappleweed Matricaria matricarioides (Less.)
Redroot pigweed Amaranthus retroflexus L.
Shepherd‘s-purse Capsella bursa-pastoris (L.)
St. John‘s-wort Hypericum perforatum L.
Tansy Tanacetum vulgare L.
White mustard Sinapsis alla L.
White sweet-clover Melilotus alba Desr.
Yellow sweet-clover Melilotus officinalis (L.) Lam.
Wild carrot Daucus carota L.
Wild mustard Sinapsis arvensis L.
Autumn
Canada fleabane Erigeron canadensis L. (=Conyza canadensis (L.) Crong)
Canada goldenrod Solidago canadensis L.
Canada thistle Cirsium arvense (L.) Scop.
Common ragweed Ambrosia artemisiifolia L.
European stinging nettle Urtica dioica L. subsp. Dioica
False ragweed Iva xanthifolia Nutt.
Narrow-leaved goldenrod Solidago graminifolia (L.) Salisb.
Red-stemmed aster Aster puniceus L.
Rough goldenrod Solidago rugosa Mill.
Tall white aster Aster simplex Willd.
3696
T Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)
can travel at least 5.1 km in sustained flight. Most
adults fly no higher than 1  m from the ground,
although some adults have been collected at eleva-
tions as high as 1,500 m. Multiple matings occur,
but a single mating is sufficient for a female to lay
viable eggs throughout her entire life. In Canada,
overwintering females oviposit from the first week
of May to the third week of June (about 50 days).
Optimal oviposition occurs between 21°C and
27°C and oviposition does not take place below
16°C. Eggs can sustain low temperatures of 10°C
for 15 days without adverse effect. Eggs are embed-
ded in the stem, in the petioles, or in the midribs of
leaves. They may be deposited singly or sometimes
in groups of two or three in close proximity.
Following eclosion, the nymphs feed immedi-
ately on the succulent parts of the host plant and
molt five times. The choice of the host plant dictates
significantly the duration of each stage. Laboratory
studies, with the temperature fluctuating irregularly
between 17°C and 30°C, showed that female lon-
gevity ranged from 31 to 68  days, whereas male
­longevity ranged from 19 to 41  days. In southern
Quebec, Canada, adults of the first generation
appear about mid-June and reach maximum abun-
dance around mid-July. During this time, adults
migrate in great numbers from early season hosts,
e.g., June bearing strawberries toward other host
plants such as the following: raspberry (Rubus spp.),
garden beans (Phaseolus vulgaris L.), potato (Sola­
num tuberosum L.), pepper (Capsicum annuum L.),
turnip (Brassica napus L.), sugar beet (Beta vulgaris L.),
red clover (Trifolium pratense L.), celery (Apium
graveolens L.), wild mustard (Sinapsis arvensis L.),
brown knapweed (Centaura jacea L.), and lamb’s-
quarters (Chenopodium album L.). This list is by no
means complete. Eggs laid by summer adults pro-
duce adults 20–25 days later. For a given area, the
seasonal sequential presence of tarnished plant
bugs on wild plant hosts is practically the same year
after year. The first generation adults mate when
they are 4–6  days old. The pre-oviposition period
varies between 9 and 13 days, with individual ranges
from 5 to 29 days. The fecundity may reach up to
140 eggs per female with an average oviposition of
0–3.4 eggs per female per day. The population
dynamics of the second generation nymphs is a
function of the immigration time of the adults, the
oviposition period of each individual and the nutri-
tive quality of the different host plants. With the
season progressing, more and more overlapping
occurs between the developmental stages and the
different generations of the tarnished plant bug. The
overlap results in a smooth exponential growth pat-
tern as opposed to a stepwise pattern. From the end
of July to the second week of September, all stages
of the bug can generally be found in the field. First
generation adults that emerge in mid-June oviposit
on several hosts and lead to a continuous emer-
gence of second generation summer adults from
the beginning to the end of August. A third genera-
tion of nymphs could occur on some cultivated
hosts such as alfalfa and asparagus, and on wild
plants such as common ragweed (Ambrosia
artemisiifolia L.), Canada goldenrod (Solidago
canadensis L.), rough goldenrod (Solidago rugosa
Mill.), tall white aster (Aster simplex Willd.), sting-
ing nettle (Urtica dioica L.), Canada fleabane
(Erigeron canadensis L.), and the red-stemmed aster
(Aster puniceus L.). In the fall, 25–30 days are needed
for the tarnished plant bug to complete its life cycle.
In southeastern Canada there are two generations
per season whereas in the cotton belt in the south-
ern USA, there are four to seven generations. Past
the second generation, it is difficult to distinguish
the generations. For example, on lamb’s quarters
characterized by continuous germination, second
and third generation adults and larvae are found on
the same plant. Therefore, the extended vegetative
and flowering period of this weed contributes to the
build-up of tarnished plant bugs in adjacent fields.
Despite some variations, the sex ratio is 1:1
irrespective of the host plant. The bugs are mainly
phytophagous; however, they can sometimes feed
as facultative predators on soft-bodied arthropods
such as aphids and mites, or as scavengers on dead
nymphs and adults of their own species.
As fall progresses, the testes and ovaries atrophy
and the adults enter diapause. Exposure of nymphs
of the first four stages (the photosensitive stages) to
 Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)
photoperiods of 12.5 h or less induces diapause in
the adult stage. Rearing these nymphs to a photope-
riod of 13.5 h or more will prevent the adults to enter
diapause. Continuous light prevents diapause in
young adults and terminates diapause in diapausing
adults. Fifth-instar nymphs and adults are not sensi-
tive to diapause-inducing photoperiods.
Attractants
There is now some evidence that virgin female tar-
nished plant bugs release an attractant to males.
However, the attractant has not yet been isolated
and identified. The presence of an aggregation
pheromone that attracts both sexes also has been
suggested. In any case, there are still no practical
applications for these findings.
Pest Host Relationships
In southeastern Canada and northeastern United
States, adults are subject to late fall temperatures
that induce the tarnished plant bug to hibernate
until the following spring. Management practices to
control this bug in fields must consider plant hosts
as reservoirs for the build-up of adults and nymphs
in the vicinity of cultivated fields. Any flowering
plant seems to attract the tarnished plant bug. Nev-
ertheless, there are a few exceptions such as dande-
lions, sowthistle, milkweed and dogbane, which are
all sap latex-type plants. Goldenrod is one of the
rare latex-type sap plants which is very attractive in
the fall to field populations of this bug.
Plant hosts range from highly attractive to
highly resistant to the tarnished plant bug. Resis-
tance to Lygus has been reported in some cultivars
of celery, alfalfa, cotton, beans and carrots. Some
plants do not attract the bug at all. For example,
outbreaks have never been reported on wheat, rye
and turf grass.
Although the tarnished plant bug is able to
develop on a wide range of hosts, field observations
show that some plants consistently support much
T 3697
higher populations than others. Management on
selected hosts at particular growth stages over a
short time, e.g., before the nymphs become adults,
may result in lowering bug populations in crop
agro-ecosystems. Sites with ephemeral, lush growth
that dries out quickly provide a release of tarnished
plant bugs and are of immediate concern during
the cropping season. In uncultivated fields, weeds
growing in sequence that are acceptable to tarnished
plant bug development will retain their bug popula-
tions throughout the year without any activity of
dispersion toward the surrounding crop lands, as
long as the site is not disturbed or dried up.
Natural Enemies
Presently, it seems that natural enemies (Table  4),
other than a few species of insect parasitoids, are not
capable of checking a L. lineolaris population once it
begins to build up. Endemic populations of L. lineo­
laris are under tremendous environmental pressure
that checks their populations. In such instances, nat-
ural enemies play an important role. We do not yet
have quantitative analyses of the intricate relation-
ships between prey (L. lineolaris) and their natural
enemies. In addition to parasitic Diptera and
Hymenoptera, an identified species of nematode has
been reported to rarely parasitize L. lineolaris adults
in Quebec. Several predators are known to attack L.
lineolaris, including damsel bugs (Orius spp.,
Anthocoridae), leaffooted bugs (Coreidae), stink
bugs (Pentatomidae), lacewings (Chrysopidae), soli-
tary wasps (Sphecidae), robberflies (Asilidae), lady
beetle larvae (Cocinellidae), and spiders (Oxyopi-
dae, Tetragnathidae and Thomisidae).
Damage
In southeastern Canada and northern United
States, overwintering adults are pests of fruits such
as apple, peach and pear. The adults injure the buds
causing a circular depression referred to as “pit” in
apples and pears (Fig.  8). In peaches, the fruit
3698
T Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae)

Tarnished Plant Bug, Lygus lineolaris Palisot De Beauvois (Hemiptera: Miridae), Table 4  Known
­parasitoids of Lygus bugs
Parasitoid name Family Target Comments
Indigenous species
Polynema pratensiphagum Mymaridae Egg 72% Lygus mortality in Quebec
Walley
Anaphes iole Girault Mymaridae Egg  
Anaphes ovijentanus Crosby Mymaridae Egg 50–85% Lygus mortality widespread
Leonard
Erythmelus miridiphagus Mymaridae Egg  
Dozier
Telenomus spp. Scelionidae Egg  
Peristenus pallipes (Curtis) Braconidae Larvae adults First generation May–June; second
generation Aug.–Sept. combined
15–20% Lygus mortality in Quebec;
38% in Ontario and 22% in Saskatch-
ewan-Alberta
Alophora opaca (Coquillett) Tachinidae Adults 7% Lygus mortality in Quebec
Alophorella sp. Tachinidae Adults 0.8% Lygus mortality in Ontario
Imported species
Peristenus stygicus Loan (USA, Braconidae Larvae Diapausing race from France and a
Sask., Alta.) nondiapausing race from Turkey;
polyvoltine
Peristenus rubricollis Braconidae Larvae From Poland; univoltine
(Thomson) (USA)
Peristenus digoneutis Loan Braconidae Larvae From France (potato, alfalfa rye
fields) released in alfalfa field in New
Jersey 1979–1988; 36% parasitism of
first generation and 29% parasitism
of second generation; released in
seed alfalfa, Saskatchewan, and
strawberries, Quebec, in 1991, 1992;
Currently, descendents from the New
Jersey releases are collected at
St. Clothilde Qc. It is bivoltine; popu-
lation at maximum abundance about
same time as Lygus populations;
attacks early stage nymphs of Lygus.

appears as if it has been gouged when small and
the injury is called “cat facing.” Furthermore, a cer-
tain percentage of fruit drop occurs following
Lygus attack. The nymphs that will comprise the
first generation attack strawberries causing mal-
formed berries where the achenes are very close to
each other and straw-colored. ­Similar to peaches,
the injury is called “cat facing.” Several vegetables
such as celery, tomato, eggplant and pepper are also
attacked by first generation adults and second gen-
eration nymphs and adults, causing flower abscis-
sion, which reduces yield in some years. In celery,
early injuries to the stalk are of no ­economic con-
sequence. However, near harvest, injury to petioles
 Taro Caterpillar or Rice Cutworm, Spodoptera litura (Fabricius)
and necrosis of leaflets leads to secondary infec-
tions by bacteria. The damage is called black joint.
It is serious and causes unacceptable economic
losses. Though cotton is not its preferred host, the
tarnished plant bug is a serious pest of cotton.
Migration occurs when the wild hosts have dried
along cotton fields. Following the completion of
the second generation, the bugs enter the cotton
fields and damage all fruiting forms of cotton. Early
to mid-June pinhead squares (immature flower
buds) are attacked and turn yellowish, dry up and
eventually drop off the plant. In addition to feeding
on pinhead squares, tarnished plant bugs also feed
on terminal shoots. This activity results in several
physiological changes caused by the toxins injected
into the meristematic tissue of the plant terminal.
The tall, fruitless plant is characterized by short-
ened internodes, swollen nodes and excessive lat-
eral branches. This condition is often referred to as
“crazy cotton.” Later, damage to larger squares
shows up as darkened anthers in white blooms
resulting in poor pollination and deformed bolls.
These are called “dirty blooms.” Eventually, the tar-
nished plant bugs even attack the bolls causing
small, dark, sunken spots on the outside of the boll
and brownish discoloration inside the boll.
 Small Fruit Pests and their Management
 Vegetable Pests and their Management
References
Bostanian NJ (1994) The tarnished plant bug and strawberry
production. Technical Bulletin 1994-1E. Agriculture
and Agri-Food Canada, St. Jean-sur-Richelieu, Canada
Day WH (1987) Biological control efforts against Lygus and
Anthocoris spp. infesting alfalfa, in the United States,
with notes on other associated mirid species. In:
Hedlund RC, Graham HM (eds) Economic importance
and biological control of Lygus and Adelphocoris
in  North America. U.S. Department of Agriculture,
Washington, DC, ARS-64, pp 20–39
Tingey WM, Pillemer EA (1977) Lygus bugs: crop resistance
and physiological nature of feeding injury. Bull Entomol
Soc Am 23:277–287
Young OP (1986) Host plants of the tarnished plant bug,
Lygus lineolaris (Heteroptera: Miridae). Ann Entomol
Soc Am 79:747–762
T 3699
Taro Caterpillar or Rice Cutworm,
Spodoptera litura (Fabricius)
John L. Capinera
University of Florida, Gainesville, FL, USA
This insect occurs in Asia, Australia, and Oceania.
There are reports that it invaded many locations
outside its natural range and was eradicated, but it is
not certain that such eradications involved this spe-
cies. A very similar but allopatric insect, Spodoptera
littoralis (Boisduval) (cotton cutworm), is found in
Africa, Madagascar, Europe and the Middle East.
For many years these two species were thought to
be the same, and although they have been consid-
ered to be separate species by most authorities since
1962, confusion lingers. Other common names
applied to S. litura include rice cutworm, tobacco
budworm and common cutworm.
Life History
The number of generations displayed by this spe-
cies depends on temperature. A generation can be
completed in less than a month, and 12 genera-
tions have been reported annually in India, though
8–10 generations is more common in the wet trop-
ics. Development ceases when temperatures are
less than about 8°C, and the upper limit for devel-
opment is about 37°C.
Eggs are spherical, somewhat flattened, and
measure about 0.4–0.6 mm in diameter. They are
deposited in clusters of 200–300 eggs, in fairly reg-
ular rows comprising three layers, and covered
with whitish scales from the abdomen of the
female moth. The eggs are orange or pink initially,
but turn black before hatching. Eggs persist for
2–3 days in the summer, but considerably longer
under cooler conditions, up to 25  days. Females
have been shown to produce 2,000–2,500 eggs.
Larvae initially are blackish green with black
heads. The older larvae are more variable, often
appearing gray, brown or almost black and with
dark markings. The latter instars bear triangular
3700
T Tarsal Claw
spots laterally on each body segment, and a yellow
dorsal stripe. They attain a length of 40–50  mm.
Young larvae feed in groups, but as they mature
they become more solitary. However, at high den-
sities they may disperse in large groups from field
to field. Normally there are six instars. Larvae are
inactive during the day, with the older instars seek-
ing shelter in the soil but the younger larvae
remaining motionless on the foliage. Larval devel-
opment may require only 12–18  days under hot
conditions.
Larvae burrow into the soil to a depth of
3–5  cm in preparation for pupation. Pupae are
dark red to reddish brown, and are found in cells
buried in the soil. The pupae are 15–22  mm in
length, and the last segment bears two hooks. Pupal
development time is only 7–10 days under warm
conditions, but requires up to 30  days under
cool conditions.
The appearance of adults are typical of
Spodoptera moths, with the forewings bearing gray,
brown, yellow and white markings, and the hind
wings whitish with a brown or gray margin and
dark veins. The wing span is about 30–38 mm. It is
nearly identical to the yellowstriped armyworm,
S. ornithogalli (Guenée), of North America. Adults
are active at dusk and during the evening. They mate
immediately upon emergence and can begin to
deposit eggs within 2 days of mating, though some-
times several days elapse before egg deposition. The
adults are short-lived, rarely surviving 7 days under
warm conditions, though persisting for 3  weeks
under cool conditions. Sex pheromones are pro-
duced and have been identified for use in traps.
Damage
This is one of the most serious crop pests in the
Asian tropics. It is highly polyphagous, feeding on
numerous vegetables, herbs, flowers, and field
crops including soybean, cotton, maize, sunflower,
rice, and grasses. Plants are often entirely defoli-
ated, and bolls or flower buds can be eaten. Young
plants may be severed at the soil surface.
Management
This species is often heavily parasitized by wasps
and tachinid flies. Both eggs and larvae are affected.
Numerous diseases also are known. However, man-
agement generally depends on use of chemical
insecticides. Insecticide resistance is an increasing
problem, however. In India, integrated manage-
ment is promoted using trap crops (sunflower and
castor plants) around crop fields, clean cultivation,
prediction of egg laying by using pheromone traps
for capture of moths, and application of neem
and nuclear polyhedrosis virus for suppression of
­larvae. Resistance has been identified in some
­varieties of peanuts.
References
CABI and EPPO (1997) Spodoptera littoralis and Spodoptera
litura. In: Quarantine pests for Europe, 2nd edn.
CABI International, Wallingford, United Kingdom,
pp 518–525
Etman AAM, Hooper GH (1979) Developmental and repro-
ductive biology of Spodoptera litura (F.) (Lepidoptera:
Noctuidae). J Aust Entomol Soc 18:363–372
Rao GVR, Wightman JA, Rao DVR (1989) Threshold tem-
peratures and thermal requirements for the develop-
ment of Spodoptera litura (Lepidoptera: Noctuidae).
Environ Entomol 18:548–551
Rao GVR, Wightman JA, Rao DVR (1993) World review of
the natural enemies and diseases of Spodoptera litura
(Lepidoptera: Noctuidae). Insect Sci Appl 14:273–284
Tarsal Claw
The claws at the tip of the tarsus.
 Legs of Hexapods
Tarsomeres
The major subdivisions of the tarsus (the foot), the
distal segment of which is called the pretarsus, and
bears claws and sometimes a pad or arolium.
 Legs of Hexapods

Tarsus (pl., Tarsi)
The jointed portion of the insect leg distal to the
tibia, consisting of tarsomeres and often bearing
claws on the distal segment (pretarsus). The “foot”
of an insect (Fig. 9).
 Legs of Hexapods
Taste and Contact
Chemoreception
Reg Chapman
University of Arizona, Tucson, AZ, USA
The sense of taste provides animals with the ability
to identify potential food by the perception of cer-
tain nutrients, and also to detect potentially toxic
materials. Insects are no exception, but unlike
most other animals their taste receptors are not
restricted to the region around the mouth and
they may be able to recognize oviposition cues,
and, occasionally, intraspecific signals as well as
food. In addition, whereas in vertebrates the taste
receptors are stimulated by chemicals in solution,
3 4
1 2
Tarsus
Tarsus (pl., Tarsi), Figure 9  Leg of a beetle (Coleoptera: Scarabaeidae) leg showing its component parts,
and a close-up of one type of beetle tarsus (foot).
Taste and Contact Chemoreception
T 3701
insects have the capacity to perceive chemicals on
dry surfaces. For this reason, it is referred to as
“gustation” or “contact chemoreception” rather
than “taste.”
Insect contact chemoreceptors are usually in
the form of hairs, or conical projections from the
cuticle, with a pore at the tip. The pore permits
chemicals to pass through the cuticle to the sense
cells beneath. Each hair, or cone, contains the sen-
sitive endings (dendrites) of (commonly) four
sensory cells, and each of these responds to a dif-
ferent range of chemicals. The ranges of chemicals
reflect the habits of the insect and also the position
and specific function of a particular hair.
Very little is known about why an insect
chemosensory cell responds to one, or some
chemicals and not to others, but it is probable that,
as in other animals, this is determined by receptor
molecules in the cell membrane of the dendrite
just inside the pore in the cuticle. A taste receptor
cell may have only one type of receptor molecule,
in which case, its response is limited to one, or a
few, structurally similar chemicals that interact
with the receptor. Other cells have more than one
type of receptor molecule, and so have the ­capacity
2
Hidden true
segment 3
4
Coxa 5
trochanter
Femur
Tibia
5
Pretarsus
3702
T Taste and Contact Chemoreception
to respond to a range of structurally different
chemicals. Some cells that are presumed to have
these different characteristics are described below.
The interaction of the appropriate chemical
with a receptor molecule leads to changes in the
electrical potential across the cell membrane and
an electrical signal is sent along the axon that con-
nects each sensory cell to the central nervous sys-
tem. Connections within the central nervous
system determine whether the insect responds
positively or negatively to the stimulating chemi-
cal, that is, whether it accepts or rejects food, or an
oviposition site. In practice, how the insect
responds nearly always depends on the integra-
tion of signals from a number of receptors.
Contact chemoreceptors are found primarily
on the mouthparts, the labrum, maxillae, labium,
and hypopharynx, and they may be especially
abundant on the maxillary and labial palps when
these are present. A small number are present on
the epipharynx (the inside surface of the labrum)
just outside the mouth in all insects that have been
investigated. Many insects also have contact
chemoreceptors on the tarsi, and on the antennae,
although most of the chemoreceptors on the
antennae are olfactory receptors. Females of some
Orthoptera, Diptera, Hymenoptera and Lepi-
doptera have contact chemoreceptors on their ovi-
positor, but this is not a general characteristic of
females even within a group.
The numbers of contact chemoreceptors asso-
ciated with the mouthparts is very large in cock-
roaches, grasshoppers and related insects. An adult
of the migratory locust, Locusta migratoria, for
example, has about 3,000 contact chemoreceptors
on the mouthparts. In these insects, additional
receptors are produced at each molt. By contrast,
much smaller numbers are present in sucking
bugs. Aphids have no contact chemoreceptors on
the exposed parts of the proboscis, but they have a
few on the epipharynx. As a result, aphids must
draw fluid into the cibarial cavity before they are
able to taste it. This is not true of all sucking bugs,
however, many of which have contact chemore-
ceptors on the tip of the labium, which is the first
mouthpart structure to contact the food prior to
feeding. Holometabolous insects also generally
have few mouthpart contact chemoreceptors,
especially in larvae. Caterpillars have only 16–20
contact chemoreceptors and this number does not
change throughout development. In grasshoppers,
species with more restricted diets tend to have
smaller numbers of contact chemoreceptors on
the mouthparts than polyphagous species. Among
caterpillars, however, this is not true. The numbers
are similar irrespective of feeding habit.
Feeding
The primary function of contact chemorecep-
tors on the mouthparts is the selection of food.
Once the insect bites into food, some receptors
become immersed in the juices released from
the food and so function very much like taste
receptors in vertebrates by detecting compounds
in solution. However, the receptors on the maxil-
lary and labial palps often come into contact
with food before the insect bites. They can detect
compounds on the dry surface of a leaf, for
example. In grasshoppers, crickets and cock-
roaches, the palps are vibrated rapidly so that the
contact chemoreceptors at their tips are brought
into a rapid series of brief contacts with the sur-
face. As many as 15 contacts per second may be
made, and each period of contact probably lasts
less than 20 ms. This behavior, known as palpa-
tion, probably serves two functions. It allows the
insect to receive a more sustained flow of infor-
mation from the receptors than would be possi-
ble if contact were maintained because the
receptors become adapted (as our taste receptors
do after the first mouthful of a sweet drink), and
it also allows the insect to sample a larger surface
area than if the palps remained stationary. The
information provided by palpation before an
insect starts to feed enables it to make feeding
decisions more rapidly and also, perhaps, to
avoid the possible intake of noxious compounds
if the food contains toxins.

Insects, like other animals, can taste the major
nutrients essential for their development, survival
and reproduction: sugars (as a source of energy),
amino acids (the building blocks for protein), and
inorganic salts and water. There is no direct evi-
dence that insects are able to taste proteins. The
specific chemicals to which an insect’s taste re­­
ceptors respond, however, vary with the feeding
behavior of the insect. It is common for one of the
sense cells in a contact chemoreceptor to be sensi-
tive to some sugars, and another to be sensitive to
some amino acids. Some insects have also been
shown to possess a “water cell,” that is, a cell that
responds to water and very dilute salt solutions,
and it is possible that this type of cell is of wide-
spread occurrence. All insects appear to have a
cell responding to inorganic salts, but this cell
exhibits increased activity as the salt concentration
increases (unlike the “water cell” whose activity
declines with increased salt concentration), and it
is probably a cell that inhibits further feeding,
ensuring that the insect does not ingest excessive
amounts of salt. The other nutrients such as ste-
rols, fatty acids and vitamins appear to be acquired
as a result of their widespread occurrence in the
insect’s food and do not require specific taste
receptors.
A cell responding to sugars does not necessar-
ily respond to all sugars, nor does an amino acid-
sensitive cell respond to all amino acids. In the
woolly bear caterpillar of the moth, Grammia
geneura, for example, a sugar-sensitive cell in one
hair only responds to the fruit sugar, fructose. This
cell probably has only one type of receptor mole-
cule that only reacts with fructose. However, a cell
in another hair close by responds to sucrose and
glucose although not to fructose. This cell probably
also has a single type of receptor molecule that
reacts with both sucrose and glucose because of
similarities in their molecular structure. In the
same way, cells in different hairs may respond to
different ranges of amino acids. This probably
allows an insect to detect food of different qualities.
Even so, not all different types of sugar or amino
acids are tasted by any one insect even though
Taste and Contact Chemoreception
T 3703
some of them are essential for its development. It
obtains a balanced diet mainly because a food with
some nutrients, which it can taste, will generally
contain most of the others, which it cannot taste.
In addition to nerve cells that respond to nutri-
ent compounds, many plant-feeding insects possess
sensory cells that respond to plant secondary com-
pounds. These compounds, alkaloids, terpenoids,
and many others, are produced by plants outside
the normal primary metabolic pathways (hence
“secondary”) and are important in the plant’s ecol-
ogy. Many of them inhibit feeding by herbivorous
animals, including insects, and the human interpre-
tation is that they taste “bitter.” Sometimes they are
also toxic. In a majority of plant-feeding insects,
stimulation of a cell by these secondary compounds
inhibits, or deters feeding, and the cells are usually
called “deterrent cells.” A deterrent cell usually
responds to several different secondary compounds,
but by no means all the different types. This almost
certainly reflects that fact that it has several differ-
ent types of receptor molecules.
Because all plants contain secondary com-
pounds, whether or not an insect feeds on a par-
ticular plant and the amount it eats is dependent
on the balance between information received from
taste cells signaling the presence of nutrients, and
deterrent cells signaling the presence of secondary
compounds. However, in some insect species that
feed only on particular plant species or groups of
plants, characterized by a specific chemical, it is
common for the deterrent cells to have lost any
sensitivity to that chemical so the plant is no lon-
ger “distasteful.” Correspondingly, some now have
a sensory cell that responds only to that compound
or class of compounds and which indicates “accept-
ability” rather than “distastefulness” to the insect.
The best-known example of this is the response to
glucosinolates. These are sulfur-containing com-
pounds characteristic of the cabbage family. For
most plant-feeding insect species, these com-
pounds stimulate deterrent cells and inhibit feed-
ing, but in many species that feed habitually on
plants in the cabbage family, the deterrent cells are
not affected. Instead, another sensory cell responds
3704
T Taste and Contact Chemoreception
to the glucosinolates, indicating acceptability so
that the insects are stimulated to feed or oviposit.
In species that feed on vertebrate blood, the
contact chemoreceptors have a sense cell that
responds to adenine nucleotides such as ATP and
ADP. These compounds are released when the
insect probes into the host’s blood vessels and
damages blood cells. They provide the insect with
an unequivocal signal that appropriate food is
available.
Not only the chemoreceptors on the mouth-
parts are involved in feeding decisions, however.
This is most obvious in fluid feeding insects like
flies and bees, where extension of the proboscis,
which is necessary before the insect can feed, is
induced if chemoreceptors on the tarsi are stimu-
lated with sucrose. In the tsetse fly, Glossina fusci­
pes, similar receptors respond to some of the
common components of human sweat, such as
uric acid and the amino acids leucine and valine.
Stimulation with these compounds causes the
insect to probe with its proboscis and is presum-
ably part of the normal host recognition process.
Tarsal receptors are also involved in host recogni-
tion by plant-feeding insects.
Oviposition
It is common for contact chemoreceptors to be
involved in oviposition, although attraction to the
oviposition site often depends on the sense of
smell. Contact chemoreception in this context has
been most thoroughly investigated in some flies
such as the cabbage fly, Delia radicum. The tarsal
receptors on this fly respond to glucosinolates on
the leaf surface of the host plant. Other insects,
like the imported cabbage butterfly, Pieris brassi­
cae, and the cabbage looper, Trichoplusia ni, that
lay their eggs on cabbage plants also have tarsal
receptors responding to glucosinolates. Contact
with these compounds induces the insects to lay
eggs. A number of butterflies drum on the leaf sur-
face with their fore tarsi when selecting a leaf for
oviposition. This appears to be a process analogous
to palpation, bringing the contact chemoreceptors
on the tarsi into a series of brief contacts with the
leaf surface. There is no evidence that the leaf sur-
face is broken by these activities, so the insect does
perceive chemicals on the surface, not from within
the plant.
Although contact chemoreceptors do occur
on the ovipositors of some insects, there is not yet
clear evidence of their roles in oviposition.
Pheromone Detection
Contact chemoreceptors are sometimes impor-
tant in the perception of pheromones involved in
sexual recognition, prevention of oviposition, and
trail following. In the tsetse flies, Glossina species,
the male recognizes a female by touching her with
contact chemoreceptors on his fore tarsi. This
contact also enables him to determine whether or
not she has mated through the perception of spe-
cific molecules in the wax on the surface of the
female’s cuticle. Changes in the proportions of
some components occur at the time of mating
because wax from the male contaminates the
female, and the male is able to detect the differ-
ence with his tarsal receptors. A similar process
occurs in Drosophila fruit flies, except that in this
case, the female wax alters as a result of changes in
synthesis in the female following mating. Females
of the German cockroach, Blattella germanica,
also have sex specific compounds in their cuticu-
lar wax which function as a sex recognition pher-
omone. At the start of courtship, the male touches
the female with his antennae, presumably detect-
ing the compounds with contact chemoreceptors
on the antennae.
Contact chemoreceptors are used by the
adults of some flies to detect oviposition deterrent
pheromones laid down by previously ovipositing
females to reduce the likelihood of competition
with their larvae. This is known to be the case in
adults of the apple maggot fly, Rhagoletis pomo­
nella, and the cabbage butterfly. The cabbage seed
weevil, Ceutorhynchus assimilis, however, detects

its oviposition deterrent pheromone with contact
chemoreceptors on the club of the antenna.
Although contact chemoreceptors are common
on insects’ antennae, this is one of the few instances
where their function is known. Many insects are
known to make rapid vibrations of the antennae
when they encounter a potential food or prey
item. This process is known as antennation, and it
is probably analogous to palpation with the insect
bringing contact chemoreceptors at the tip of the
antenna into brief contacts with the substrate.
Parasitic Hymenoptera, for example, are com-
monly seen doing this when they encounter a
potential host.
Tent caterpillars follow chemical trails depos-
ited by conspecifics. The trails are detected by con-
tact chemoreceptors on their maxillary palps.
It is almost certain that there are many situa-
tions in which insects use contact chemoreceptors
on their antennae or tarsi for the perception of
intraspecific signals.
 Ultrastructure of Insect Sensilla
References
Chapman RF (1995) Chemosensory regulation of feeding. In:
Chapman RF, de Boer G (eds) Regulatory mechanisms
in insect feeding. Chapman and Hall, New York,
101–136 pp
Glendinning JI, Chaudhuri N, Kinnamon SC (2000) Taste
transduction and molecular biology. In: Finger TE,
­Silver WL, Restrepo D (eds) The neurobiology of taste
and smell. Wiley-Liss, New York, 315–351 pp
Taxis (pl., Taxes)
A directional movement in response to an envi-
ronmental stimulus, directed toward or away
from a stimulus. A movement toward the stimu-
lus is considered to be a positive taxis, a move-
ment away is a negative taxis. Types of taxes
include anemotaxis, astrotaxis, chemotaxis,
­geotaxis, hygrotaxis, phonotaxis, phototaxis, rhe-
otaxis, and thermotaxis.
Teaching and Training Entomology: Institutional Models
T 3705
Taxon (pl., Taxa)
A group of organisms, populations or taxonomic
groups considered to be sufficiently different
from other groups to be treated as a unique group
from the perspective of classification or taxon-
omy. For example, a species is a taxon when it is
compared to another species; likewise, higher
level groups such as families and orders can be
referred to as taxa.
 Classification
Taxonomy
The principles and procedures according to which
species are named and assigned to taxonomic
groups.
 Classification
Teaching and Training
Entomology: Institutional Models
Carl S. Barfield, Marilyn E. Swisher
University of Florida, Gainesville, FL, USA
Research on insects, whether to understand basic
biology or to provide management strategies,
most often occurs within thef context of an insti-
tutional paradigm. Precisely the same is true for
teaching/training programs and extension. The
structure of an organization in which research-
ers, trainers or extension specialists work is cru-
cial to understanding the goals, motivations and
successes of those human resources. Understand-
ing the institutional framework within which
programs are developed and delivered is there-
fore an important consideration when evaluating
program effectiveness.
There are five principal models of institutional
and procedural frameworks within which research,
teaching and/or extension programs associated
with entomology occur. Three are fairly widely
used and two have the potential to become global.
3706
T Teaching and Training Entomology: Institutional Models
The very framework chosen within which to pursue
entomology may well affect the types and quality of
information developed. Evaluating the effectiveness
of entomo­logical programs cannot be complete
without recognizing the institutions within which
such programs are developed and reside.
The degree to which entomological programs
developed under one paradigm can function suc-
cessfully when transferred to another is therefore
an important and an intriguing issue, but one that
has been virtually ignored on a global basis. Each
of the five major models currently used has advo-
cates and critics, and each has relative strengths
and weaknesses. However, discussion of program
strengths and weaknesses most often fails to con-
sider the institutional context in which they have
developed historically, and thus fails to provide a
comprehensive analysis of when, how and why
these programs succeed or fail.
The Land Grant System: USA
During Abraham Lincoln’s presidency, the
United  States Congress was moved to provide
legislation directly aimed at assisting farmers.
This made both practical and political sense, as
some 65% of the U.S. population was involved
in agriculture in one way or another. Under
Lincoln’s guidance, the United States Department
of Agriculture was established in 1861. Then, four
successive Federal Acts (Morrill Land Grant Act,
Hatch Act, second Morrill Act and Smith-Lever
Act), dating from 1862 to 1914, set aside lands for
agricultural research and put the infrastructure
and human resources in place to conduct that
research. The second Morrill Act (1890) set aside
a second set of lands and infrastructure for the
development of what are often termed Histori-
cally Black Colleges and Universities (HBCUs),
and the Smith-Lever Act (1914) created the
­Federal Extension System.
The Land-Grant system is based on the
­concept of combining teaching, research, and
extension within a single institution, and it took
about 50 years to establish all three functions. All
50 states and U.S. protectorates and territories
employ the system. America has led the world in
agricultural production since the Land Grant
­system was established.
Proponents of the Land-Grant model point
to the productivity of American agriculture and
the associated research infrastructure. Indeed,
due in part to the Federal and state investment in
this institutional model, the USA is today the
world’s leading producer of food with only about
1.8% of the population involved in food produc-
tion. The USA grants more graduate degrees in
the agriculture-related disciplines than any other
nation, and more international students seeking
advanced degrees in agriculture choose to study
in the United States than anywhere else. Including
extension in the model indicates the importance
of a forward and backward link between farmers
and researchers. Finally, this model ensures that
advances in agricultural technology to find their
way into the classroom very quickly, ensuring that
future generations of agricultural professionals
and farmers are able to apply the new technolo-
gies (Fig. 10).
Not everyone agrees that this model is ideal.
Critics of the Land-Grant model point out several
weaknesses in the system:
Research
Extension Teaching
(outreach) (degree programs)
Farmers
Teaching and Training Entomology: Institutional
Models, Figure 10  Basic structure and flow of
information in a Land-Grant Institution as
originally conceived.

1. Over the years, extra-mural grants have supplanted
Federal and state direct support for agricultural
research and extension. Grants programs are fickle
and trendy. Land-grant institutions have a long
history of “following” extra mural priorities (inte-
grated pest management in the 70s, sustainable
agriculture in the 80s, and genetic engineering
now). The wholesale commitment to these types
of trends by significant percentages of land-grant
scientists is indicative of how susceptible this
model is to abrupt shifts in priorities in the quest
to acquire funds and publish. Research is driven
more by granting agency priorities than by farmer
needs.
2. Due in part to the emphasis on extra-mural fund-
ing, Land-Grant institutions tend to recruit faculty
with ever-narrowing expertise so they can com-
pete successfully for grants. As a result, the system
lacks scientists who have either the skills or the
incentives to integrate knowledge across disci-
plines. Individuals who are capable of critically
analyzing the potential impacts of new technolo-
gies in a broader social, economic and ecological
framework are rare.
3. The departmental and college management struc-
ture of Land-Grant institutions is, in many ways,
the antithesis of the type of holistic program struc-
ture needed to resolve real problems. University
units are rewarded for their individual productiv-
ity, not for their collective cooperation. While uni-
versities constantly discuss the need for
inter-disciplinary approaches, their very structure
often prevents them from implementing effective
cross-disciplinary solutions.
4. The ability of the USA to capitalize on the high
productivity of Green Revolution agriculture is as
much attributable to good fortune as to agricul-
tural research, and it is likely not sustainable. Green
Revolution agriculture depends on high levels of
off-farm inputs that make successful farmers more
dependent on a few transnational corporations
that supply seed, fertilizers, equipment, and chemi-
cals while also increasing the farmers’ debt. Other
farmers simply cannot obtain these inputs. There
appears to be an internal conflict of priorities in
Teaching and Training Entomology: Institutional Models
T 3707
the Land-Grant Model. One priority is to feed the
masses at any cost. The other is to keep small farm-
ers in business for the social good.
5. Teaching in Land-Grant institutions often is the
single least rewarded activity. Reward and profes-
sional advancement depend largely on the amount
of grant dollars obtained and the number of pub-
lications produced. Relevance to real farm prob-
lems may not rank high among the factors taken
into consideration for faculty promotion.
6. Extension often does not work as it was conceptu-
alized. The fundamental idea was for extension to
serve as the voice of the farmers and to vocalize
the research needs seen by farmers as priorities.
That extension voice would then explain those pri-
orities to university researchers who, using their
research expertise, would investigate the issues,
develop solutions and have the extension voice
deliver those solutions back to the farmers. In real-
ity, researchers are driven by grant priorities, rather
than extension-relayed farmer needs.
7. Finally, critics point out that the USA has moved
from an original farm policy designed to keep
farmers on the farm and farming profitable, to a
“cheap food” policy designed to feed urban popu-
lations who, by and large, elect Federal officials.
The Land-Grant infrastructure evolved to pay lit-
tle attention to the promotion of agricultural pro-
cedures that would make farming sustainable and
conserve natural resources.
While the debate continues, the sheer volume of
output from Land-Grant programs is impressive.
In the USA, the Land-Grant system encompasses a
wide range of farming enterprises. Large scale, cor-
porate farming often becomes a source of informa-
tion for Land-Grant scientists as corporations have
the capital to invest in staff and research on their
crops and pests that tax-based Land-Grant institu-
tions do not. Small farmers often cannot afford to
adopt the technologies proposed by Land-Grant
scientists and tend to utilize a mix of modern
­science and traditional farming practices.
The system has not gained acceptance out-
side the U.S. and, in fact, has really not ever been
3708
T Teaching and Training Entomology: Institutional Models
r­ eplicated elsewhere, although components of the
system have been implemented in other places.
This model depends greatly on a collaborative
relationship among peers for its success. Peer
review, for example, is a major factor in evaluating
the quality of teaching, research and extension.
Similarly, funding for the system involves Federal,
state and local support, and farmers must be
empowered to ensure that their problems and pri-
orities are imposed on the entire structure. All of
these characteristics are typical of the social and
political structure in the United States. The poor
“transportability” of the U.S. system, especially to
non-European based cultures and to nations
where democracy is not the norm, may be due, in
large part, to the absence of an appropriate social,
cultural and political context for the system. The
Land-Grant model may be culturally insensitive,
but not necessarily wrong. Agricultural produc-
tivity appears to be like every other increasingly
globalized activity: one cannot compete if one
doesn’t play the top-level game. This, of course, is
not highly acceptable to politically sensitive peo-
ple who want to maintain local culture and merely
improve agricultural productivity. Global compe-
tition likely will demand local cultural changes in
the way farmers and governments spend their
time and money.
Training and Visit (T&V): World
Bank
T&V is a child of the World Bank, and this model
was conceptualized and first utilized in Asia in the
1970s. This hierarchical system began in India,
Turkey, Burma, Nepal, Sri Lanka and Thailand,
and today exists in more than 40 nations. The basic
premise of the T&V system is that much more
information and technologies exist than are used
by farmers, and the principal reason for this is
the  ineffectiveness of extension delivery systems.
T&V thus places major emphasis on training and
­outreach. Research is most often limited to site-­
specific adaptive research of existing technologies.
While more recent T&V programs have tended
to  re-emphasize the research component, the
approach continues to focus heavily on outreach.
T&V is a top-down approach. A subject mat-
ter specialist trains a limited number of regional
extension agents who, in turn, provide training
to local extension agents who, in turn, train farm-
ers. This approach emphasizes the timeliness of
actions, and the progress of agricultural produc-
tivity at the farm and regional levels is “tracked” by
the training process. For example, training on
improved seedbed preparation will be delivered
just before the time when seedbed preparation is
to occur. Frequent, regular reporting from the bot-
tom up is a key feature of the T&V model. The
Land-Grant system has “field days” and “demon-
stration plots” where farmers can come to witness
innovations. While not hierarchical in nature, as is
T&V, the idea is somewhat the same.
Proponents of T&V argue that the system is
ideal because it focuses on those human resources
that are native to indigenous cultures, provides a
“filter” to take existing technology and adapt it to
local conditions, and it is both relevant and timely.
T&V takes complete advantage of cultural and
social hierarchies already in place. The fact that
T&V is currently utilized in over 40 nations, so say
the proponents, is indicative of its relevance. Sim-
ply put, it works.
Critics of T&V point to several short­
comings:
1. Methods are geared to the top, best-educated, most
articulate facilitators (regional extension person-
nel). Most T&V programs end up with a paltry
number of highly capable facilitators. The meth-
ods that are emphasized both confuse and leave
behind the other participants in the system. One
result is that the less capable extension agents train
their local agents poorly, and the farmers who rely
on them, in essence, receive poor advice.
2. In the same vein, T&V historically has not sanc-
tioned facilitators for not attending all training
sessions. One result is poorly equipped facilitators,
and the problem progresses down the hierarchy.

3. This approach, in many ways, “force fits” the T&V
timetable into an often-unreceptive farmer sched-
ule resulting in poor adoption of advice.
4. T&V programs historically are narrow in perspec-
tive and not linked to broader, yet relevant, issues
of great concern to farmers. Timely seedbed tech-
nology is useless if not linked to socially relevant
local schedules and to lending periods and priori-
ties of local banks.
5. T&V programs were developed for irrigated sys-
tems where water was controlled and never
attempted to develop procedures exportable to
rain fed agriculture.
6. Many analyses have shown T&V approaches to be
overly costly and non-sustainable.
T&V differs from the Land-Grant system in its
almost sole focus on a hierarchical extension-
training approach. An interesting note is that vir-
tually all the countries where T&V is employed are
in World Bank-funded efforts in Asia. T&V does
not appear to have been widely adopted elsewhere.
However, the essence of T&V sometimes is prac-
ticed in other countries like Jamaica despite no
formal funding of projects actually called T&V.
Once again, cultural and social factors may
play an important role in determining how well
this system “travels” from its Asian heartland to
other parts of the world. The very hierarchical
model that assumes that knowledge flows “down-
ward” from more educated and knowledgeable
experts to practitioners (farmers) would not, for
example, be very acceptable to many farmers in
the United States or perhaps in most societies
where egalitarian norms are strong.
Farming Systems: United States
Agency for International
Development
The farming systems model originated from pro-
grams in Latin America and, over the last two
decades, has been promoted by a variety of interna-
tional development agencies. The single largest
Teaching and Training Entomology: Institutional Models
T 3709
advocate of this model in the 1980s was the United
States Agency for International Development
(USAID). Many of the CGIAR centers (notably CIP,
CIMMYT and IITA) also have used this model.
The farming systems model differs widely
from T&V in that farming systems primarily
emphasizes research, not extension. Underlying
the farming systems model is the assumption
that most existing technology has not been
adapted to specific regional or local conditions.
Farmers are, therefore, unable to adopt and uti-
lize what would be useful methods. The major
emphasis of farming systems is on site-specific,
adaptive research. While there is episodic inven-
tion of “new technology,” the major emphasis
focuses on local tests of existing technologies.
Proponents of this model argue that there are
major differences between the farming systems
model and the Land-Grant model. In practice,
those differences are often hard to discern. Both
models depend on strong linkages between
research and extension and are difficult to imple-
ment in places where the two functions are not
housed in the same institution. Further, many
advocates of the Land-Grant system argue that
both models emphasize features such as on-farm
research, site-specific testing and multidisci-
plinary research teams. There is, in practice, one
major difference between the two models. The
farming systems model emphasizes research
much more than extension, and farming systems
projects that demonstrate mass dissemination of
information are rare.
A basic tenet of the farming systems model is
that many global farmers have been by-passed by
the Green Revolution. Their land holdings or their
economies were too poor to take advantage of
high-yielding agriculture and its associated inputs.
Thus, the advocates say the most relevant approach
is the use of a multidisciplinary “rapid rural
appraisal” team to ask farmers’ opinions, followed
by research aimed at tailoring existing technology
to individual farmers’ fields (Figs. 11 and 12).
Critics of the farming systems model point to
a number of constraints on its effectiveness:
3710
T Teaching and Training Entomology: Institutional Models
Teaching and Training Entomology: Institutional
Models, Figure 11  Farming systems training effort
in The Gambia, West Africa.
Teaching and Training Entomology: Institutional
Models, Figure 12  Farming systems project to
teach proper goat-dipping techniques for tick
control in Kenya. Slide provided by Dr. Sandra Russo,
International Programs, University of Florida.
1. The disciplinary make-up of the initial rapid rural
appraisal team can severely bias what the team
determines is pertinent research.
2. Farming systems teams have often been unable to
define their tasks and, consequently, served only to
“spread the gospel” of farming systems rather than
to provide holistic solutions for real problems.
Farming systems failed in Africa for precisely this
reason.
3. Many farming systems projects to date have
focused on crop variety and/or fertilizer trials – the
very things that these farmers supposedly could
not afford, thus giving rise to the farming systems
model in the first place.
4. To date, adherents of the farming systems model
have been primarily economists, anthropologists
and a few agronomists. The broad spectrum of
agricultural disciplines apparently has not b ought
into the basic premise of farming systems.
5. It is an expensive system, relying on a highly
trained and educated body of researchers becom-
ing very familiar with local conditions, problems
and farmers. The central role of the multi-disci-
plinary team, along with the emphasis on the site-
specificity of knowledge, means that any institution
using this approach must make a relatively large
investment in the local farming systems team and
cannot spread the effect of that investment across
a very large geographic area. Not surprisingly, like
T&V, most places using the farming systems model
also have been the recipients of funding from the
principal donor advocating the model.
The basic argument for the origination of the
farming system model would seem pertinent, and
the approach has been tried in a number of loca-
tions with mixed results. Like the Land-Grant
model, which it resembles in many other aspects,
the farming systems model depends on mutual
respect among peers and between agricultural
professionals and farmers. In societies where there
are strong biases against effective communication
between individuals of differing social, economic
or cultural status, the all-important communica-
tion between researcher and farmer is likely to fail.
Again, the success of this system may well depend
on the social and cultural context in which it exists,
and its distinct lack of success in some parts of
the world may reflect cultural and social realities
rather than simply the ineffectiveness of the sys-
tem itself in solving farmers’ problems.
Interestingly, the World Bank funded both
T&V and Farming Systems projects in Africa.
T&V came first as an extension effort and was fol-
lowed by farming systems as a research effort
(Malawi, Tanzania, Ethiopia). World Bank saw

these two models as complementary. Yet, African
successes at solving real problems in a cost effec-
tive manner are hard to find.
Training-Driven Research:
Indonesian Integrated Pest
Management
This model is relatively new and has not been
implemented in many places. Basically, it has been
developed as part of an Asia-wide integrated pest
management effort funded originally by the Aus-
tralian government and is now managed by the
Global Integrated Pest Management Group within
FAO in Rome, Italy. It offers exciting possibilities
to overcome many of the flaws inherent in the
other three models.
Training-driven research is based on two fun-
damental premises (i) do not conduct research
unless it is needed and (ii) use training as the tool
to identify what research is needed. This model is
like T&V in that it trains personnel who, in turn,
train others and farmers. It is like farming systems
in that it focuses only on “relevant” research, and it
is like the Land-Grant model in that it combines
training, extension and, when needed, research.
Farmers and those who assist and advise them
need to be trained. Thus, experts establish a rigorous,
field-based training program for the farmer support
system, then for the farmers. Beginning with field
preparation, each and every step in the agricultural
production annual cycle is demonstrated to the
trainees, both in the field and on site. Experience of
the trainers, literature and formal knowledge pos-
sessed by the trainers are incorporated into the
training course. As long as the information exists to
proceed in relevant fashion through all the steps of
production (from field preparation, to fertilization,
to pest management, to harvesting, to marketing),
there is no need for research (Fig. 13).
If, at any step, the trainer recognizes that the
information to train appropriately does not exist,
there is a call for “research.” This may take the
form, however, of a demonstration rather than a
Teaching and Training Entomology: Institutional Models
T 3711
Teaching and Training Entomology: Institutional
Models, Figure 13  In-field training for rice
farmers and support staff at a farmer field school,
Indonesia.
full-blown, randomized experiment. In any case,
the product of this research is not a journal article,
but rather feedback provided directly to the train-
ing program. This is an iterative process resulting,
sooner or later, in an ability to appropriately train
farmers and their assistants without conducting
research until a new, unknown situation arises.
This model differs markedly from the Land-
Grant model where funded research is the top
priority. Further, the first priority of Land-Grant
research is not training, but publication and the
volume of such publications produced is ger-
mane to continued employment in the Land-
Grant system. Training-driven research also
offers a paradigm to regiment discipline exper-
tise. Often, Land-Grant multidisciplinary teams
attacking some aspect of agriculture will find,
once the problem is truly understood, they have
the wrong expertise on the team (e.g., hiring a
bacteriologist when a virologist was needed).
Training-driven research avoids this issue by first
identifying the particular need, then seeking the
appropriate expert.
Training-driven research, to date, has not
been attempted in enough places to have many
proponents or critics. One criticism to date focuses
on TDR’s inability to demonstrate any significant
research accomplished after identification of the
3712
T Teaching and Training Entomology: Institutional Models
problem in training. Indonesian rice has been the
principal target to date. As it expands and is
attempted, similar to the first three models, inher-
ent strengths and weakness will be identified.
Farmer Participatory Research:
CGIAR Network
Concerns over the lack of appropriate technology
transfer have given rise to a more recent institu-
tional paradigm. Farmer participatory research
(FPR) has its origins within the CGIAR system
and, from all appearances, has had its greatest
impact to date in Asia. The conceptual foundation
for FPR is a belated appreciation of mainstream
agricultural scientists for the importance of indig-
enous knowledge to agricultural systems man­
agement, especially with resource-poor, marginal
farmers.
Operationally, FPR begins with four funda-
mental steps (i) community-based dialogue with
individuals or small groups used to identify local
changes in agriculture over a generation or two;
(ii) community-based analysis used to identify
high-priority problems that need resolution;
(iii)  community-based inventory of local meth-
ods attempted to solve the key agricultural prob-
lems; and (iv) community-based assessment of
how well methods tried in (iii) have performed.
The purpose of FPR is to initially learn how farm-
ers think and assess agricultural productivity and
damage. Only then can new technology be injected
in a socially and culturally relevant fashion.
A recent FPR project in Viet Nam illustrates
how the approach functions. Vietnamese farmers
were invited to test the heuristic, “We do not need to
spray insecticides in the first 30  days after trans-
planting [rice].” Volunteer rice farmers were invited
to participate, and each reported results based on
individual assessment of perceived damage. Ana-
lytical variables used to determine success or failure
of the project included farmers’ beliefs, intentions,
spray frequencies, timing and targets, yields, inputs
and other management practices (Fig. 14).
Teaching and Training Entomology: Institutional
Models, Figure 14  Viet Nam farmer participatory
training session on evaluation of insecticides
during first 30 days after sowing. Photo provided
by Dr. Kong Luen Heong, International Rice
Research Institute, Los Baños, Philippines.
Such experiments, if managed properly, usu-
ally are inexpensive and easy to conduct, and they
facilitate farmer learning by pragmatically “test-
ing” a new idea. The process provides researchers
the opportunity to learn how farmers think and
perceive success or failure. The FPR approach can
be quite expensive if attempted over large areas.
The presence of well-educated scientists will affect
farmers differentially, and care must be taken to
minimize this influence by including farmers
at  all levels of planning and decision-making.
Reductionist scientists often view FRP as scien-
tifically “weak,” however, those using this approach
must remember that the idea is to evaluate farmer
responses and learn how they perceive success
and failure. The idea is not to conduct well-­
controlled, reductionist experiments. Adoption
rates for new varieties of plants and improved
technology are well-documented in the literature,
however, much less is known about the adoption
or adaptation of information into farmer deci-
sion-making.
Fundamental to FPR is a concerted effort to
train local agriculturists to proceed through the
above four steps so that, after a few iterations, local

farmers and their support network work indepen-
dently of outside influence. Unlike reductionist
science, FPR begins by assuming that indigenous
peoples have usable solutions to many agricultural
problems or they would not have survived. The
effort is to extract those solutions up front and,
by doing so, convince local farmers that they will
not be treated simply as passive recipients of mod-
ern, science-based information. Rather, they will
be partners in the experimentation and delivery
phases of agricultural development. There is grow-
ing evidence that the most effective extension pro-
grams in Land-Grant models also operate this way.
Unfortunately, this is not yet the norm.
FPR is a unique approach and quite different
from station-based research and traditional exten-
sion-delivery systems. It is, in many ways, the
antithesis of the Land-Grant model. Unlike farm-
ing systems, FPR does not have to “adapt” station-
based research because the blend of indigenous
knowledge and modern science is inherent in FPR.
Unlike the T&V approach, there is no hierarchy
involved and no loss of information between tiers.
FPR most closely resembles the training-driven
research model, but has been tried in more places
to date than TDR. There are on-going efforts in
Asia, Africa and Latin America that use FPR as the
paradigm. In Ecuador, small groups of farmers
form committees and decide on a theme they want
to research and then conduct that research under
the guidance of an extension specialist. Colombia,
under the auspices of CIAT, has adopted the same
approach. There is increasing awareness that talk-
ing with farmers is an improvement over talking at
farmers.
Unlike the Land-Grant, T&V and farming
systems models, FPR is a new approach. In
essence, it has been developed out of the percep-
tion that the other models have failed to resolve
real problems with marginal farmers. The concept
of formalized farmer field schools appears unique
to TDR and FPR, although, Land-Grant extension
experts would argue their “turn row conversations”
with farmers serve precisely the same purpose. As
TDR and FPR gain maturity, the global agricultural
Teaching and Training Entomology: Institutional Models
T 3713
community can begin to assess their real impact
and their relative value as compared to the other
three institutional paradigms.
In agricultural societies of relative wealth
where individuals, not social groups, make deci-
sions, and where egalitarian norms prevail, sys-
tems resembling, at least in part, the Land-Grant
system have prevailed. Land holdings and econo-
mies conducive to high-yielding agriculture seem
to be requirements for the success of Land-Grant
style entomological programs, probably because
of the emphasis on the ability of individual farm-
ers to make critical decisions about how they will
manage their resources. The other four models
have both been conceptualized and implemented
with farmer groups who have virtually none of
these characteristics. The latter groups consist of
farmers that are relatively poor, often make group
or community decisions, typically have poor access
to credit and are labor intensive. These models
appear to be more successful in places where cul-
tural norms play a stronger role in determining
acceptance of new practices than in places where
decisions about technological innovation are less
subject to social and political control.
By far, the Land-Grant system is the model
that adheres most rigorously to reductionist exper-
imentation. Large numbers of farmers under the
Land-Grant, T&V, and farming systems approaches
are today still treated as passive recipients of infor-
mation, not as active participants in the identifica-
tion and generation of new information. The
farming systems approach does ask farmers what
they think is important as a way to initiate the
model. Training-driven research and Farmer Par-
ticipatory Research truly involve the farmer and
the associated support system as active partici-
pants in the process. Both these latter paradigms
make use of indigenous knowledge systems and
thus strive to have as end products agricultural
programs that are blends of traditional approaches
and modern science.
All five models (Table  5) have inherent
strengths and weaknesses, but only three have
been attempted to date on a fairly broad scale.
3714
T Teaching and Training Entomology: Institutional Models

Teaching and Training Entomology: Institutional Models, Table 5  Characteristics of five institutional
models of agricultural (including entomology) research, training and extension
Characteristic Land-Grant T&V Farming Training driven Farmer participa-
systems research tory research
Major focus on Yes No Yes No Yes (with an
research altered definition
of research)
Major focus on Yes        
publication
Major focus on Yes Yes No Yes No
extension
Focus on use of No No No Yes Yes
indigenous
knowledge
Major focus on No Yes No Yes Yes
farmer training
Targets users with Yes No No No No
relatively good
resources
Targets marginal No Yes Yes Yes Yes
users
Regiments techni- No No No Yes Yes
cal expertise
Puts farmers in No No No Yes Yes
active role
Combines research, Yes No No Some Inherently
training and
extension
Sufficiently tested No No No No No
outside area(s) of
origin
Area(s) targeted to USA Asia; some Latin America; Asia Asia; some Latin
date Africa; some Africa America; some
some Latin Africa
America

Clearly, the questions asked about insects, the
methods chosen for investigation, the methods
used in training and the consequences of ento-
mological programs can vary markedly from
one model to the next. Recognition of which
model predominates in any effort is fundamen-
tal to success, and global entomologists need to
address, perhaps in a side-by-side comparative
fashion, just how transportable information
developed under one model is to farmers living
under another. This could be one of the reasons
that “technology cannot be simply exported.”
International donor organizations clearly need
to be attentive to matching the institutional
model being promoted with appropriate cul-
tural, social and economic norms.

An Example
How might the use of an exotic biological control
agent in a particular crop be implemented under
each of the five models? For argument, the crop is
soybean and, among its insect pests, is one that
pesticides have failed to control. It is the key pest
and it limits yield annually. The idea is to try a bio-
logical control approach.
Under the Land-Grant Model
Entomologists with biological control expertise,
either individually or in small groups, would survey
the literature for what is known about biological
control of the target pest. Two avenues would be
explored initially: the potential use of indigenous
natural enemies and the importation of exotic ones.
As the indigenous complex was not maintaining
the pest’s population density below acceptable lev-
els, the choice might be made to search for exotic
natural enemies. The USDA/APHIS protocol would
be utilized for permits, and travel likely would be to
China, the indigenous home of the soybean plant. If
the pest has been subjected to biocontrol previously
through the efforts of others and the results were
published, travel to China might not be necessary.
Collections of potential natural enemies would
likely result in the importation of each and every
one found to inflict mortality on the pest in China.
In quarantine, each potential natural enemy would
be checked for hyperparasites, and then reared to
sufficient densities to test any deleterious effects a
release might have. Later, progeny of the imports
would be released and evaluated for effectiveness.
Results would be published in the refereed journal
literature. At this point, extension agents and farm-
ers would best get access to the information if they
had been working in teams of individuals from the
various agencies involved. Otherwise, those respon-
sible for implementation would need to be keenly
aware of the refereed journal literature.
Practical use of the new imported natural
enemy(ies) might demand a mass rearing facility.
Teaching and Training Entomology: Institutional Models
T 3715
Thus, further development could occur if, and only
if, someone procured the resources for that facility
and dedicated it to the rearing and release of natu-
ral enemies in soybean. If inoculative releases
worked, the problem would be less costly. A key
point here is the fragile relationship between
research and extension. Researchers perceive
that they get “rewarded” for publishing the results,
not implementing them. Extension specialists
have to be alert to know the new technology has
been developed, especially if they have not been
included as part of the overall team. Viewed as too
simplistic a solution by some, one way around this
dilemma is to have scientists who have formal,
evaluated appointments in both research and
extension.
Under the T&V Model
Once someone else did the research, experts who
understood biological control could bring the
imported biocontrol agents to a regional training
session where extension specialists were being
trained. Those extension agents could be shown
how to identify the natural enemies, what they did
to the pests and how to tell if the biological control
worked. They also could be taught how to establish
a cottage rearing operation. This process would
continue down the training hierarchy, provided
there were enough natural enemies to go around
and provided the extension specialists had enough
formal education to grasp some basic entomology
and the concept of biological control. A lot of use-
ful information likely would get lost between
training tiers, leaving the ultimate farmer user
wondering what all the fuss was about.
Under the Farming Systems Model
The entire issue would likely never even come up
unless there was an entomologist or other biological
scientist on the rapid rural appraisal team who was
aware of the biological control agents that might be
3716
T Teaching and Training Entomology: Institutional Models
tested on local farms. Given the presence of the
expertise, biocontrol agents could be imported,
released on the farm and evaluated, with the farmers
observing. If the biological control was effective,
farmers would of course want to adopt it and the
entire farming systems effort would have to become
more akin to a T&V effort to train the farmers about
the conservation of natural enemies and perhaps a
cottage rearing and release operation.
Under the Training-Driven Research
Model
Like farming systems, this model would demand
that trainers be up to date on the latest research
literature and recent progress to even know there
was a new biological control agent that might be
used locally. If so, use of the agent in field training
exercises would be quick and would not have to
pass through as many tiers of training as with the
T&V model. The same problem outlined above
exists in this model, too. It does little good to edu-
cate farmers about a new technique and entice
them to adopt it if nobody teaches them how to
implement it in a self-sufficient fashion.
Under the Farmer Participatory
Research Model
If the CGIAR or other staff working with local
farmers were able to identify the indigenous knowl-
edge including experiences with natural enemies,
there likely would be receptivity to the importation
and use of an exotic biocontrol agent. In fact, such
indigenous knowledge might even identify a better
candidate for use than the one potentially coming
from China. If there was no evidence that indige-
nous knowledge systems reflected previous expo-
sure to natural enemies, training in the concepts
and uses of natural enemies would, in essence, have
to occur. Techniques to sustain the biocontrol
effort, if accepted in local culture, would become
part of the training.
Some General Conclusions
Institutional models for the research–extension–
training activities would appear to best serve and
reflect the societies in which they originate. The
Land-Grant model likely could never develop in a
strong hierarchical society. Much of the success of
T&V in Asia and Israel comes from the fact that
the organization of T&V “fits” those societies. The
farming systems approach or Land-Grant approach
do not work well in places where people are sim-
ply afraid of, or are unused to, expressing their
opinions (e.g., Haiti and Cameroon).
There does appear to be a single model poten-
tially usable in the wide array of situations that
exist in today’s world: farmer participatory research.
All farmers and farming communities, save large
industry systems, have an indigenous culture. This
is especially true for resource poor farmers any-
where in the world. They have survived to date
with, to one extent or another, a blend of traditional
approaches and modern science. FPR and, to
almost as great an extent, TDR offer what appear
to be extremely high probabilities for solutions to
agricultural problems that are acceptable to farm-
ers almost by definition, that include farmers in
the  process and that avoid the inherent loss of
information quality that occurs in the transfer
of information.
There is debate over the extent to which the
Land-Grant system involves farmers as active par-
ticipants. No doubt, the better extension systems
do just that, however, the extent to which farmer
involvement permeates the breadth of Land-Grant
efforts has not, to our knowledge, been gauged.
FPR has been harder to implement in relatively
wealthy nations like the USA where farmers see
their tax revenues as providing agricultural ser-
vices and resources they can tap “free of charge”
without having to participate themselves.
Very few people outside the USA really under-
stand the role of the extension specialists in the
Land-Grant Model. To make this model work as
designed, this is a key position, yet, some Land-
Grant universities only recently have begun to

employ individuals with formal, evaluated
appointments in BOTH extension and research.
Others utilize the inter-agency committee
approach, and still others do not address the prob-
lem in any overt fashion. Joint appointments are
still the exception, not the rule. The whole idea of
state specialists grew up informally in the Land-
Grant model as a need, but has over time become
detached from formal research. Europeans do not
employ extension advisory groups at all.
Three of the aforementioned systems have a
rather disappointing track record on environ-
mental issues. The reason is that all three fail to
really focus on the farmer and long-term sustain-
ability. It is hard to think of the off-site impacts of
items like synthetic, organic pesticides if the farm
is not viewed as part of a larger ecological and
cultural system. Farming Systems appears to have
the worst track record of the group on environ-
mental and pest issues, with T&V a close second.
The Land-Grant model is a classic example of
how the system can derail on environmental
issues (e.g., total commitment to pesticides for
almost 25  years). FPR and TDR try overtly to
avoid this problem by beginning their paradigm
with farmer knowledge. Many modern Land-
Grant extension personnel argue that current
extension programs involve farmers in active
decision-making more now than at any time in
history.
Relationships among research, extension and
training, independent of institutional models,
demand choices be made on various levels. Some
cultural, social, and economic systems clearly are
more amenable to one choice versus another:
·· Public versus private
·· Government versus non-government
·· Top-down (bureaucratic) versus bottom-up par­
ticipatory)
·· Profit versus nonprofit
·· Free versus cost-recovery
·· General versus targeted sector
·· Multipurpose versus single purpose
·· Technology-driven versus need-oriented
Teaching Entomology: A Review of Techniques
T 3717
The role of publicly funded research and
extension is changing. In the U.S., large-scale farm-
ers depend less and less upon information gener-
ated and delivered through Land-Grant models.
Part of the reason is that more and more of total
agricultural productivity comes from corporate,
rather than individual farmer, sources. Corpora-
tions have their own staff. The agricultural chemi-
cal companies provide all sorts of information and
technical advice, but are single-minded in approach
and profit motivated. Even in developing nations,
where farming systems, T&V, FPR and TDR have
predominated, they have been sponsored mostly
by international donors and have regressed once
funding ceased. So, just what is the role for public
sponsored research-extension-training? There is a
role if such programs will re-define their clientele
base from richer corporate-industrial programs to
poorer, smaller farming enterprises and beginning
producers. With this new clientele definition must
come a commitment to long-term sustainability of
both the farmer and the farm.
References
Barfield CS, Swisher ME (1994) Integrated pest management:
ready for export? Historical context and international-
ization of IPM. Food Rev Int 10:215–267
Benor D, Baxter M (1984) Training and visit extension. World
Bank, Washington, DC, 199 pp
Shaner WW, Phillips PF, Schmehi WR (1982) Farming sys-
tems research and development: guidelines for develop-
ing countries. Westview, Boulder, 405 pp
Teaching Entomology: A Review
of Techniques
Carl S. Barfield
University of Florida, Gainesville, FL, USA
Both positive and negative interactions with insects
have long been a part of the human experience.
However, people have not always had an opportu-
nity to study insects in any formal, ­systematic
3718
T Teaching Entomology: A Review of Techniques
f­ ashion. Insects as biological organisms and various
institutions where they can be studied are both part
of the discussion on teaching entomology.
With the Neolithic Revolution (ca. 8,000 bce),
humans began the process of sedentary agricul-
ture and civil development. Social scientists have
provided us with at least anecdotal information
on some of the roles played by insects in the
human quest for survival and expansion. Early
in  human existence, insects vectored diseases,
competed for food, consumed structures and
were general irritants. They also were subjects of
curiosity and sources of food and food products
like honey.
Insects are the single largest and most diverse
group of living organisms on Earth, and humans
begin noticing and interacting with them almost
from birth. Insects are among the first living organ-
isms that children notice, and today’s elementary
education includes a host of activities that center
on insects – butterfly gardens, games, music and
use of the Internet being but a few examples. Stu-
dents can choose to study entomology formally as
part of their college education. A bit of historical
context on the university as an institution where
entomology is taught is relevant.
Entomology and Higher Education
Virtually none of the biological sciences existed as
logical, written disciplines until Aristotle, and not
until the ancient Greeks did the study of insects
become characterized by the delight in observa-
tional opportunity insects provided. The 11th
Book of the Roman Pliny’s Historia Naturalis
(ad 77) was the most comprehensive treatise on
insects to date; however, it contained almost no
original observations. Pliny’s time and writings
marked the beginning of a body of knowledge that
would allow university degree programs to arise
in the ninteenth century.
Higher education in Europe, from antiquity
until the end of the middle ages, was maintained
in the monastic and cathedral schools, enriched by
a huge influx of knowledge from the Islamic world.
These institutions eventually developed into uni-
versities as products of cross-cultural influence.
Modern universities thus treasure a multi-cultural
faculty and student body and a plethora of teach-
ing styles. Those early European institutions were
places where ideas spread, and where local and
national authority was engaged. Entomology was
not an area of formal study in these early institu-
tions. Insects were engaged as plentiful examples
of the biological world and, fairly often, as “pests.”
Indeed, the first real concerns about insects as a
group were more in the context of “sources of
products” (e.g., honey) and “competitors” (e.g.,
agricultural pests) than just for the need to under-
stand their biology and history. The Catholic
Church would often put “bad” insects on trial and
hire them defense attorneys, ultimately “banish-
ing” them from select provinces. These practices
occurred fairly frequently from the middle ages
right up to the start of the nineteenth century.
Both the Bible and the Torah refer frequently to
insects, paying special attention to the parables
that can be extracted from insect life and to
whether or not select insects are kosher. Entomol-
ogy was important because most everyone had
personal experiences with insects, not because it
was a recognized area of study.
The study of entomology was nested within
the general biological sciences in Europe and
America throughout the seventeenth and most of
the eighteenth centuries. Things began to change
toward the start of the American Civil War. In
1862, President Abraham Lincoln established the
United States Department of Agriculture and set
in motion what would ultimately be three key
Federal Acts to institutionalize the research and
teaching (Morrill Land Grant Act and Hatch Act)
and extension (Smith-Lever Act) functions by
which all Land-Grant Universities are recognized
today. While entomology is taught at many higher
education institutions, the vast majority of American
entomology majors are housed within colleges
of  agriculture and life sciences at Land-Grant
institutions. Part of the reason for this situation is

that, to many in the general public, insects are
viewed as pests and colleges of agriculture were
developed, at least in part, to help solve the public’s
pest problems.
After WWII, departments of entomology grew
at almost every Land-Grant institution. Today,
many of these institutions offer undergraduate
degrees in entomology, and most offer graduate
degrees. An undergraduate major in entomology,
depending on the institution, will take 18–30 h of
entomology courses offered in sequence. Graduate
entomology degrees take 30–90 additional hours,
the majority of which are insect-related. Graduate
degrees usually include a research experience.
Teaching Entomology at the
University Level
The present treatise will focus very little on the
content of entomology courses; rather, the focus
will be aimed at the style and methods through
which any given content may be delivered.
Clearly, different styles are applicable to differ-
ent audiences, and the professor of any single
course must understand the background and
motivation of his/her audience before the most
appropriate style can be selected. Interestingly,
this is not how it usually works. Most often, any
professor has his/her long-adopted style, and it
is left to the clientele (students) to make the
adjustments. There are possible consequences
of this long-adopted practice, as illustrated in
Table 6.
These various professor roles translate in
myriad ways to an individual style used in the pro-
fessor-student classroom experience. The entire
point is that there is not a single best way to teach.
The capabilities of both professor and students are
basic ingredients in the choice of teaching style.
An assessment of the students’ optimum learning
style early in the term is ideal if the professor has
both the desire and the capability to shift teaching
styles to align with learning styles. Here are a few
possibilities (Table 7).
Teaching Entomology: A Review of Techniques
T 3719
The Socratic, Discussion Approach
This approach to teaching entomology is used
most often in small classes and can be applicable
to either entomology students or general students
simply curious about insects. It is commonly used
in undergraduate honors classes at large universi-
ties, and small colleges and universities often use
this approach throughout their curriculum. Stu-
dents who take these classes typically are inter-
ested, motivated, and engaging. They are willing
to read and discuss a plethora of historical, social
and current issues related to insects and then per-
haps, via a series of essays, analyze and critique
what they have read. In this context, entomology
becomes merely the biological medium in which
to have students develop their interpersonal, ana-
lytical, critical thinking, oral presentation, and
English grammar skills. Such students may become
enticed to explore entomology as a major and an
ultimate career, but most often these students, if
they are interested in the biological sciences at all,
are focused on medicine or veterinary medicine.
Success in this approach demands specific
criteria on the part of both students and professor.
The professor must be knowledgeable of a wide
array of entomological issues and literature. Even
more important, he/she must be charismatic,
engaging and able to entice bright students to
develop curiosity about entomology. The professor
must be able to write and speak well, as these stu-
dents will discern quickly between what is said
and what is done in critique of written and oral
presentation performances. The students must be
engaging and willing to participate in class discus-
sions. The Socratic Approach is, in many ways, the
antithesis of more traditional presentation of copi-
ous facts about insect morphology, physiology,
behavior and control. The idea is to entice students
to explore, on their own, issues presented incom-
pletely in discussion periods, thus developing skills
that will serve them well during their university
tenure. This approach will simply not work if either
the students or the professor are not engaging or if
the class resorts to a host of information-laden

Teaching Entomology: A Review of Techniques, Table 6  Five models for the presence of an instructor in the classroom (summarized from
Grasha 1966)
  Expert
Professor role Source of knowledge; sta-
tus as expert; gets stu-
dents prepared
Advantages Copious information;
development of skills
Disadvantages Volume of information;
students may be intimi-
dated; lack of focus on
underlying processes that
led to information
3720
T
Formal authority Personal model Facilitator Delegator
Status symbol; reinforces Role model; teaches Emphasizes personal Focuses on student
correct, acceptable and students to emulate him student–professor independence;
Teaching Entomology: A Review of Techniques
standard methods; estab- as model interactions; guides serves as a resource
lishes learning goals learning; creates inde-
pendent students; sup-
ports and encourages
Clear expectations; identi- Emphasis on direct Personal flexibility; Students become
fication of acceptable observation and follow- focus on students’ independent
approaches ing the role model needs and goals; open- learners
mindedness
Rigidity in approach to Feeling of inadequacy if Time-consuming; often Student anxiety;
students students feel they can- lacks positive student may be mis-
not live up to model reinforcement perceived as ready
for independent
work

Teaching Entomology: A Review of Techniques, ­Table 7  Comparison of five entomology teaching styles
  Socratic Lecture/lab
Experientially based No No
Focus on insect facts No Yes
Focus on student Yes No
­analytical skills
Demands large No No
resources
Teacher focused No Yes
Student focused Yes No
Ideally requires supple- No No
mental funding
slides, films, blackboard text or, more frequently
now, Power Point or Internet presentations.
Topics typical of this style of teaching may
include many that do not appear, on the surface, to
have anything to do with entomology. However,
discovering their links to entomology is part of
the desired outcome. For example:
1. Pliny’s Historia naturalis
2. The Idea of “Food Insurance”
3. Social attitudes on pesticides versus pharmaceuticals
4. What was The Green Revolution?
5. In your supermarket, what foods are indigenous to
the contiguous 48 states?
6. Medieval higher education?
7. Colonial American living?
8. What is social Darwinism?
9. Who is Norman Borlaug and what did he do?
10. What is the role of empiricism in science?
For example, in a classroom of 20 or so students,
the professor initiates a discussion about the diet
of Colonial Americans. Initially, the professor
seeks to understand what the students already
know about this subject. He discovers this by
­asking them and expecting them to engage in
­dialogue with him and with each other. The con-
versation expands to include the crops grown
and  the problems the colonists had with food
­production. Analogies are drawn periodically to
Teaching Entomology: A Review of Techniques
T 3721
Land lab FFS Internship
Yes Yes Yes
Yes (limited) Yes (limited) Yes (limited)
Yes Yes Yes
Yes Yes No
No No No
Yes Yes Yes
Yes Yes Yes
modern agriculture and its problems. As some of
the problems were insect related, the dialogue
eventually permits the students to discover the
linkages between Colonial American diet and the
study of insects, as well as the various means of
controlling those insects under social and techno-
logical conditions existing in colonial times. The
result is a group of students who are better able to
place insects and entomology into appropriate
historical context and then draw inferences to the
importance of entomology today.
This teaching style assuredly contributes to
the student’s knowledge of biological science and
thus meets both professorial and student objec-
tives in this context. There is a decent chance this
approach will entice such students to become
interested in entomology as a major and a career –
something the vast majority of them have never
before considered. Many will not even know it is
possible to major in entomology.
The Lecture/Lab Approach
By far, the most common way entomology is
taught in modern universities is as a 3- or 4-credit
hour course. This involves a series of lectures (2–3
per week) and 1–2 laboratory sessions per week.
Lectures are used to present facts about entomol-
ogy, and the lab is experientially based and involves
3722
T Teaching Entomology: A Review of Techniques
dissection and study of the various physical and
physiological features of insects. Interestingly,
what actually occurs during the lecture period can
follow any of the teaching styles presented in this
paper; however, by far the most common is using
the professor as the expert whose role it is to pass
entomological facts and knowledge on to the stu-
dents. The labs, if scheduled as typically desired,
mirror the lecture periods and provide visual,
hands-on experience for the topics discussed that
week during lecture.
Lecture approaches vary from professor to
professor, but there is concern under this model to
ensure sufficient information is imparted to justify
the student moving on to the next course in the
sequence. General undergraduates who simply
want biological science credits do take these type
courses just because they want to learn about
organisms they have experienced daily. It is the
entomology majors, however, who professors feel
the need to get ready for continued study of ento-
mology. Lectures are replete with facts, drawings,
Ocellus Compound eye
Maxilla
Mandible
Labrum
Maxilla
Labium
Dorsal aorta
Esophagus Crop Gastric caeca
Brain Heart Eggs
Pharynx
Subesophageal
ganglion Salivary Ventral
glands
nerve cord
Teaching Entomology: A Review of Techniques, Figure 15  Elements of insect morphology and
anatomy.
information; labs follow suit. Figure  15 illustrate
typical information presented under this style.
The emphasis is often on learning facts about
insects. Professors pursue these facts in various
ways. Some choose a systematic approach that
focuses on the principal orders and a comparison
of their morphologies, physiologies, behaviors and
control. Others use a type of comparative biology
approach that may compare insect adaptations
with those of other animals (Fig. 16). While ­various
entomological issues may be discussed, students
spend time hearing the expert impart expertise,
then committing that expertise to memory. Labs
will have students dissecting, searching for, and
identifying these morphological structures, and a
test may include a lab practical where students
must identify parts labeled. This is precisely the
approach used in Colleges of Medicine.
Entomology lecture/lab courses do not have
to unfold in any pre-determined fashion, and
many professors use creativity in what they impart
as entomological knowledge. The point here,
Colon Rectum Anus
Ganglion
 Teaching Entomology: A Review of Techniques
T 3723

­ owever, is that introductory entomology courses

h c­ ollection and preservation methods, plus insect
are typically taught for entomology majors or at
least biological science majors, not for non-science
students, despite the fact that diverse students
often enroll. Under this approach, more emphasis
is placed on facts about insects than on issues
associated with insects. This is not a criticism, but
rather an observation.
Introductory entomology textbooks offer a
range of approaches to teaching the subject. Most
will begin with chapters that discuss the general
importance of insects to science and to humans.
From there, the authors’ approaches vary greatly.
Likely, the most common approach is to begin
immediately with external and internal anatomy
and physiology. Sensory systems, reproduction,
development, life history, and systematics follow.
Then, insects as part of special habitats (e.g.,
aquatic and terrestrial systems) are presented, fol-
lowed by subjects like insect societies, insects and
plants, predation, parasitism, medically important
insects, insect pest management and collection/
preservation methods. Several texts will place
systematics, immediately following introductory
chapters. In any case, most existing entomology
texts will cover the above subjects, independent of
which order of presentation is chosen.
The teaching approach used is tied more to the
bent and capability of the individual professor than
to the subject matter. One teaching strategy is more
of a comparative biology approach that might
compare, for example, the insect leg and locomo-
tion to analogous structures and functions in mam-
mals, birds, reptiles, etc. This approach is effective
in placing insects and their adaptations in perspec-
tive among all animals and is depicted in Fig. 16.
Another strategic approach is to compare
insects among the various orders and explore meta-
morphosis, wing type, locomotion, habitat, life
­history, etc., as a means to compare-and-contrast
the different orders of insects. This approach is
illustrated in Fig. 17.
There is no shortage of information (journals,
books, Internet sources) from which to supple-
ment the basic text to expand student knowledge

Femur
Tibia

Tarsus

Trochanter Pretarsus

Coxa
Tarsomeres
Tarsal claws Arolium

First digit, phlanges 1 & 2

Glenoid fossa
Carpometacarpus Radiale Trioseal canal
Radius Acromion process
of the scapula
Second digit, phalanx 2
Second digit, phalanx 1 Ulnare Coracoid
Third digit, phalanx 1
Ulna Blade of the scapula

Olecranon process of the ulna

Teaching Entomology: A Review of Techniques, ­Figure 16  Comparative biology approach to teaching

insect leg morphology and its analogous structure and function in other animals. Human leg unlabeled;
an exercise might be for students to locate ­analogous structures on human anatomy.
3724
T Teaching Entomology: A Review of Techniques
Teaching Entomology: A Review of Techniques,
Figure 17  Neopterous (a) versus Paleopterous
(b) wing types characteristic of different orders of
insects.
of insects both as biological organisms and as
social entities interacting with humans. Indeed,
social scientists (especially anthropologists) often
use insects to illustrate daily life, problems and
indigenous approaches indicative of specific cul-
tures. Some instructors of basic entomology will
include sections on indigenous cultures and the
role insects played therein.
Increasingly, entomology departments are
offering courses to non-science majors. This is
both as a way to educate undergraduates to the
possibility of entomology as a major and as a
mechanism to capitalize on the general student’s
previous experience with insects and their
required enrollment in a specific number of sci-
ence courses. Perusal of university catalogs usu-
ally will reveal courses such as: The Insects, Bugs
and People, Pesticides and Pills, Ecology and
Human Intervention, Insects and Society, The
Insect World and You. These type courses typi-
cally are taught in one of two diverse formats.
First, they frequently appear as honors courses
taught to small-sized classes consisting of very
intelligent students. In this context, the aforemen-
tioned Socratic style is most prevalent. Such stu-
dents are often searching for creative majors, as
their academic credentials permit them to select
most any major they desire. The second prevalent
delivery format is a lecture, replete with detailed
syllabus and copious illustrations, to a large class.
This delivery style is the aforementioned lecture/
lab, but without the lab portion in most cases.
Most every academic unit, including entomology,
in a large university now offers such courses for
non-majors. Strategically, these courses expose
searching students to possibilities of a major they
had not theretofore considered. Further, these
courses allow students more flexibility in fulfill-
ing general education requirements.
Internships
Most professional disciplines in the biological sci-
ences require extensive internship experiences
prior to certification. One cannot imagine a
licensed Medical Doctor or Veterinarian without
such experiences before they are sanctioned to
ply their trade. The basic biological sciences in
general, and entomology as one example therein,
do not typically make such requirements. How-
ever, those parts of entomology related to agricul-
tural plant protection often do require internships
as part of graduation requirements. While won-
derful in their intent and educational possibili-
ties, internships are not without their potential
problems.

An internship typically occurs toward the
end of an undergraduate degree program. The
idea is to match a student’s need for hands on
experience with a public or private sector busi-
ness. The student would typically leave the uni-
versity and locate at the business site for 1–2
semesters. Under the supervision of the business
contact, the student would work daily in several
of the tasks in which the business is involved. This
might include plot preparation, fumigation, sam-
pling, pest control, assessment of pest damage,
interaction with the public, identification of insect
pests, bookkeeping, and seminars. The entire
experience would be aimed at permitting the stu-
dent to translate academic knowledge obtained to
marketplace demands. The university professor in
charge of internships would make periodic visits
to assess the student’s progress and to witness
first-hand the range of activities in which the stu-
dent was involved. The student would register for
a university course and pay associated tuition,
and he/she may or may not receive salary com-
pensation for the work.
Matching undergraduates with appropriate
public or private internship opportunities often
means asking them to relocate or commute for
1–2 semesters during their undergraduate studies.
Many students are reticent to encumber the addi-
tional travel and per diem costs. Parents express
similar concerns. If an internship is a requisite for
graduation, care must be taken to ensure the
intern’s experience does not resort to a more trivial
exercise based on student economics rather than
on learning needs. Care also must be taken to
ensure the business contact understands the needs
of the student intern and is not simply looking for
a short-term source of cheap labor. Medical and
Veterinary interns accept the requisite; however,
they are older, graduate students, away from paren-
tal influence and knowledgeable that the economic
pay-offs of certification are potentially great. Often,
none of these issues are the same for undergradu-
ates. The more successful undergraduate intern
programs provide financial support, if justified, to
offset additional costs to students.
Teaching Entomology: A Review of Techniques
T 3725
Field-Based Courses
This section refers to courses taught totally in the
field, not to courses where sporadic field trips are
part of a lecture/lab style. If field-based courses are
targeting agricultural entomology, they require
facilities: land, equipment, etc. There is debate over
the cost needs for such facilities. Some feel ade-
quate field-based courses are limited only by the
creative imagination of professors teaching them.
Others feel adequate land, equipment and staff are
crucial to the success of such courses. As universi-
ties often do not consider such teaching resources
high-priorities, these courses often piggyback onto
research efforts, using plots developed for some
professor’s research. This can work, but often
encounters problems as the timing associated with
teaching conflicts with the timing of needed
research activities.
Many universities have natural areas that can,
within certain guidelines, be used to teach various
aspects of entomology. In any case, the fundamen-
tal idea in a field-based course is to provide stu-
dents with experiential learning. Under ideal
conditions, such a course would be offered on
facilities set aside exclusively for teaching and
would be under the control of teachers so that the
timing of activities could occur in an orderly fash-
ion consistent with educational paradigms.
Also known as the Land-Laboratory Approach,
this style is somewhat analogous to a teaching
­hospital where doctors and nurses get experiential
learning under real situations – all supervised by
professorial experts. Where else is it possible to give
developing professionals the opportunity to gain
practical experience in a supervised learning
environment? Many educators feel such practical
experience should be a mandatory part of science
education.
Joliet Junior College in Joliet, Illinois, exempli-
fies the intent and structure of the Land-Laboratory
concept. As stated in their advertisements, they exist
to “serve as a teaching tool for instructors to use
hands-on learning as a means to reinforce class-
room instruction.” The Land-Laboratory exists as
3726
T Teaching Entomology: A Review of Techniques
101 acres of land donated for the exclusive purpose
of teaching. The Pennsylvania State University
has a similar facility dedicated to land analysis. In
most cases, Land-Laboratories exist because the
land and perhaps the infrastructure needed to make
it operational were donated. Rarely do universities
encumber the costs of a Land-Laboratory from
their operational budgets.
The Escuela Agrícola Panamericana (Pan
American School of Agriculture, EAP) in Honduras,
Central America, provides an example of both
experiential learning and the Land-Laboratory
style (Fig.  18). Students attend from throughout
the Caribbean Basin and beyond and spend 0.5 day
in class and 0.5 day in the field in a wide array of
agricultural experiential learning activities includ-
ing land preparation, planting, harvesting, pro-
cessing, marketing, plant protection, outreach and
Teaching Entomology: A Review of Techniques,
Figure 18  Zamorano students in land-laboratory
exercise, Pan American School of Agriculture,
­Honduras, Central America.
with both plant and animal systems. Entomology
plays a prominent role in the experiences of the
“Zamoranos.”
Teaching at the International Rice Research
Institute (Philippines) exemplifies the same
approach and has been in place much longer than
the EAP. The general trend is for international
research institutes that also teach to place a higher
premium on Land-Laboratory approaches than
do U.S. universities. This is true likely because they
have the land and labor to make this approach
work and because they understand that hands-on
experience for their student clientele is of maxi-
mum importance.
Extra-University Models
The international arena offers a variety of teach-
ing approaches aimed directly at farmers and
­professionals who provide technical support to
farmers. In this context, the stakes (possible food
self-sufficiency) are much higher than the pursuit
of an undergraduate college degree. These pro-
grams offer both challenge and opportunity to
university-based degree programs in entomology.
The Farmer Field School Approach
The principal sponsor and promoter of this
approach is the United Nations Food and Agricul-
ture Organization, Rome, Italy. Principally, the
Global Integrated Pest Management Group within
the UN/FAO developed this model based on expe-
riences in Rice Integrated Pest Management pro-
grams in Indonesia. This approach serves as a
model that universities might want to emulate in
those aspects of entomological education that
demand experiential learning.
The FFS was established to provide training
to farmers and their support network (research-
ers and extension specialists) on the problems
and opportunities associated with specific crops
(Fig. 19). The idea is to follow crop development

Teaching Entomology: A Review of Techniques,
Figure 19  Farmer field school training in
­corn-based agriculture, Honduras.
from land preparation to marketing of the ­harvest,
teaching at every step the techniques demanded,
the pests encountered, the sampling needed, the
pest management approaches needed, etc. Those
same trained people obtain the multiplier effect
by training others. The idea is to teach, in a hands-
on fashion, the details for any specific crop. As the
crops change, so do the issues and thus additional
training may be needed. In 2002, FAO is assisting
Korea in the establishment of a junior college
level curriculum of study based exactly on the
FFS concepts. Students would hold night sessions
on the more general aspects of, say, entomology.
Unlike the lecture/lab approach typical of Ameri-
can Universities, the FFS approach begins with
the field and then moves to general classroom
experience (Fig. 20).
The FFS approach served as the basis for
development of The Farmer Centered Agricultural
Resources Management (FARM) Program that,
until funding declined, consisted of the member
countries of China, India, Indonesia, Nepal, Phil-
ippines, Sri Lanka, Thailand and Viet Nam. The
entire FARM program was supported by the
UNDP and implemented by FAO. In 2002, there
were 19 sites in eight nations covering some 10,000
Asian households (Figs. 21 and 22). FARM, and
its parent idea, the FFS, was one of the most
rapidly expanding teaching resources in the world.
Teaching Entomology: A Review of Techniques
T 3727
Teaching Entomology: A Review of Techniques,
Figure 20  Farmer field school classroom training,
Indonesia.
It offered practical hands-on training that could
be supplemented with more traditional academic
education in a wide array of subjects, including
entomology. Sadly, politics overtook needs and
funding was cut to the point the program vanished
in its original form.
The purpose of the FFS is not pursuit of aca-
demic degrees. Training is focused on the speci-
ficities of individual crops or cropping systems
and is increasingly supplemented with “after
hours” academic work on subjects like entomol-
ogy. Students are adults, not undergraduates in
pursuit of degree requirements. Results of this
educational style are improved chances of food
self-sufficiency, not a B.S. degree and employment.
However, in the few places where the fundamental
3728
T Teaching Entomology: A Review of Techniques
Teaching Entomology: A Review of Techniques,
Figure 21  Farmer field school plot facilities for
rice-based agriculture, Indonesia.
Teaching Entomology: A Review of Techniques,
Figure 22  In-field training on rice insects,
Indonesia.
concepts of the FFS or its close relative, the Land-
Laboratory, have been directly combined with
academic programs, the results have been aston-
ishing. These are the rare situations that make
agricultural and entomological education the
most analogous to professional school education
in the USA.
Cross Style Comparisons
Three things limit what style is used to teach ento-
mology (i) imagination, (ii) budget, and (iii) either
professor or student capability. The most appro-
priate criterion for a comparison among styles is
whether or not students achieved course objec-
tives. The reality is that various styles have differ-
ent intents and expected outcomes. The problem
occurs when a style of teaching is used that
has  a  low probability of generating the desired
outcomes.
Use of the lecture/lab approach where the lec-
ture is used to present copious facts about insects
which are to be memorized and repeated on a mul-
tiple choice exam may not be the most appropriate
for a group of students who have selected beginning
entomology for its general education function and
who are simply curious about insects. Not providing
the future field practitioner of agricultural entomol-
ogy a field-based experience will not achieve desired
outcomes in the most efficient manner.
If the professor desires students to become
independent thinkers, capable of analysis and
presentation, playing the role of “expert” who
imparts facts about insects that are to be learned
and demonstrated on an exam is probably not
the most ideal approach. Tailoring teaching style
to a particular student audience is hard, not easy.
It takes effort and does not occur auto­matically.
Just like any other aspect of the human experi-
ence, some professors can do it and others can-
not. This is not a criticism, but a fact. Ideal
learning experiences tend to occur in ­entomology
or any other subject when care is taken to match
the style of teaching to the needs and learning
styles of students in that class that term. Adop-
tion of a single teaching style to be used through-
out one’s tenure is, quite literally, a “hit and miss”
proposition where desirable and less desirable
outcomes will occur among semesters.
The key to any professor adjusting to
dynamic learning styles of students is an ability
to gauge quickly their response to a variety of
styles. Literally, what works well one term and
gets students involved and responsive is not
automatically what will work best next term,
given a new group of students. Many, if not
most, university professors of basic entomology
 Tegmen (pl., Tegmina)
T 3729

courses offered to entomology or science majors,

do not attempt to adjust to perceived student
learning styles. Such adjustments are much more
common in entomology courses offered to non-
science majors.
 Teaching and Training Entomology:
Institutional Models

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Pennsylvania
Smith RF, Mittler TE, Smith CN (eds) (1973) History of
entomology. Annual Reviews, Palo Alto, California,
517 pp
References

Common IFB (1990) Superfamily Hyblaeoidea. In: Common

Teak Moths (Lepidoptera:
Hyblaeidae)
John Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Teak moths, family Hyblaeidae, are a small tropical
family of 18 species, mostly Indo-Australian and in
the genus Hyblaea (one pantropical species is also
established in southern Florida). The family is in
the superfamily Pyraloidea in the section Tineina,
subsection Tineina, of the division Ditrysia (some-
times placed in its own superfamily, Hyblaeoidea).
Adults medium size (25–49  mm wingspan), with
head relatively smooth-scaled; haustellum naked;
labial palpi porrect and prominent; maxillary palpi
3- to 4-segmented. Maculation mostly shades of
brown, with colorful spotted hindwings. Bodies are
usually robust. Adults are diurnal or perhaps cre-
puscular. Larvae are leaf rollers. Host plants are in
Bignoniaceae and Verbenaceae. One economic
species: the teak leafroller. Due to their robust form,
these moths were often associated with Noctuidae
in the past (Fig. 23).
IFB, Moths of Australia. Melbourne University Press,
Melbourne, pp 334–337
Dalla Torre KW von (1928) Die Hyblaeinen (Noktuiden).
Entomol Jahrb 37:162–164
Koning HS de, Roepke W (1949) Remarks on the morphol-
ogy of the teak moth, Hyblaea puera Cr. (Lep. Hyblaei-
dae). Treubia 20:25–30
Singh B (1956) Description and systematic position of lar-
vae and pupa of the teak defoliator, Hyblaea puera
Cramer (Insecta, Lepidoptera, Hyblaeidae) Indian
Forest Records (n.s.). Entomology 9:1–16
Viette PEL (1962) Les Noctuidae Hyblaeinae de Madagascar
(Lep.). Bull Mens Soc Linn Lyon 30:191–194
Technical Grade
A chemically pure preparation. This is often used
to describe research-grade pesticides as opposed
to commercial formulations.
 Insecticides
Tegmen (pl., Tegmina)
The thickened front wing of Orthoptera and
related insects.
 Wings of Insects
3730
T Tegula

Tegula Telmophages
A small flap or lobe at the anterior edge of the Arthropods that feed at blood vessels, and specifi-
forewing of some insects. It is also known as the cally from pools of blood created by lacerating
patagium. vessels (contrast with solenophages).

Telegeusidae Telson
A family of beetles (order Coleoptera). They com-
The terminal portion of the abdomen bearing the
monly are known as long-lipped beetles.
anus. In insects the telson is usually found only in
 Beetles
the embryonic stage. It is not normally recognized
as a body segment in insects, but it is in some other
invertebrates.
Telephone-Pole Beetles
Members of the family Micromalthidae (order
Coleoptera). Template
 Beetles
A macromolecular mold for synthesis of another
macromolecule. Duplication of the template takes
Teloganellidae two steps; a single strand of DNA serves as the
template for a complementary strand of DNA or
A family of mayflies (order Ephemeroptera). mRNA.
 Mayflies

Tenaculum
Teloganodidae
In Collembola, a small structure on the third
A family of mayflies (order Ephemeroptera). abdominal segment that serves as a clasp for the
 Mayflies furcula (Fig. 24).
 Abdomen of Hexapods

Telomere
Tenebrionidae
Telomeres are the physical ends of eukaryotic
chromosomes. They protect the ends of chromo- A family of beetles (order Coleoptera). They com-
somes and confer stability. Telomeres consist of monly are known as darkling beetles.
DNA repeats and the non-histone proteins that  Beetles
bind specifically to those sequences.  Darkling Beetles

Telopodite Teneral

The portion of the limb beyond the base; the The condition of an insect after molting but before
shaft. the new cuticle has hardened.
 Tent Caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae)
T 3731

In the earlier literature, tent caterpillars were

Antenna
referred to the genus Clisiocampa which was
Pretarsus
Tibiotarsus Eye erected by Curtis in 1828, unaware that Hübner
Femur
Pronotum had already named the group.
Trochanter Species of Malacosoma occur throughout the
Mesonotum
Coxa
Precoxae Holarctic region. Although the taxonomy of the
Metanotum
Collophore group is far from settled, currently there are 26
valid species. Six of these occur in North America
Tenaculum (catch)
and the rest in Eurasia. A number of these species
are also further divided into subspecies. The best-
known of the tent caterpillars are the North
American species, particularly the eastern tent
caterpillar, M americanum (Fig.  25), the western
tent caterpillar, M. californicum and the forest tent
Manubrium
caterpillar, M. disstria (Fig.  26). Of the Eurasian
Dens
Furcula species, M. neustrium is the best known and has
Mucro (spring) the broadest geographical range.

Tenaculum, Figure 24  Lateral view of a springtail
(Collembola).
Tent Caterpillars
Some members of the family Lasiocampidae
(order Lepidoptera).
 Tent caterpillars, Malacosoma spp.
 Lappet Moths
 Butterflies and Moths
Tent Caterpillars, Malacosoma
spp. (Lepidoptera:
Lasiocampidae)
Terrence D. Fitzgerald
State University of New York at Cortland,
­Cortland, NY, USA
Tent caterpillars occur in the family Lasiocampi-
dae and are related to silk moths in the families
Bombycidae and Saturniidae. Tent caterpillars are
placed in the genus Malacosoma established by
Hübner in 1820. The name Malacosoma derives
from the Latin for malakos (soft) and soma (body).
Life Cycle and Behavioral Ecology
Little detailed information is available for many of
the species of Malacosoma, but the evidence we
have suggests that their life history features are sim-
ilar to those of the eastern tent caterpillar, the most
studied of the group. The seasonal history and
behavioral ecology of this species is described here.
The eastern tent caterpillar obtains all the
energy required for its adult life while still a larva
and reproductively mature moths emerge from
their cocoons in late spring. Females secrete sex
pheromones to attract males. Mating typically
takes place soon after eclosion and the female may
oviposit the evening of the same day she emerges.
The moth produces a single egg mass, typically
containing 150–250 eggs, though larger egg masses
are not uncommon. The egg mass is attached to a
branch of the host plant and is covered with a foamy
substance termed spumaline. The material serves to
protect the eggs from desiccation and may also pre-
vent parasitoids from reaching the larvae inside the
eggs. Embryogenesis proceeds rapidly and fully
formed larvae can be found within the shells of their
eggs several weeks following oviposition. The
sequestered caterpillars undergo an obligatory
3732
T Tent Caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae)

Tent Caterpillars, Malacosoma spp. (Lepidoptera:

Lasiocampidae), ­Figure 25  Eastern tent
caterpillar, Malacosoma americanum: (a) egg
masses of the eastern tent caterpillar with and
without spumaline (left) and of the forest tent
caterpillar (right) (b) mature larvae, (c) adults.
(Photos by Terrence Fitzgerald.)
Tent Caterpillars, Malacosoma spp.
(Lepidoptera: Lasiocampidae), F ­ igure 26 
­Forest tent caterpillar, Malacosoma d ­ isstria:
(a) larvae hatching on egg mass, (b) m ­ ature
larvae, (c) adult. (Photos by Terrence
Fitzgerald.)

­ iapause which is broken only after exposure to cold

d may obtain food by mining buds. Development
temperatures over the winter. Eclosion of the cater- occurs rapidly and most species finish the active lar-
pillars in the spring is closely synchronized with the val stage of their life cycle in 6–8 weeks. The last of
flushing of leaves of the host tree but if eclosion the six larval instars spins a cocoon in a protected
occurs before leaves have flushed the young larvae place and the moth emerges about 2 weeks later.
 Tent Caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae)
All tent caterpillars are social species that live
in sibling groups. Although they are commonly
viewed as pests because of their habit of defoliat-
ing forest and ornamental trees, they are among
the most social of all caterpillars and exhibit many
noteworthy behaviors. Their life histories are high-
lighted by four collective behaviors: shelter build-
ing, thermal regulation, cooperative foraging, and
predator defense.
For those species that make large, permanent
tents such as the eastern tent caterpillar, the tent
site is selected by the first instar caterpillar, typi-
cally in a part of the tree that receives the early
morning sun. In the eastern tent caterpillar, the
parent moth may facilitate this process by select-
ing an oviposition site on the south side of a tree.
The tent is expanded daily to accommodate the
growing colony, allowing the caterpillars to rest,
molt, and thermoregulate in synchrony. Silk is
added to the structure during episodes of spinning
which precede bouts of foraging. The colony
expands their tent until they enter the last stadia
of their lives as caterpillars; the last instar retains
its silk to construct its cocoon.
The tent is multi-functional. It serves primar-
ily as a secure mat, providing the caterpillars with
purchase during their extended periods of rest.
The tent also serves as a staging area from which
colonies launch intermittent forays in search of
food. It may also serve as a communication center
where successful foragers alert their hungry tent
mates to food discoveries as detailed below. The
extent to which the tent protects the caterpillars
from predators and parasitoids is unclear. When
the caterpillars rest within the tent they may be
secure from certain predators and parasitoids that
cannot enter the structure. However, the caterpil-
lars often rest on the outside where they are more
vulnerable but not defenseless. Caterpillars assem-
bled on the surface of the tent respond to preda-
tors with a defensive body-flicking display. The
display may serve to alert tent mates to danger.
Tent caterpillars are active during the time of
the year when the days are typical cool and the
tent serves the important function of facilitating
T 3733
thermoregulation. Although eastern tent caterpil-
lars are capable of locomotion at temperatures as
low as 3–5°C, they cannot process food at temper-
atures much below 15°C. The caterpillars can
achieve temperatures in excess of ambient only by
basking in the sun, and on cool and cloudy days
they grow little if at all. The caterpillars have dark
bodies and are effective behavioral thermal regu-
lators but the tent enables the caterpillars to elevate
their body temperatures far above ambient. They
aggregate on the surface of the tent or within the
structure. When basking on the surface, the cater-
pillars arrange themselves in a tight cluster, mini-
mizing heat loss due to wind currents. The tents
act like greenhouses, trapping the heat of the
morning sun. Because of its layered structure, the
tent is thermally heterogeneous and the caterpil-
lars can adjust their temperature by moving from
layer to layer. One study showed that a cluster of
models simulating an aggregation of caterpillars
basking in the sun on the tent surface achieved
temperatures as great as 44°C in excess of ambient
temperature. Indeed, the tent may become so hot
by midday that the caterpillars overheat and take
evasive action to avoid the sun. They do this by
moving to the shaded side of the tent and by hang-
ing suspended in the air, attached to the tent only
by the posterior ends of their bodies. This mini-
mizes the amount of heat that is conducted to their
bodies from the hot tent surface and maximizes
the cooling effect of convective air currents.
Eastern tent caterpillars secrete a chemical
trail marker as they move over the branches of the
host tree. The marker is secreted from the ventral
surface of the tip of the abdomen and caterpillars
actively mark trails by lowering and dragging the
tips of their abdomens against the substrate.
Although eastern tent caterpillars also lay silk
strands as they move over branches, silk does not
elicit trail following; the elicitation of trail follow-
ing is dependent on the trail pheromone.
The eastern tent caterpillar utilizes a bilevel
trail system consisting of exploratory and recruit-
ment components. Hungry foragers in search of
food mark exploratory trails with a pheromone as
3734
T Tent Caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae)
they move over the bark surface. The caterpillars
show great reluctance to move over surfaces not
already marked with the exploratory trail phero-
mone, advancing slowly in close proximity to
others. Exploratory trails enable foraging columns
to stay together without necessitating direct phys-
ical contact among the caterpillars. Larvae that
locate food and feed to repletion lay down recruit­
ment trails as they follow their exploratory trails
back to the tent. Recruitment trails are more
effective in eliciting trail following than explor-
atory trails; they function to lead hungry tent
mates to food finds in a manner similar to the
recruitment trails of ants and termites. It is pres-
ently not known whether the difference between
exploratory and recruitment trails is qualitative
or quantitative, but recent studies of the related
genus Eriogaster suggest that the difference may
be quantitative.
The foraging system of the forest tent cater-
pillar differs from that of the eastern tent caterpil-
lar in that the larvae range widely in search of food
and do not establish a nest or other permanent
resting site. The caterpillars travel between feeding
sites en masse, laying down an exploratory trail
marker as they proceed. After feeding, the caterpil-
lars move to a temporary resting site or bivouac.
Trails marked by the caterpillars immediately after
feeding are more stimulating than exploratory
trails and serve to recruit fed colony mates to the
new bivouac where they rest en masse.
Studies undertaken to identify the trail pher-
omone of the eastern tent caterpillar showed that
the chemical 5β-cholestane-3,24-dione, isolated
from the tips of the abdomens of eastern tent cat-
erpillars, elicited trail following when applied to
paper cards at rates as low as 10−10  g/mm trail.
Bioassays, however, showed that while the chemi-
cal was competitive with the exploratory trails
of  the caterpillar, it was not competitive with
authentic recruitment trails. A number of com-
pounds with similar structure were subsequently
obtained and bioassayed for activity. Of these, the
steroid 5β-cholestane-3-one (Fig.  27) proved
more effective in eliciting trail following than
CH3 CH3
CH3 CH3
CH3
O
H
Tent Caterpillars, Malacosoma spp. (Lepidoptera:
Lasiocampidae), Figure 27  5β-cholestane-3-one, a
chemical that elicits trail following in caterpillars.
5β-cholestane-3,24-dione and was shown to be
fully competitive with the authentic recruitment
trails of the caterpillar.
Tent caterpillar larvae are highly sensitive to
the amount of pheromone present in trails and
carefully compare trails at branch junctures by
sweeping their maxillary chemoreceptors from trail
to trail. Caterpillars choose stronger over weaker
trails and newer over older trails when foraging
allowing them to move efficiently between feeding
and resting sites.
Economic Importance and
Caterpillar Outbreaks
Gregarious caterpillars are among the most eco-
nomically important of forest and shade tree
insects. Studies indicate that about 70% of the lepi-
dopterous pests of trees capable of achieving out-
break proportions deposit eggs in batches and over
half of these form social larval aggregates. The abil-
ity of social species of caterpillars to reach outbreak
numbers has been attributed to enhanced predator
defense, collective thermoregulation, and foraging
efficiency. Although all species of North American
tent caterpillars may be capable of achieving out-
break numbers, the most significant are the forest
tent caterpillar, the eastern tent caterpillar, the
western tent caterpillar (M. californicum), and the
southwestern tent caterpillar (M.  incurvum). Mal­
acosoma disstria is the best-known of these species,
 Tent Caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae)
causing considerable damage during its periodic
outbreaks. Surveys conducted by the U.S. Depart-
ment of Agriculture showed that between 1953 and
1983, the forest tent caterpillar achieved outbreak
status on 70 occasions. The Eurasian species
M. neustrium is an economically important defoli-
ator of oak and other forest and shade trees.
It is commonly reported that outbreaks of
tent caterpillars occur at ten-year intervals but
the historical record shows that the actual interval
between successive outbreaks varies widely. The
most complete records of forest tent caterpillar
outbreaks are from Ontario, Canada. From 1867 to
1987, province-wide outbreaks occurred at inter-
vals of 9–16  years. Caterpillars remained in out-
break numbers for 1–8 years (average = 3 years).
In Manitoba and Saskatchewan, outbreaks occurred
at 6–16 year intervals from 1923 to 1957 but some
areas in these provinces experienced only one out-
break in the 34-year period.
Density dependent mortality factors that
bring population explosions of the tent caterpil-
lar to a close are fungal, viral, and to a lesser
extent bacterial diseases, starvation, and preda-
tors and parasitoids. The primary density inde-
pendent factors are elements of the weather. Cool
and cloudy springs can be lethal for tent caterpil-
lars. As noted above, studies of the eastern tent
caterpillar show that when a tent caterpillar’s
body temperature drops below about 15°C, the
insect cannot digest food. Although air tempera-
ture in the spring is often less than this threshold
temperature, caterpillars bask in the sun to raise
their core temperatures. However, basking is not
possible if there is dense cloud cover, and a pro-
longed episode of cool, cloudy weather can lead
to the death of the caterpillars due to starvation.
A combination of density dependent and density
independent mortality factors may interact to
bring a population explosion to a close. Thus, dis-
ease may sweep through a population of forest
tent caterpillars, precipitated by the cool and wet
weather that favors the pathogen Furia.
In addition to its importance as a defoliator,
the eastern tent caterpillar has been implicated in
T 3735
the death of horses. During the spring of 2001 and
2002 horse breeders in central Kentucky experi-
enced an unprecedented loss of foals, a phenome-
non now known as Mare Reproductive Loss
Syndrome or MRLS. In 2001 alone, more than
3,000 mares aborted, causing an estimated loss of
over $330 million. At the time of the abortions
there was an outbreak of tent caterpillars, and stud-
ies showed that pregnant mares fed the caterpillars
aborted their foals. The exact cause of MRLS is not
known but one possibility is that irritation of the
mare’s gut by setal fragments facilitates the inva-
sion of bacteria which infect the placenta and
induce abortion. Apparent instances of MRLS have
also been reported from other areas experiencing
outbreaks of tent caterpillars including New York,
New Jersey, Florida, and Washington State.
References
Bernard B, Webb B, LeBlanc M (2003) Gastric administration
of eastern tent caterpillars causes early fetal loss in preg-
nant mares. In: Proceedings of the First Workshop on
Mare Reproductive Loss Syndrome. University of
­Kentucky Agricultural Experiment Station Publication
SR-2003-1, p 79
Casey TM, Joos B, Fitzgerald TD, Yurlona M, Young P (1988)
Group foraging, thermoregulation, and growth of east-
ern tent caterpillars in relation to microclimate. Physiol
Zool 61:372–377
Crump D, Silverstein RM, Williams HJ, Fitzgerald TD (1987)
Identification of the trail pheromone of the eastern
tent caterpillar Malacosoma americanum (Lepidoptera:
Lasiocampidae). J Chem Ecol 13:397–402
Dirikolu L, Hughes C, Harkins D, Boyles J, Bosken J, Lehner F,
Troppmann A, McDowell K, Tobin T, Sebastian M,
­Harrison L, Crutchfield J, Baskin SI, Fitzgerald TD
(2003) The toxicokinetics of cyanide and mandelonitrile
in the horse and their relevance to the mare reproduc-
tive loss syndrome. Toxicol Mech Methods 13:199–211
Filotas MJ, Hajek AE, Humber RA (2003) Prevalence
and  biology of Furia gastropachae (Zygomycetes:
Entomophthorales) in populations of the forest tent
caterpillar (Lepidoptera: Lymantriidae). Can Entomol
135:359–378
Filotas MJ, Hajek AE (2004) Influence of temperature and mois-
ture on infection of forest tent caterpillars (Lepidoptera:
Lasiocampidae) by the entomopathogenic fungus Furia
gastropachae (Zygomycetes: Entomophthorales). Environ
Entomol 33:1127–1136
3736
T Tenthredinidae

Fitzgerald TD, Costa JT (1986) Trail-based communication Tephritidae

and foraging behavior of young colonies of the forest
tent caterpillar Malacosoma disstria Hubn. (Lepi-
doptera: Lasiocampidae). Ann Entomol Soc America A family of flies (order Diptera). They commonly
79:999–1007 are known as fruit flies (but not to be confused
Fitzgerald TD (1995) The Tent Caterpillars. Cornell Univer- with small fruit flies, Drosophilidae)
sity Press, Ithaca, New York
Fitzgerald TD, Jeffers PM, Mantella D (2002) Depletion  Flies
of host derived cyanide in the gut of the eastern tent
caterpillar, Malacosoma americanum. J Chem Ecol
28:257–268 Teratembiidae
Joos B, Casey TM, Fitzgerald TD (1988) Roles of the tent in
behavioral thermoregulation of eastern tent caterpillars.
Ecology 69:2004–2011 A family of web-spinners (order Embiidina).
Kane E, Kirby E (2001) Death in the bluegrass. Equus  Web-Spinners
287:60–68
Nothnagle PJ, Schultz JC (1987) What is a forest pest? In: Bar-
bosa P, Schultz JC (eds) Insect outbreaks. Academic,
New York, pp 59–80 Teratomyzidae
Roessingh P, Peterson SC, Fitzgerald TD (1988) The sen-
sory basis of trail following in some lepidopterous
larvae: contact chemoreception. Physiol Entomol
A family of flies (order Diptera).
13:219–224  Flies
Ruf C (2002) Social life-styles in caterpillars: behavioral
mechanisms and ecological consequences. Ph.D. disser-
tation, University of Bayreuth, Bayreuth, Germany
Stehr FW, Cook EF (1968) A revision of the genus Malaco­ Tergum
soma Hübner in North America (Lepidoptera: Lasio-
campidae): systematics, biology, immatures, and The dorsal section of a body segment. Also called
­parasites. Smithsonian Institution, U.S. National Museum
Bulletin, p 276 tergite. They sometimes are named after their
Webb BA, Barney WE, Dahlman DL, DeBorde SN, Weer C, body segment (e.g., mesotergum is the tergum of
Williams NM, Donahue JM, McDowell KJ (2004) Eastern the mesothoracic segment) (Fig. 28).
tent caterpillars (Malacosoma americanum) cause
mare reproductive loss syndrome. J Insect Physiol
50:185–193
Termen
In Lepidoptera, the edge of the wing in the distal
Tenthredinidae (lateral) area.

A family of sawflies (order Hymenoptera, subor-

der Symphyta). They commonly are known as
common sawflies. Terminal Arborization
 Wasps, Ants, Bees, and Sawflies
An extensive branching of the dendrites at the end
of a nerve cell (Fig. 29).

Tentorium
Terminal Filament
The internal invaginations of the exoskeleton
occurring in the head tergite. Long, slender projections from the last abdominal
 Head of Hexapods segment.
 Termites (Isoptera)
T 3737

Mesothoracic wing

Mesotergum Metathoracic wing

Conjuctiva 1st abdominal tergum

Metatergum
Protergum
Metapleural wing process
Metapleural suture

Tympanum
1st abdominal spiracle
Mesopleural wing process
Mesothoracic spiracle Metathoracic spiracle
Mesepisternum
Metathoracic leg process
Mesopleural suture
Mesepimeron Metepisternum

Mesothoracic leg process

Coxa of mesothoracic leg

Tergum, Figure 28  Head and thorax of a grasshopper ( Orthoptera).

Dendrite
Termites (Isoptera)
Axon
Perikaryon
Rudolf H. Scheffrahn
Terminal University of Florida, Ft. Lauderdale, FL, USA
Perikaryon
Arborization

Termites are small to medium-sized orthopteroid

Axon Dendrite insects that are cryptic in habit. All species live in
eusocial colonies and feed primarily on cellulose.
Terminal Arborization, Figure 29  Diagrams of Although referred to in older literature as “white
insect nerve cells ­showing direction of nervous ants,” termites are unrelated to ants. The name of
impulse (adapted from Chapman 1998, The the order is derived from the Greek words “iso”
­insects: structure and function). (equal) and “ptero” (wing) that describe the simi-
lar length and shape of both the fore and hind
wings of the reproductive alates. Mature colonies
Termitaphididae are composed of task-specific castes that typi-
cally include one or more pairs of reproductives,
A family of bugs (order Hemiptera, suborder about 0–25% soldiers, and a majority of imma-
Pentamorpha). ture or sterile workers. During part of the year,
 Bugs colonies may also contain some maturing or fully
winged reproductives (alates, imagos) destined
to leave their colony in brief, but often intense,
Termitarium dispersal flights. The order Isoptera is divided
into seven families. The family Rhinotermitidae
A termite nest, or the artificial net used to house is divided into seven small and closely allied
termites in a laboratory. ­subfamilies and the Termitidae into four large
3738
T Termites (Isoptera)
Termites (Isoptera), Table 8  
Order: Isoptera, the termites
Family: Hodotermitidae, Old World Harvester Termites
Family: Kalotermitidae, Drywood and Dampwood Termites
Family: Mastotermitidae, Giant Northern Australian
Termite
Family: Rhinotermitidae, Lower Subterranean Termites
Subfamily: Coptotermitinae
Subfamily: Heterotermitinae
Subfamily: Prorhinotermitinae
Subfamily: Psammotermitinae
Subfamily: Rhinotermitinae
Subfamily: Stylotermitinae
Subfamily: Termitogetoninae
Family: Serritermitidae
Family: Termitidae, Higher Termites
Subfamily: Apicotermitinae, Soldierless Termites
Subfamily: Macrotermitinae, Fungus-Growing Termites
Subfamily: Nasutitermitinae, Nasutiform Termites
Subfamily: Termitinae
Family: Termopsidae, Primitive Dampwood or Rottenwood
Termites
Total
and diverse subfamilies (Table  8). By historical
convention, all but 2% of termite genera end in
the suffix “termes,” the Latin word for termite.
Phylogeny and Fossils
Termites are closely related to cockroaches and
mantids. Based on molecular and morphological
characters, the Mastotermitidae are the most
primitive termite family, followed by the Termop-
sidae, Hodotermitidae, Kalotermitidae, Serriter-
mitidae, Rhinotermitidae, and finally the “higher”
termites of the family Termitidae. The earliest
fossil records of termites are from the Cretaceous
period (144–65 million years before present,
YBP) and include the families Mastotermitidae,
Hodotermitidae, and Termopsidae. Cretaceous
No. genera No. species
3 19
21 452
1 1
14 350
1 79
3 143
1 18
1 8
7 56
1 43
1 3
2 2
240 2,021
42 215
14 365
93 674
91 771
5 21
286 2,870
fossils consist of wings or imago bodies in sedi-
mentary deposits or amber. Excellent soldier
and alate fossils have been found for the Masto-
termitidae, Kalotermitidae, Rhinotermitidae,
and Nasutitermitinae in Dominican amber from
the Oligocene to early Miocene (20–30 million
YBP). Over one hundred extinct termite species
have been identified worldwide except from
Africa.
Description of Important Taxa
The family Mastotermitidae consists of a single
primitive species, Mastotermes darwiniensis, a large
subterranean nester that attacks sound wood in
northern Australia. The alates of M. darwiniensis
have some roach-like characters and queens lay

eggs in batches that resemble cockroach ootheca.
The Termopsidae are large to very large primitive
wood-nesting termites found in damp logs in tem-
perate forests of both hemispheres. The Hodoter-
mitidae are an Old World family consisting of large
termites that nest in the soil and openly forage in
grasslands and savannas for herbaceous growth.
Unlike other termites, the eyes of Hodotermitidae
workers are rather well developed. The Kaloter-
mitidae include wood-dwelling species found
throughout the tropics and subtropics. Although
some species require wood with moderate to high
moisture content, other kalotermitids thrive in low
moisture conditions and are called drywood ter-
mites. Drywood termites produce characteristic
six-sided fecal pellets that are stored in galleries
and periodically ejected from the wood through
surface holes. One drywood species in particular,
Cryptotermes brevis, is a worldwide pest known
only from structural lumber and furniture.
The family Rhinotermitidae is worldwide in
distribution and contains primarily wood-feeding
subterranean nesters and includes some of the most
important pest genera attacking buildings: Coptot­
ermes (Coptotermitinae), Heterotermes, and Reticu­
litermes (Heterotermitinae). A few Coptotermes are
known to build mounds in Australia. The Prorhino-
termitinae (Prorhinotermes) typically locate their
nests inside and under damp logs near oceanic
coastlines. The Psammotermitinae constitute one
genus (Psammotermes) of subterranean termites
that occurs in arid lands of Africa and the Middle
East. Some genera of the Rhinotermitinae, such as
the neotropical Rhinotermes and the paleotropical
Schedorhinotermes have dimorphic soldiers, one
with large mandibles and the other with an extended
labrum, that bear little or no resemblance to one
another. The monogeneric subfamilies Stylotermi-
tinae and Termitogetoninae are limited to central
and Southeast Asia, respectively. The Serritermiti-
dae are an obscure family known only from a few
collections of two species in Brazil.
By far the largest termite family is the Termiti-
dae inclusive of all evolutionarily advanced or “higher
termites.” The soldierless subfamily Apicotermitinae
Termites (Isoptera)
T 3739
includes grass feeders and humivores. Most apico-
termitine species live in diffuse underground ­gallery
systems but some African genera, such as Apico­
termes, build elaborate geometrically proportioned
nests. The Macrotermitinae are an Old World
­subfamily of large mound-building termites. These
medium to very large termites eat fungus grown on
special combs in their nest. Many species provision
the fungus with herbaceous vegetation that is gath-
ered by workers from forests, grasslands, and agro-
ecosystems. The massive 8 m high chimney mounds
of Macrotermes have classically defined the land-
scape of the African savanna. The Macrotermitinae,
which also include the diverse genera Microtermes
and Odontotermes, range east to the Philippines.
The Nasutitermitinae are a tropicopolitan subfam-
ily of arboreal, mound, and subterranean nesting
termites that are characterized by long-snouted sol-
diers. The snout, or nasus, is the armature from
which a volatile and sticky secretion is exuded as
a  defensive mechanism. Some Nasutitermitinae,
primarily in the genus Nasutitermes, feed on wood
and can be serious pests of structures, while others
are humivores. In some Neotropical genera, e.g.,
Armitermes, the soldiers have both a nasus and long
sickle-shaped mandibles. The subfamily Termitinae
is the most diverse of all the termitid subfamilies.
Included is the genus Cubitermes of sub-Saharan
Africa which is characterized by mushroom-shaped
mounds. The pantropical Termes and related genera
have soldiers with snapping mandibles and arboreal
or rotten log nests. The Amitermes and related
­genera like Microcerotermes occur in the tropics
and subtropics worldwide where they feed on wood,
grasses, and cellulosic debris. Amitermes is subter-
ranean nester in the Nearctic Region while species
from northern Australia build large epigeal mounds.
Microcerotermes tend to be arboreal or subterra-
nean in nesting habit.
Diversity and Distribution
Almost 2,900 termite species in 286 genera have
been described and it is likely that more than 4,000
3740
T Termites (Isoptera)

species may ultimately be recorded. Termites are
found in all zoogeographic regions of the world
and many oceanic islands between latitudes of
about 50°N (southern British Columbia) and 45°S
(southern Chile and South Island, New Zealand)
(Table  9, Figs.  30 and 31). The greatest diversity,
measured by numbers of genera and species, occurs
in the tropical non-arid regions of Africa, Asia, and
the Americas. Some regions show remarkable spe-
ciation by single genera such as the Cryptotermes
from the circum-Caribbean with 25 species, the
Amitermes of Australia with 61 species, the Nasuti­
termes of the Neotropics with 72 species, and
the Odontotermes of tropical Asia with nearly 100
species. Certain genera, such as Reticulitermes
(Rhinotermitidae) and all those of the Termopsi-
dae are characteristic elements of more temperate
climates. In turn, Heterotermes and Neotermes,
respectively, occupy similar niches in the tropics.
Numerous genera are found in all tropical regions
of the world. These include the Neotermes, Glyptot­
ermes, Kalotermes, Procryptotermes, Cryptotermes
(Kalotermitidae), Coptotermes, Heterotermes, and
Prorhinotermes (Rhinotermitidae), and Anoplot­
ermes, Microcerotermes, Amitermes, Termes, and
Nasutitermes (Termitidae).
International trade has facilitated the spread
of “weedy” species from native habitats across nat-
ural barriers to non-native locations worldwide.
Human transport, especially by boat, has facilitated
the spread and establishment of about a dozen
major pest species. Among them are the drywood
termites (Kalotermitidae) Cr. brevis (West Indian
drywood termite), Cr. havilandi, Cr. dudleyi,
Cr.  domesticus, Cr. cynocephalus, and Incisitermes
minor (Western drywood termite). Invasive species
among the lower subterranean termites include
Coptotermes formosanus (Formosan subterranean

Termites (Isoptera), Table 9  Occurrence of termite families and subfamilies of termitidae by zoogeo-
graphic region
Family Region
Austral- Ethiopian Oriental Malagasy Nearctic Neotropi- Palaearctic Papuan
asian cal
Hodotermiti-   X         X  
dae
Kalotermiti- X X X X X X X X
dae
Mastotermi- X              
dae
Rhinotermiti- X X X X X X X X
dae
Serritermiti-           X    
dae
Termopsidae X X X   X X X  
Termitidae X X X X X X X X
Subfamily
Apicotermi-   X X X X X    
tinae
Macrotermi-   X X X        
tinae
Nasutitermi- X X X X X X   X
tinae
 Termites (Isoptera)
T 3741

Nearctic Palearctic
Oriental

Ethiopian Papuan

Neotropical Australasian

Malagasy

Termites (Isoptera), Figure 30  Worldwide occurrence of termites in the major zoogeographic regions.
Unshaded areas (northernmost North America, Eurasia, southernmost South America) do not support
termites.

Papuan i­ magos, and the mandibles of all castes have mod-

Australasian erate to heavy sclerotization. Termite workers and
Palaearctic
imagos have chewing mouthparts, filiform or
moniliform antennae, and a shield-like pronotum
Neotropical behind the head. Soldier mandibles are highly
developed to atrophied and variable in shape
depending on the defenses employed. Important
Ethiopian morphological characters used to classify termites
include wing venation and mandible dentition in
Nearctic
imagos, head capsule and mandible shape in sol-
Malagasy
diers, and gut configuration and mandible denti-
tion in workers. Alates have compound eyes and
ocelli while eyes of other castes are reduced to
Oriental spots or are completely absent. The tarsi of most
Termites (Isoptera), ­Figure 31  Proportion of termites are not well suited for climbing smooth
termite genera found in the eight zoogeographic surfaces. Worker and soldier bodies are usually
regions. light colored but some have darker pigmentation.
Alate bodies and wings range in color from pale
yellow to black. Soldier head capsules range in
termite), Co. gestroi, and Reticulitermes flavipes color from light yellowish to orange, reddish-
(Eastern subterranean termite). Among the Ter- brown, or black. Among the smallest of termite
mitidae, only one species, Nasutitermes costalis, has soldiers is Atlantitermes snyderi (Nasutitermi-
become established in a non-native habitat. tinae) from Trinidad and Guyana with a total
length of 2.5 mm while one of the largest is Zoot­
ermopsis laticeps (Termopsidae) from Arizona and
Morphology Mexico at 22 mm long. The largest termite alates
are the African Macrotermes measuring up to
All termite castes are soft-bodied. Only the soldier 45 mm in length with wings while the smallest is
head-capsules, the heads and bodies of some Serritermes serrifer (Serritermitidae) at 6 mm with
3742
T Termites (Isoptera)

wings. Alates of some Incisitermes and Glyptot­
ermes (Kalotermitidae) and Apicotermitinae are
less than 7 mm long with wings (Figs. 32 and 33).
Life Cycle and Behavior
The inception of a termite colony occurs when a
male and female alate pair after a dispersal flight.
Flights are typically associated with weather condi-
tions superimposed over annual cycles. Rainfall is a
prerequisite for flights by many subterranean
species. The beginning of a rainy season coincides
with flights by many species. After separation from
their wings along specialized suture lines, the repro-
ductive pair runs in tandem until a suitable nesting
site is encountered and selected. Once in the pro-
tected site, e.g., a crevice in a branch, a tree hole, or
underneath a log or stone, the new king and queen
build a small nuptial chamber in which the first eggs
are deposited and hatch into larvae. The first batch
of developing workers and first soldier are cared for
by the reproductives. The workers, usually blind and
composed of both sexes, in turn begin to forage and
feed the royal pair, ­soldiers, and younger sibling lar-
vae. Feeding is accomplished by trophallaxis in which
food is passed mouth-to-mouth from workers to their
dependent nestmates. As foraging and food resources
increase, the size and reproductive output of the queen
grow accordingly. The abdomens of mature queens
in the Rhinotermitidae and ­Termitidae, filled with
egg-swollen ovaries, reach a state of near immobility

Termites (Isoptera), Figure 32  Termite castes. (a) Eggs and larvae of Cryptotermes brevis (Kalotermitidae),
Florida. (b) Soldier (L), worker, nymph, and alate of Amitermes floridensis (­ Termitinae), Florida. (c) King
(top) and queen of Incisitermes minor (Kalotermitidae), California. (d) Queen (center) of Nasutitermes
rippertii (Nasutitermitinae), Bahamas.
 Termites (Isoptera)
T 3743

Termites (Isoptera), Figure 33  Termite soldiers. (a) A. Constrictotermes sp. in amber, ­Dominican Republic.
(b) Cryptotermes brevis (Kalotermitidae), Florida. (c) Rhinotermitidae: ­Coptotermes formosanus (L),
­Heterotermes sp., and Reticulitermes flavipes, Florida. (d) Rhinotermes marginalis ­(Rhinotermitidae) ­major
(L) and minor, Dominican Rep. (e) Macrotermes sp. (Macrotermitinae) major, Kenya. (f) Nasutitermes
­costalis (Nasutitermitinae), Trinindad. (g) Termes hispaniolae (Termitinae), St. Croix. (h) ­Amitermes amicki
­(Termitinae), Aruba. (i) Microcerotermes arboreus (Termitinae), Trinidad. Scale bars = 1 mm.

called physogastry. In the Kalotermitidae, castes
develop along a single line with both soldiers and
alates molting from the immature worker (pseuder-
gate) line. In the higher termites, each caste differen-
tiates along separate developmental pathways after
hatching with the workers becoming sterile adults.
Unlike social Hymenoptera, the king is retained and
periodically fertilizes the queen. After a number of
years when a large crop of workers and soldiers are
present, the colony matures to produce its first batch
of alates, completing the reproductive cycle. Colo-
nies will produce alates for many years after matu-
ration. Termites have some complex symbiotic
­relationships with a community gut-inhabiting
microorganisms. Various bacteria (prokaryotes) and
protists (eukaryotes) are important for cellulose
digestion, nitrogen fixation, and metabolism. Pro-
tists are absent from the Termitidae. Termites also
produce their own cellulytic enzymes. Proctodeal
feeding, the transfer of gut contents via anus to
mouth, facilitates the exchange of gut biota to freshly
molted nestmates (Fig. 34).
Defense Mechanisms and Natural
Enemies
Termites are an ideal food source for other ani-
mals. They are relatively slow moving, soft-bodied,
and rich in fat and protein. Termites passively
3744
T Termites (Isoptera)

Termites (Isoptera), Figure 34  Termite colonies. (a) Zootermopsis angusticollis ­( Termopsidae), California.
(b) Neotermes castaneus (Kalotermitidae), Florida. (c) Anoplotermes n. sp. (­Apicotermitinae), Bahamas.
(d) Nasutitermes costalis, (Nasutitermitinae), Florida. Scale bar = 5 mm.

avoid casual predation because of their cryptic
habits of living in nests, feeding mostly under
cover, and foraging in narrow galleries con-
structed in soil or wood. Most termite species,
however, have a highly specialized soldier force to
defend the colony from specialized invaders,
especially ants. Soldiers of the Kalotermitidae,
Termopsidae, and Hodotermitidae rely solely on
mechanical defenses including powerful crushing
mandibles. Some kalotermitid genera, e.g., Cryp­
totermes and Calcaritermes, have soldiers with
plug-shaped or phragmotic heads used to seal off
nest galleries in wood from ants. Termites in other
families use various combinations of biting, pierc-
ing, or slashing mandibles and repellent, sticky,
and/or toxic chemical secretions which they
exude, brush, or squirt onto ants. In most species
of Nasutitermitinae, soldier mandibles are alto-
gether lacking and instead, the soldiers use their
conical nasi to squirt repellent secretions over
several body lengths.
Many animals, especially birds, bats, rodents,
reptiles, and amphibians opportunistically gorge
themselves on termite alates during dispersal
flights. Some large mammals, such as the aardvark
and aardwolf of Africa, pangolins of the paleotrop-
ics, anteaters of the neotropics, the echidna of Aus-
tralia, and the sloth bear of Asia are specialized
predators of termites and use claws and long
tongues to excavate and feed inside hard nest struc-
tures. Humans, especially in Africa, trap and eat
Macrotermes alates during seasonal dispersal flights
from their mounds.
Some arthropods have evolved an association
with termites that includes living in termite nests.
Those arthropods that have an obligate relationship
with the termite colony are called termitophiles.
Usually the termitophiles rely on termites for both
 Termites (Isoptera)
T 3745

food and shelter. The great majority of termitophiles
are beetles. Some staphylinid beetles even resemble
their hosts. Other termitophile taxa include isopods,
millipedes, phorid flies, and silverfish.
Ecology
Termite nests consist of a network of galleries that
interconnect all colony members and foraging
sites.  Nest types include single-piece wood nests,
(Termopsidae, Kalotermitidae), diffuse subterra-
nean nests (Mastotermitidae, Rhinotermitidae, Ter-
mitidae), hollow tree, log, and stump nests connected
to other food resources via subterranean galleries
(Rhinotermitidae, Termitidae), on-soil (epigeal)
mounds (Hodotermitidae, Rhinotermitidae, Ter-
mitidae), and arboreal nests (Termitidae). Arboreal
nests are constructed of feces while epigeal nests are
composed mostly of soil (Fig.  35). Foraging is the
means by which termite colonies locate and exploit
new food resources. If such resources are abundant,
secondary nest structures may be constructed
nearby. Usually workers, but in some cases soldiers,
follow specific search patterns to locate food. If food
is encountered, the foragers will recruit additional
nestmates to exploit the food source for the colony.
When on exposed surfaces, foraging trails are usu-
ally protected from predators by tube or sheet-like
enclosures made of feces or soil. Recruitment to
food locations is enforced and oriented by chemical
trails released from the sternal gland located on the
ventral surface of the abdomen. Large immovable
food sources may be covered with a protective fecal
or soil sheeting. Smaller food items such as leaves
and grasses are either covered with soil sheeting or

Termites (Isoptera), Figure 35  Termite workings. (a) Fecal pellets of Cryptotermes brevis (Kalotermitidae),
Florida. (b) Exposed damage and aerial nest of Coptotermes formosanus (Rhinotermitidae), Florida. (c) Nest
galleries of Neotermes jouteli (Kalotermitidae) in structural lumber, Florida. (d) Arboreal nest of Nasutitermes
rippertii (Nasutitermitinae), Bahamas. (e) Soil mound of Macrotermes sp. (Macrotermitinae), Ivory Coast.
(f) Foraging tubes of Microcerotermes arboreus (Termitinae), Trinidad.
3746
T Termites (Isoptera)
are subdivided and carried back to the nest for con-
sumption, storage, or fungal gardens. Foraging ter-
ritories for single termite colonies may extend 100 m
or more from the nest. Water, either in food or sub-
strata, can have a profound influence on foraging.
Most termites forage in the direction of moisture
gradients and prefer moist foods and nesting sites.
In savannas and arid lands, surface objects caste heat
shadows that are often investigated by termites for-
aging near the soil surface.
Although cryptic for the most part, the abso-
lute numbers of termites in most tropical and
semitropical forests, deserts, and savannas ranges
from several hundred to thousands of individual
termites per square meter. Colony populations of
termites vary from several hundred (Kalotermiti-
dae) to several million (Rhinotermitidae, Termiti-
dae) individuals.
The biomass of termites often rivals that of
terrestrial vertebrates and ranges from less than
1 g/m3 to over 10 g/m3. Food consumption by ter-
mites can be greater than that of large ungulates.
Termite foods include dry, moist, wet wood, bark,
live wood, leaf litter, soil (humus), live and dried
grasses and herbs, and leaves, lichens, fungi, and
algae. Termites are also significant, albeit, relatively
minor sources of global atmospheric methane and
carbon dioxide. Termites, along with earthworms,
create large turnover and aeration of organic and
mineral content in soil and thus benefit plant
growth and nutrient cycling.
Termites as Pests
About 10% of the termite species worldwide attack
structural lumber, wood products of a broad array
including paper, and agricultural and forage crops.
About 1–2% of all species are major pests and account
for the bulk of the untold billions of dollars in dam-
age caused by termites around the world each year.
The vast majority of termites is a cryptic and essen-
tial component of the environment but has very little
direct impact on humans. Termite control in devel-
oped countries relies on chemical applications in
the  form of specialized residual soil termiticides,
wood preservatives, baits, dusts, and fumigants often
applied by professional pest control operators. People
in developing countries may treat termite infesta-
tions with unsafe or unproven methods or simply
replace damaged and infested wood.
Collecting
Because termites are delicate and can desiccate
rapidly, they should be preserved in alcohol (85%
ethanol is best) while still alive. A hatchet, trowel,
and aspirator are essential collecting tools. Obvi-
ous places to collect termites include nests, forag-
ing tubes, and dead limbs and logs. Subterranean
species also congregate under boulders, stones,
and other surface debris. Herbivore dung, under
which some subterranean termites forage, is
another surface feature to collect from. Small dried
twigs on trees, tree holes, leaf litter, and disturbed
areas such as road, trail sides, or even garbage
dumps are good collecting places. A few species
even infest branches, stems, and roots of live trees
and shrubs. Termite alates that fly at dusk or at
night are attracted to lights where they can be col-
lected by aspirator or net. Because identification
relies heavily on characters of soldiers or imagos,
one should take multiple samples of each caste
present. When alates are not found, one might be
lucky to find a queen, king, or both. Nestmates
from one colony should be combined as a single
sample to confirm their relationship.
 Wood-Attacking Insects
 Termites (Isoptera) in South America
References
Abe T, Bignell DE, Higashi M (eds) (2000) Termites: evolution,
sociality, symbiosis, ecology. Kluwer, Dordrecht, 466 pp
Edwards R, Mill AE (1986) Termites in buildings. Their biol-
ogy and control. Rentokil, East Grinstead, 261 pp
Krishna K, Weesner FM (eds) (1969) Biology of termites, vol. 1.
Academic, New York, 598 pp
Krishna K, Weesner FM (eds) (1970) Biology of termites,
vol. 2. Academic, New York, 643 pp

Pearce MJ (1997) Termites: biology and pest management.
CAB International, New York, 172 pp
Termites (Isoptera) in South
America
Reginaldo Constantino
Universidade de Brasília, Brasília, Brazil
Termites are abundant in most parts of South
America, especially in tropical lowland forests,
savannas and grasslands. In many places, termi-
taria comprise a conspicuous element of the land-
scape. Early European naturalists who traveled in
South America often mentioned termite damage
or termite constructions in their writings. The
South American fauna contains representatives of
the termite families Kalotermitidae, Rhinotermiti-
dae, Serritermidae, Termitidae, and Termopsidae
(Figs. 36 and 37). This fauna comprises 76 genera
(54% endemic) and 422 known species (90%
endemic). Family Serritermitidae, which includes
two genera and three species, is restricted to South
America. Table 10 summarizes the number of genera
and species recorded in each country. The termite
faunas of Brazil, Argentina, Guyana, Chile and
Trinidad are relatively better studied, while the
faunas of Colombia, Ecuador, Paraguay and Suri-
name remain very poorly known. The knowledge
in the remaining countries is intermediate.
Taxonomy
Family Kalotermitidae
This family is represented in South America by
67 species and 11 genera. Genera Eucryptotermes
and Tauritermes are endemic and genus Coma­
termes occurs only in South America and Panama.
The most diverse genera of Kalotermitidae in this
region are Neotermes (16 species), Cryptotermes
(11 native species) and Glyptotermes (10 species).
Four species of Cryptotermes have been introduced
Termites (Isoptera) in South America
T 3747
from other regions as urban pests: C. brevis,
C.  domesticus, C. dudleyi and C. havilandi. How-
ever, only C. brevis is widespread and there is a
single unconfirmed record of C. domesticus from
Trinidad. In general, this family has been little stud-
ied in South America, and there are still many
undescribed species.
Family Rhinotermitidae
There are 21 species of rhinotermitids reported
from South America, belonging to six genera:
Acorhinotermes, Coptotermes, Dolichorhinotermes,
Heterotermes, Reticulitermes and Rhinotermes.
Acorhinotermes is endemic, with only one species,
and Dolichorhinotermes is mostly endemic, with
five species in South America and one in Panama.
Heterotermes is the most important genus, with six
species. Heterotermes tenuis is the most common
species and an important agricultural pest. Despite
the low diversity, this is a very important family
including several major pests. Two species of Rhi-
notermitidae were introduced into South America
and became major urban pests: Coptotermes gestroi
in Brazil and Reticulitermes flavipes in Chile and
Uruguay.
Family Serritermitidae
This family is endemic to South America and
includes two genera and three species. Serritermes
serrifer is endemic to the Cerrado and lives in nests
built by Cornitermes spp., where it feeds on the
dark organic matter of the nest walls. The genus
Glossotermes includes two species, G. oculatus
from Guyana, and G. sulcatus from Brazilian
­Amazonia. Glossotermes feeds on decayed wood.
Family Termitidae
This the largest family and comprises 76% of the
South American species. The so-called nasute
3748
T Termites (Isoptera) in South America

Termites (Isoptera) in South America, Figure 36  (a) South ­American Kalotermitidae (soldiers)
(1) Eucryptotermes wheeleri; (2) Tauritermes vitulus; (3) C
­ omatermes ­perfectus, major soldier;
(4) C. perfectus, minor soldier. (b) South American Rhinotermitidae (­ soldiers) (1) H­ eterotermes l­ ongiceps,
major soldier; (2) H. longiceps, minor soldier; (3) Acorhinotermes s­ ubfusciceps, soldier; (4) R
­ hinotermes
marginalis, major soldier; (5) R. marginalis, minor soldier. (c) S
­ erritermitidae (soldiers) (1) S­ erritermes
serrifer; (2) Glossotermes oculatus. (d) South American Termopsidae, P ­ orotermes quadricollis
(Termopsidae), (1) dorsal and (2) lateral views. (e) Soldiers of South American m ­ andibulate nasutes
(Termitidae: Nasutitermitinae) (1) Labiotermes emersoni; (2) Embiratermes neotenicus; (3) ­Cyrilliotermes
cashassa; (4) Curvitermes odonthognathus; (5) Rhynchotermes nasutissimus;
(6) ­Macuxitermes triceratops (drawings previously published in Zootaxa and used with permission).
 Termites (Isoptera) in South America
T 3749

Termites (Isoptera) in South America, Figure 37  (a) Soldiers of South American nasute termites
(Termitidae: Nasutitermitinae). (1–2) Angularitermes clypeatus; (3) Caetetermes taquarussu; (4) Coatitermes
clevelandi; (5–7) Velocitermes heteropterus, major, intermediate and minor soldiers. (b) Soldiers of South
American Termitinae (Termitidae) (1) Cavitermes tuberosus; (2) Genuotermes spinifer; (3) Orthognathotermes
humilis; (4) Dihoplotermes inusitatus, major soldier; (5) D. inusitatus, minor soldier (6) Neocapritermes
pumilis; (7) Crepititermes verruculosus; (8) Planicapritermes planiceps; (9) Onkotermes brevicorniger;
(10) Cylindrotermes parvignathus (drawings previously published in Zootaxa and used with permission).

t­ ermites (subfamily Nasutitermitinae) are the mound-builders. Some species of Cornitermes,

dominant group, with more than 50% of the spe-
cies. Genus Nasutitermes alone includes 65 South
American species. Most species of this genus are
wood-feeders and live in arboreal carton nests,
but some are subterranean or mound builders.
The other 35 genera of Nasutitermitinae occur
in South America, 22 of them endemic. Among
them, Syntermes is the most diverse, with 23 spe-
cies, including some of the largest known ter-
mites. They are mostly subterranean and feed
on leaf or grass litter. Another important genus
is Cornitermes, with 14 species, most of them
such as C. cumulans, occur in high densities and
dominate the landscape of some grasslands.
Other common and diverse genera of Nasutiter-
mitinae are Armitermes, Embiratermes, Labiot­
ermes and Velocitermes. Subfamily Termitinae is
the second in diversity, with 16 genera (10 endemic)
and 72 species in South America. The most
important genus is Neocapritermes, with 16  spe-
cies. Other common genera are Termes, Microc­
erotermes, Spinitermes, and Orthognathotermes.
Very few South American Termitinae are strict
wood-feeders and many are soil-feeders. A few
3750
T Termites (Isoptera) in South America

Termites (Isoptera) in South America, Table 10  Number of termite genera and species recorded in
South America
Country Kalotermitidae Rhinotermitidae Serritermitidae Termitidae Termopsidae Total
gen. sp. gen. sp. gen. sp. gen. sp. gen. sp. gen. sp.
Argentina 5 10 1 2 – – 23 43 1 1 30 56
Bolivia 3 3 4 6 – – 24 87 – – 31 96
Brazil 7 26 4 12 2 2 54 268 – – 67 308
Chile 3 4 1 1 – – – – 1 1 5 6
Colombia 5 8 3 4 – – 13 26 – – 21 38
Ecuador 2 6 – – – – 8 19 – – 10 27
French – – 5 6 – – 27 52 – – 32 58
Guiana
Guyana 5 14 5 10 1 1 30 69 – – 41 94
Paraguay – – 1 1 – – 21 36 – – 22 37
Peru 3 3 3 4 – – 18 48 – – 24 55
Suriname 1 1 – – – – 6 15 – – 7 16
Trinidad & 6 16 3 4 – – 15 25 – – 24 45
Tobago
Uruguay 2 2 1 1 – – 5 6 – – 8 9
Venezuela 7 11 4 8 – – 20 50 – – 31 69
Total 11 67 6 21 2 3 56 330 1 1 76 422

species have been reported damaging living Family Termopsidae

plants, but in general they are of little economic
importance. Subfamily Apicotermitinae is also
important and diverse, but has been very little
studied. All New World species of this subfamily
are soldierless and most are subterranean, soil-
feeders, and live in diffuse nests in the soil. They
are difficult to collect and identify and have been
neglected by termitologists. The South American
species are classified in five genera: Anoplotermes,
Aparatermes, Grigiotermes, Ruptitermes and Teti­
matermes. Anoplotermes is the most common
and diverse, with more than 25 South American
species, and also occurs in North and Central
America. The other four genera are endemic to
South America and have a few species each. Rup­
titermes feed on leaf litter. These termites are
important in the soil fauna, but are not pests
(Fig. 37 and 38).
Porotermes quadricollis is the only representative
of this family in South America. It occurs only
in the Valdivian forests of Chile and Argentina,
living in humid places. Porotermes quadricollis
may ­damage structural wood, but it is not an
important pest.
Vegetation Zones of South
America and Their Termite Fauna
South America can be divided into distinct vegeta-
tion zones or biomes, each with a more or less
typical termite fauna (Fig. 39). These zones are not
homogeneous and the limits between them are
not precise. There are no termites at higher eleva-
tion in the Andean region.
 Termites (Isoptera) in South America
T 3751

Termites (Isoptera) in South America, Figure 38  (a) Workers of Ruptitermes reconditus (Termitidae:
­Apicotermitinae) feeding on leaf-litter. (b) Nest of Syntermes wheeleri (Termitidae: Nasutitermitinae)
in a pasture. Top right: soldier. (c) Nests of Cornitermes ­cumulans ­( Termitidae: Nasutitermitinae) in a
grassland in the Cerrado region. Bottom right: soldier. (d) A ­ rmitermes teevani (Termitidae:
Nasutitermitinae) in the Amazon forest. (e) Nest of Nasutitermes sp. (Termitidae: ­Nasutitermitinae) in a
grassland in the Amazon region. Top right: soldier. (f) Arboreal nest of C ­ onstrictotermes cyphergaster
(Termitidae: Nasutitermitinae). Top right: C. cyphergaster. Bottom right: Inquilinitermes fur (Termitinae),
an obligatory inquiline termite which feeds on the organic matter of the nest wall. (g) Nest of
Microcerotermes sp. (Termitidae: Nasutitermitinae) in a dry forest (“cerradão”). Bottom right:
soldier.
3752
T Termites (Isoptera) in South America
The largest and most diverse zone is Amazonia,
with nearly 6 million km2, mostly covered by tropi-
cal rain forest. About 250 termite species have
been  recorded in Amazonia. Termite biomass in
Amazon forests has been estimated as about 2 g/m2,
which corresponds to nearly 20% of the total
­animal biomass. As many as 60–70 species can
be  found in a single hectare of upland Amazon
­forest. The genus Nasutitermes is dominant, and
their arboreal nests are conspicuous in the forest.
Mound builders are also common, but most mounds
are relatively small. Many termite genera are endemic
to the Amazon region, including Glossotermes,
Anhangatermes, Caetetermes, Coendutermes, Macux­
itermes, Rotunditermes, Triangularitermes, Corni­
capritermes, and Planicapritermes.
The second largest zone is the Cerrado, a
kind  of savanna vegetation which covers almost
2 million km2. Termites are extremely abundant in
the Cerrado and their mounds comprise a con-
spicuous element of the landscape, reaching den-
sities between 300 and 750 nests/ha. There are
about 150 species recorded in this region, almost
half of them endemic. Litter-feeding termites are
abundant in the Cerrado, and forage on the sur-
face at night in large numbers. Mound-building
Cornitermes can reach impressive densities in
some places and are considered keystone species.
The Atlantic forest originally covered 1.2
­million km2, but has mostly been destroyed and
only about 8% remains. There are approximately
70 termite species recorded from the Atlantic for-
est. The dominant termites are arboreal nesting
Nasutitermes spp. Dry-wood termites (Kaloter-
mitidae) are also abundant. Mounds are much less
common in this region than in Amazonia and
the Cerrado. The termite fauna is more diverse in the
northern part, which shares many species with
the Amazon forests.
The termite fauna of the Caatinga vegetation, a
xerophytic open forest or savanna of northeastern
Brazil, is poorly known. There are little more than
20 species recorded for the entire region, but some
recent surveys indicate the presence of many
undescribed species. Mounds and arboreal nests
are rare, just a few per hectare. The most common
genera are Heterotermes, Nasutitermes, Constricto­
termes and Amitermes.
The Chaco region is a large extension of
­xerophytic open forest of Bolivia, Paraguay and
northern Argentina. Its termite fauna is still little
known, but it seems to be similar to that of the
Cerrado. There are only about 20 termite species
recorded in this region, but it is likely that the total
number is considerably higher, probably including
undescribed taxa.
The Pampa region of Argentina, Uruguay and
southern Brazil is mostly covered by open grass-
land, which is often used as pasture. There are
about 32 species recorded for this region, but many
seem to be restricted to patches of forest. Most of
these species are also present in the Atlantic forest,
Chaco or Cerrado. Typical species of the Pampa
grassland are Cortaritermes fulviceps (=Nasuti­
termes fulviceps), Procornitermes striatus and Termes
saltans.
The Llanos of Venezuela and Colombia is a
tropical grassland situated in the Orinoco basin.
Its termite fauna is poorly known, but it seems to
be composed mainly of mound-building Nasuti­
termes and Velocitermes, which may reach high
densities and feed on grass litter.
The Caribbean zone of Colombia and
­Venezuela includes tropical forest and xerophitic
vegetation. Its termite fauna shares many species
with Central America and the Antilles. The forests
are dominated by arboreal nesting Nasutitermes,
especially N. corniger, N. ephratae and N. acajutlae.
Amitermes foreli, Heterotermes convexinotatus,
Microcerotermes sp., and Obtusitermes sp. are also
common.
The North Pacific region, which includes part
of Colombia and Ecuador, is mostly covered by
tropical forests connected to Central America. Its
termite fauna is little known, but it is also domi-
nated by Nasutitermes spp. and includes at least
one endemic species, Cornitermes acignathus.
Patagonia is the southernmost portion of
South America, including part of Argentina and
Chile. The vegetation of this region is mostly

Termites (Isoptera) in South America, Figure 39  termes spp., which occur in most cities north of
Main v­ egetation zones of South America (above),
and current distribution of two introduced termite
species (Rhinotermitidae) in South America (below).
Termites (Isoptera) in South America
T 3753
grassland. The only termite that occurs in the low-
land of Patagonia is Onkotermes brevicorniger,
with a southern limit near 43°S.
The Valdivian forest zone is located in Chile
and a small part of Argentina. The dominant veg-
etation is temperate rain forest. There are only two
termite species native to this region, both also
endemic: Porotermes quadricollis and Neotermes
chilensis.
Termites as Urban and Structural
Pests in South America
Many termite species live in urban spaces in South
America. More than 20 species have been reported
in some cities. However, few of them can be con-
sidered pests and most live in green spaces such
as gardens and urban parks. The most important
pest species have been introduced from other
regions: Cryptotermes brevis, Cryptotermes dud­
leyi, Cryptotermes havilandi, Coptotermes gestroi,
and ­Reticulitermes flavipes. Crytotermes brevis is
an ubiquitous house termite present in most cities
except in cold places. The southernmost record for
this species is Montevideo (34°51ʹS). Cryptotermes
dudley and C. havilandi have been reported in a
few cities in Brazil and Trinidad. Coptotermes
gestroi (previously also referred to as Coptotermes
havilandi, a synonym), is a very destructive species
native of Southeast Asia, which was introduced in
Brazil in the 1920s. It was first recorded in Rio de
Janeiro in 1923, and today it is present in many
large and important cities. Reticulitermes flavipes,
which is native of North America, was introduced
into Uruguay (Montevideo) in the 1960s and into
Chile in the 1980s, where it became an important
urban pest. Before the introduction of Reticuli­
termes, these regions were relatively free of termite
problems. Among native species, the most impor-
tant urban pests are Nasutitermes spp. and Hetero­
30°S. Nasutitermes corniger is a wood-feeder, arbo-
real nesting termite, which occurs from Mexico to
northern Argentina and is a major pest in many
3754
T Termitidae

cities. Nasutitermes macrocephalus is also present
in many cities and has a similar biology. Heterot­
ermes ssp. are subterranean wood-feeders which
are widespread and may damage wood. There are
six species in South America, the most common of
which is H. tenuis.
Termites as Agricultural Pests in
South America
Constantino R (1998) Catalog of the living termites of the
New World (Insecta: Isoptera). Arq Zool 35:135–231.
Updated online version available at http://www.unb.br/
ib/zoo/docente/constant/catal/
Constantino R (2002) The pest termites of South America:
taxonomy, distribution and status. J Appl Entomol
126:355–365
Constantino R (2002) An illustrated key to Neotropical ter-
mite genera (Insecta: Isoptera) based primarily on sol-
diers. Zootaxa 67:1–40

Several cultivated plants are significantly damaged Termitidae

by termites in South America, especially sugarcane,
upland rice, and eucalyptus. Other plants affected A family of termites (order Isoptera).
include maize, cotton, peanuts, soybean, coffee,  Termites (Isoptera)
cassava, fruit trees and vegetables. Termites may
cause injury to plants by feeding on roots, leaves,
stems, and woody tissue. The most important pests
Termitology
belong to genera Heterotermes, Nasutitermes, Cor­
nitermes, Procornitermes, and Syntermes. Besides The scientific study of termites.
injuring living plants, some termites also build  Termites (Isoptera)
large mounds, which may be a problem for the use
of machinery and reduce the useful soil surface.
Some species of mound-building Cornitermes are
present at high densities in pastures, but their effect Termitophile
is controversial. Farmers dislike their presence but
they do not seem to cause real loss of production. An organism that spends at least part of its life
These are all native species and, unlike the urban cycle with termites.
pests, they are associated with their natural biomes.
Therefore, a plant species may be damaged by
­different termite species in different regions. The fol-
lowing conditions favor termite damage in agricul- Termopsidae
ture: (i) use of exotic crops, which are not resistant
A family of termites (order Isoptera). They also are
nor tolerant to termites; (ii) no-tillage systems,
called primitive dampwood termites or rotten-
because subterranean termite colonies develop
wood termites.
better in undisturbed soil; (iii) non-irrigated crops
 Termites
or crops that are under stress, because vigorous
crops are more tolerant to termites.
 Termites (Isoptera)
Territorial Pheromone
References
Pheromones that serve as markers, delineating
territory used by an insect and causing others of
Araujo RL (1970) Termites of the Neotropical Region. In:
Krishna K, Weesner FM (eds) Biology of termites, vol. 2. the same species to avoid that space.
Academic, New York, 527–576 pp  Pheromones
 Tetracampidae
T 3755

Tertiary Period secretions is the spermatophore, a sac containing

sperm (Fig. 40).
A geologic period extending from about 65 to  Reproduction
2 million years ago. The beginning of the Ceno-
zoic era.
 Geological Time Tethinid Flies
Members of the family Tethinidae (order
Diptera).
Tessaratomidae
 Flies
A family of bugs (order Hemiptera, suborder
Pentamorpha).
 Bugs Tethinidae
A family of flies (order Diptera). They commonly
are known as tethinid flies.
Test  Flies

The covering of scale insects (Hemiptera: various

families). The test is a glandular secretion consist-
ing of wax, polyphenols and proteins. It provides
protection for the nymph and adult that secrete it,
and then for the eggs which the female deposits
within it.
Tetracampidae
A family of wasps (order Hymenoptera).
 Wasps, Ants, Bees, and Sawflies

Ovary
Ovariole
Testicular Follicles Calyx
Lateral oviduct
Tubules in the testes that form sperm. Spermatheca
 Testis Accessory
 Reproduction gland
Median oviduct
Vagina

Testis (pl., Testes)

An assemblage of testicular follicles, each of which

produces sperm (spermatozoa). Each testis emp-
ties into a tube called the vas deferens, the seminal
vesicles, and then into the ejaculatory duct. The
seminal vesicles may be simply an extension of
the  vas deferens, or may be expanded for sperm Testis (pl., Testes), F
­ igure 40 ­Diagram of a male
storage. Associated with the ejaculatory duct is the reproductive s­ ystem as found in Tenebrio
accessory gland, which produces secretions that (Coleoptera) (adapted from Chapman 1998, The
aid in sperm transfer. Most noteworthy of the insects: structure and function).
3756
T Tetratomidae

Tetratomidae Texas Cattle Fever

A family of beetles (order Coleoptera). They This ailment is caused by a tick-transmitted
commonly are known as polypore fungus protozoan.
beetles.  Piroplasmosis
 Beetles

Texas Citrus Mite, Eutetranychus

banksi McGregor (Acari:
Tetrigidae Tetranychidae)
A family of grasshoppers (order Orthoptera). They
These mites are citrus pests in North America.
commonly are known as pygmy grasshoppers or
grouse locusts.
 Grasshoppers, Katydids and Crickets
Thanatosis
This behavior is also called death-feigning, a
Tettigarctidae response to disturbance displayed by some insects
that may help them escape predation. For exam-
A family of bugs (order Hemiptera, suborder ple, when disturbed, beetles may release their
Cicadomorpha). hold on a plant, retract their legs, and drop to the
 Bugs ground. Likewise, chrysidid wasps may roll into a
ball and drop. Thanatosis may be displayed in
addition to or instead of other defensive reac-
Tettigometridae tions such as stridulation, dodging, flight or reflex
bleeding. For example, Crioceris asparagi
A family of bugs (order Hemiptera, suborder (Coleoptera: Chrysomelidae) displays severe
­Fulgoromorpha). All members of the suborder are thanatosis, dropping at even minor disturbance,
referred to as planthoppers whereas its sibling ­species C. duodecimpunctata
 Bugs displays only mild thanatosis but readily
stridulates.

Tettigoniidae Thaumaleidae
A family of katydids (order Orthoptera). They com- A family of flies (order Diptera). They commonly
monly are known as longhorned grasshoppers. are known as solitary midges.
 Grasshoppers, Katydids and Crickets  Flies

Texas Beetles Thaumastellidae

Members of the family Brachypsectridae (order A family of bugs (order Hemiptera, suborder
Coleoptera). Pentamorpha).
Beetles  Bugs
 Thermoregulation in Insects
T 3757

Thaumastocoridae population level. Because cells are units of chemical

A family of bugs (order Hemiptera). They some-
times are called royal palm bugs.
 Bugs
Theileria
An important genus of protozoans causing disease
in animals, and transmitted by ticks.
 Piroplasmosis
Theileriosis
Several related diseases caused by infection with
Theileria protozoans, and transmitted by ticks.
 Piroplasmosis
Thelytokous Parthenogenesis
A type of parthenogenesis wherein females pro-
duce only diploid females from unfertilized eggs.
Theochodaeid Scarab Beetles
Members of the family Ochodaeidae (order
Coleoptera).
 Beetles
Therevidae
A family of flies (order Diptera). They commonly
are known as stiletto flies.
 Flies
Thermoregulation in Insects
Allen Sanborn
Barry University, Miami Shores, FL, USA
Temperature is a physical component of the environ-
ment that affects animals from the subcellular to the
reactions and chemical reactions are temperature
dependent, animal activity is determined by tem-
perature. Temperature has been shown to be an
important influence on all aspects of insect life.
Numerous studies have shown that temperature
influences cellular activity by changing the efficiency
of enzymes, changes the physiological responses of
tissues such as nerves and muscles, alters the rate of
development, determines when species emerge, lim-
its the biogeography of species, and determines
when a species can be active. There are two strategies
for any animal to deal with temperature: they can be
a thermoconformer or a thermoregulator.
A thermoconformer is an animal that permits
its body temperature to fluctuate with, and is about
equal to, environmental temperature. For many
insects, being a thermoconformer is determined by
the size or activity patterns of a species. For exam-
ple, a very small insect will exchange heat with the
environment so rapidly that its body ­temperature
will always approximate ambient temperature, or a
nocturnal insect with a low metabolism may not be
able to elevate body temperature above ambient
conditions. The major problem with being a ther-
moconformer is that enzymes must be able to work
over a greater temperature range than the enzymes
of a thermoregulator. This means that the enzymes
are less efficient at any particular temperature in
the thermoconformer. The benefit to being a ther-
moconformer is that an animal spends no time or
metabolic energy attempting to regulate body
temperature.
A thermoregulator is an animal that maintains
body temperature within a limited range regardless
of changes in ambient temperature. A thermoregu-
lator has the benefit of keeping its enzymes and
physiological systems within the temperature range
where they operate most efficiently. The cost to a
thermoregulator is the use of time or metabolic
energy needed to maintain their body temperature
within a specific temperature range. Thermoregula-
tors can be classified as either ectotherms or endo-
therms based on the source of the energy used in
the  regulation of body temperature (the terms
3758
T Thermoregulation in Insects
poikilotherm or cold-blooded and homeotherm
or  warm-blooded are no longer used due to
ambiguities).
An ectotherm is an animal that uses energy
from the environment to regulate body temperature.
These animals generally are heliotherms, using the
radiant energy of the sun to regulate body tempera-
ture, but there are also thigmotherms, animals that
use the energy of the substrate to regulate body tem-
perature. Ectothermy is a metabolically inexpensive
form of thermoregulation. The major metabolic
expense is the cost of transporting the animal from
sun to shade. The problem with ectothermy is the
animal is still dependent on the environment for a
heat source and thus activity. This problem was
solved by the evolution of endothermy.
An endotherm is an animal that produces
metabolic heat specifically for thermoregulation.
Endotherms have been identified in a wide variety
of insects orders. The source of heat in endother-
mic insects is the flight musculature. Endothermic
insects will increase heat generation through mus-
cular activity to elevate body temperature to the
range necessary for activity. The heating can occur
without flight or wing movements but shivering
can be observed in many night flying moths or
bees at flowers on cool days prior to take-off. The
body temperatures of endothermic insects have
been recorded more than 35°C above ambient
temperature. The use of metabolic energy for ther-
moregulation frees the endotherm from possible
environmental constraints on activity.
Behavior
Thermoregulation can occur through behavioral
and/or physiological mechanisms. The first option
used by any organism to thermoregulate is behav-
ior. Behavioral mechanisms are metabolically
inexpensive and produce immediate results. Very
simple forms of behavioral thermoregulation are
changing body orientations and shuttling between
the sun and shade. Changing body orientation
to the sun is a common behavior that alters the
heat exchange of an insect. When an insect has a
low body temperature, it will sit in an exposed
position to gain radiant heat from the sun. Often
they will orient their body axis perpendicular to
the sun to maximize radiant heating. Conversely,
when an insect has an elevated body temperature,
it will seek a shaded location to decrease the radi-
ant gain and lose heat to the environment. Also,
insects will orient their body parallel to the sun’s
rays when they have an elevated body tempera-
ture, which minimizes the exposed surface area
and radiant heat uptake. One benefit an insect has
in thermoregulating is its small size. The high surface
to volume ratio means that heat exchanges quickly
with the environment and it can take advantage of
small microclimates within the habitat.
Microhabitat selection is another important
behavioral mechanism of thermoregulation. For
example, a desert insect can change the ambient
temperature to which it is exposed by more than
30°C simply by selecting a particular microhabitat
within the environment. Insects will also employ
vertical migration as a means to optimize the ambi-
ent conditions in which they are found. Desert ani-
mals will move away from the ground as ground
temperature (and the boundary layer above the
earth) becomes warmer. Similarly, if it is cool and
windy, insects will move toward the ground in an
effort to find a warmer microclimate. Stilting is a
similar behavior seen in some beetles and grass-
hoppers. When their body temperature is low, the
insects will press their body against the ground to
increase the rate of heat uptake by conduction and
keep their body in the warm boundary layer next
to the ground. When their body temperature
becomes elevated, they will extend their legs, lifting
their body as high as possible above the ground.
These types of behavioral mechanisms are used by
endotherms as well as ectotherms.
Physiology
Physiological mechanisms of thermoregulation can
occur through endothermy, evaporative cooling, or

thermal adaptation. Endothermic insects generally
use the heat generated by the flight musculature to
raise body temperature. The flight musculature is a
good source of heat because it makes up a signifi-
cant portion of body mass and it is a highly aerobic
tissue. Electrical recordings from the muscles of
moths and bees show that the moths shiver (simul-
taneously activating wing elevator and depressor
muscles) to elevate heat production. As the body
temperature of the insect increases, the activity of
the wing elevator and wing depressor muscles
become more out of phase and flight is then initi-
ated. Overheating is prevented by varying the rate
of heat production, through circulatory adapta-
tions that increase heat loss, or through the cessa-
tion of activity. The functional significance of
endothermy has been described for many insect
species and represents the diversity of insect behav-
ior. Endothermy permits such diverse behaviors as
flight, foraging, acoustic activity, dung ball rolling,
maintenance and defense of territories, the use of
habitats unavailable to ectothermic species, preda-
tor avoidance, defense, brood incubation, and hive
temperature regulation.
Evaporative cooling represents a significant
avenue of potential heat loss for animals. The prob-
lem with using evaporative cooling is that there
must be a water source for the animal to replace
water used for cooling. The small size of insects
means they have a relatively small water reservoir
in their bodies, but several evaporative cooling
mechanisms have evolved in insects. Evaporative
cooling by extruding a bubble from the mouth has
been described in moths and bees. A bubble of
saliva is extended, heat is lost as water evaporates,
the bubble is withdrawn back into the mouth to
pick up more heat, and the process is repeated until
the animal is sufficiently cool. This system is very
good at cooling the head but is limited in its ability
to cool the entire body. Locusts evaporatively cool
through an abdominal pumping mechanism while
some caterpillars will spread rectal fluid on their
ventral surface to cool through evaporation.
Another group of insects in which evaporative
cooling has been studied extensively is cicadas.
Thermoregulation in Insects
T 3759
Cicadas can avoid the potential water balance
problems because they feed on xylem fluid. Thus,
the desert cicadas that evaporatively cool have
access to a water source that other animals cannot
use. As a result, desert species like Diceroprocta
apache (Davis) and Okanagodes gracilis Davis can
continue their activity while other animals in the
environment have sought shelter from the extreme
desert heat. In addition, these animals can survive
water loss of over 40% of their total body mass.
Water is evaporated through pores in the cuticle of
the thorax and abdomen of cicadas. The evapora-
tive response of cicadas appears to be energy depen-
dent, as toxins can eliminate the response and the
response can change dramatically by altering ambi-
ent temperature. Evaporative cooling responses are
not universal in insects and appear to be restricted
to desert species or species whose metabolism may
cause dangerous increases in body temperature.
A final physiological mechanism of thermo-
regulation is thermal adaptation. Insects will
adapt their enzymes to work best under particu-
lar thermal conditions. The enzymes will show
optimal activity temperatures that are related to
their environment. In addition, the membrane
composition of insects will change dependent
upon where the insect lives and even with the
daily fluctuations in ambient temperature. These
changes in membrane composition are necessary
to maintain the fluidity of the membrane and,
thus, the integrity of the cell.
Finally, there have been several morphologi-
cal adaptations that assist insects in thermoregu-
lating. Light coloration in hot environments or
dark coloration in cool environments changes the
rate of heating and the maximum temperature
that can be attained by an insect which increases
the time a species can be active in their particular
environment. In fact, some dragonflies undergo
a  temperature dependent color change to alter
the  amount of radiation uptake. Animals from
warmer climates may also reflect more infrared
radiation. There are desert beetles that have highly
convex elytra forming a large subelytral space
that  acts to  decrease heat transfer to the body
3760
T Thermotaxis
while the ­animal is active in the sun. Some desert
tenebrionid beetles have legs that are much ­longer
than their forest relatives. These long legs elevate the
animal above the boundary layer and significantly
increase the time of activity for the species. Many
endothermic and ectothermic species that live in
cool habitats are covered with pile. The pile acts as
insulation to help conserve heat within the body.
References
Heinrich B (ed) (1981) Insect thermoregulation. Wiley,
New York, 328 pp
Heinrich B (1993) The hot-blooded insects: strategies and
mechanisms of thermoregulation. Harvard University
Press, Cambridge, MA, 601 pp
May ML (1979) Insect thermoregulation. Annu Rev Entomol
24:313–349
May ML (1985) Thermoregulation. In: Kerkut GA, Gilbert
LI (eds) Comprehensive insect physiology, biochem-
istry, and pharmacology. New York, Pergamon, pp
507–552
Sanborn AF (1998) Thermal biology of cicadas (Homoptera:
Cicadoidea). Trends Entomol 1:89–104
Sanborn AF, Villet MH, Phillips PK (2004) Endothermy in
African platypleurine cicadas: the influence of body size
and habitat (Hemiptera: Cicadidae: Platypleura spp.).
Physiol Biochem Zool 77:816–823
Thermotaxis
Taxis response with respect to temperature.
Thick-Headed Flies
Members of the family Conopidae (order Diptera).
 Flies
Third Generation Insecticide
Organic insecticides derived from knowledge of
insect’s hormones. By mimicking hormones, the
insecticides provide great selectivity, and are less
disruptive to nontarget organisms.
Thomas, Cyrus
Cyrus Thomas was born at Kingsport, Tennessee,
USA, on July 27, 1825. A lawyer and Lutheran
minister by training, he became one of America’s
foremost systematists and economic entomolo-
gists. Thomas had little formal education and did
not attend college; nevertheless, he learned sci-
ence, mathematics, and practiced law. He sought
an area of science where he could be recognized,
and which could be mastered with little expense
and the materials at hand; entomology met those
needs. While still practicing law, he began to
publish entomology papers. Thomas served with
the Hayden Geological Survey of the territories
of the West and Southwest from 1869 to 1874.
From 1874 to 1876 he taught natural history at
the University of Illinois, and was state entomol-
ogist for Illinois, publishing six annual reports.
Thomas served on the United States Entomolog-
ical Commission for 5  years. One of his most
significant achievements was to author a com-
prehensive treatment of Aphididae, included in
the “Third annual report of the state entomologist
of Illinois on noxious and beneficial insects,” pub-
lished in 1879. He is also remembered for author-
ship of the “Synopsis of the Acrididae of North
America,” published in 1873. In his taxonomic
work he named chiefly aphids and grasshoppers.
Despite a successful career in entomology, he
devoted the last 25 years of his life to archaeologi-
cal and ethnological studies, and became an
authority on the Cherokee, Shawnee, and Maya
people. Thomas died at Washington, DC, on
June 27, 1910 (Fig. 41).
References
Anonymous (1910) Obituary, Cyrus Thomas, Ph.D. Entomol
News 21:387–388
Essig EO (1931) A history of entomology. Macmillan,
New York, 1029 pp
Mallis A (1971) American entomologists. Rutgers University
Press, New Brunswick, NJ, 549 pp

Thomas, Cyrus, Figure 41  Cyrus Thomas.
Thomson, Carl Gustav
Carl Gustav Thomson was born at Skaane, Sweden,
on October 13, 1824. He became a student at Lund
in 1843, and attained his Ph.D. in 1850. Beginning
in 1850 he worked in various capacities at the
Lund Zoological Museum. Thomson tackled dif-
ficult taxonomic problems successfully. He stud-
ied principally Hemiptera, Hymenoptera, and
Coleoptera, but also Diptera. A prolific author, he
published nearly 9,000 pages during his lifetime,
though his work on Diptera is not highly regarded.
He died on September 20, 1899, in Lund, Sweden.
References
Papavero N (1971, 1973) Essays on the history of Neotropical
Dipterology with special reference to collectors
(1750–1905). Museu de Zoologia, Universidade de São
Paulo
Herman LH (2001) Thomson, Carl Gustav. Bull Am Mus Nat
Hist 265:150–151
Thoracic Plate
In caterpillars, the shield-like dorsal covering or
plate on the body segment immediately behind
the head, usually dark in color. Also known as the
cervical shield.
Thorax of Hexapods
T 3761
Thorax
The second or middle of the three major body
regions of insects, and the section bearing wings
(if present) and jointed (true) legs.
 Thorax of Hexapods
Thorax of Hexapods
Severiano F. Gayubo
Universidad de Salamanca, Salamanca, Spain
The arthropods, and particularly the insects, pres-
ent a basic model of body organization constructed
on a metameric base, about which is produced the
process of tagmosis. This process consists of the
grouping of a variable number of segments to
form a suprasegmentary unit called the tagma.
Tagmosis is probably produced to establish a
more operative model in the development of cer-
tain functions important to the life of those ani-
mals. In this case, in the hexapods, the thoracic
tagmata have come about by the grouping of three
segments, called the prothorax, mesothorax and
metathorax, which have developed principally for
locomotion.
The formation of the thorax by three seg-
ments was pointed out in the nineteenth century
by Adouin and later recognized by the majority of
authorities, except by some like Verhoeff, who at
the beginning of the twentieth century considered
that the intersegmentary regions were authentic
segments, whereby five segments would form the
thorax. This theory was rapidly rejected, as it was
demonstrated through comparative studies of
morphology and embryology that the hexapod
thorax consists of only three segments.
Except in the apodous larvae of certain orders,
each thoracic segment carries a pair of legs, and in
addition the winged forms present a pair of wings
on the mesothorax and on the metathorax, with
both segments constituting a functional “sub-
tagma” called the pterothorax. The presence of legs
and wings on the thorax demonstrates that it is a
3762
T Thorax of Hexapods
tagma specialized for locomotory function, devel-
oped and controlled by muscles and ganglia situ-
ated in the thorax itself. It is probable that this
locomotory function originated the differentia-
tion of the thoracic tagma from the other two that
form the body of the hexapods: the head and the
abdomen (Figs. 42–47). The fact that the thorax is
found basically formed in the most primitive
hexapod groups and that it appears perfectly indi-
vidualized in the first stages of ontogenetic devel-
opment makes one think that the differentiation
of this tagma ought to have occurred in early peri-
ods of insect evolution. As much from the struc-
tural as functional point of view, the hexapod
thorax is the most specialized and centralized
tagma if we compare it with analogous tagmata of
other arthropods.
Before beginning a description of the thorax
itself, it is necessary to emphasize the existence of
an anterior region of the body called the neck or
cervical region (Fig. 42), which is of mixed origin:
labial and  prothoracic. The morphological, embryo-
logical, musculature and neurological data demon-
strate that the neck results from the fusion of the
dorsal and ventral parts of the labial and prothoracic
Mesothoracic wing
Mesotergum
Conjuctiva
Protergum
Mesopleural wing process
Mesothoracic spiracle
Mesepisternum
Mesopleural suture
Mesepimeron
Mesothoracic leg process
Coxa of mesothoracic leg
Thorax of Hexapods, Figure 42  Lateral view of a grasshopper head and thorax (Orthoptera:
Romaleidae).
s­ egments, respectively. The cervical sclerites can
be found in the dorsal position (dorsal cervical or
dorso-cervical sclerites), lateral (lateral cervical
or  latero-cervical sclerites) and ventral (ventral
cervical or ventro-cervical sclerites) (Figs.  42
and 43). The lateral cervical sclerites can originate
from the anterior part of the propleura [some
Thysanura (Zygentoma) and the majority of
holometabolous insects] or from the presternal
region (hemimetabolous insects and Coleoptera).
The dorsal cervical sclerites are considered struc-
tures of secondary formation and are united ante-
riorly to the dorsal posterior margin of the occiput.
The same occurs with the ventral ones.
Modern studies of the hexapod thorax began
with the decade of the 1940s, particularly such
authors such as Snodgrass, Weber, Barlet, Carpen-
tier, Francois, La Greca, and Matsuda. As in each
arthropod segment, each hexapod segment presents
a dorsal region called the notum or tergum, another
ventral region named the sternum, and between the
two, a zone that constitutes the pleuron.
The tergal region presents variations in the
number of sclerites and sutures, whose interpreta-
tion in Pterygota should be analyzed with a previous
Mesothoracic wing
1st abdominal tergum
Metatergum
Metapleural wing process
Metapleural suture
Tympanum
1st abdominal spiracle
Metathoracic spiracle
Metathoracic leg process
Metepisternum

Coxa of mesothoracic leg
Trochanitin
Coxa of prothoracic leg
Trochanitin
Prosternal spine
Prosternum
Mesepisternum
Mesosternum
Mesothoracic furcal pit
Prothorax Mesothorax Mesothorax
Thorax of Hexapods, Figure 43  Ventral view of a grasshopper thorax (Orthoptera: Romaleidae).
understanding of what occurs in the Apterygota.
The Protura display a more elaborate tergum
whose homologization with the rest of the hexa-
pods is difficult. In Diplura, Archaeognatha and
primitive Thysanura, an anterior zone exists,
which, according to Matsuda, is named the pseu-
doprescutum. It is separated from the rest of the
tergum by a pseudoprescutoscutal suture that pro-
duces toward the interior a suture named the
pseudophragma. The study of Nicoletia is interest-
ing in that it explains the passage of a primitive
tergum to another evolved in the Pterygota by the
loss of the pseudophragma, which would have no
functional significance on developing a phragma
with the incorporation of an acrotergite; the pseu-
doprescutoscutal suture would be transformed
into the prescutoscutal suture and the pseudopres-
cutum into the prescutum. In the case of Lepisma,
a narrow antenotum (delimited by an antecosta), a
prescutum and a scutum (separated by a prescu-
toscutal suture) and a postnotum united laterally
to the pleuron are differentiated; these sclerites are
already homologous to those of the Pterygota.
The tergal region of the pterothorax of Ptery-
gota (meso and metathorax of winged insects),
presents sclerites delimited by two types of sutures:
Thorax of Hexapods
T 3763
Coxa of metathoracic leg
2nd abdominal tergum
1st abdominal sternum
2nd abdominal sternum
Metathoracic furcal pit
Metasternum
Metepisternum
Abdomen
some homologous to those of the Apterygota and
other, new ones that appear by the wings. The
wings, in addition, produce modifications in the
zone of insertion that fundamentally affect the lat-
eral margins of the tergum (Fig. 44).
Among the sutures homologous to those of
the Apterygota are the antecosta, which delimited
anteriorly a zone that corresponds to the acroterg-
ite and gives rise to a phragma toward the interior.
The prescutoscutal suture is situated behind the
antecosta, delimiting a sclerite named the pres-
cutum, whose lateral zones form the prealar arms.
Among the sutures not homologous to those
of the “Apterygota” stands out the scutoscutellar
suture, which has a sinuous form and reaches the
axillary ligament. This suture separates two scler-
ites, an anterior (scutum) from another posterior
(scutellum). The proper parapsidal lines and the
lateral parapsidal lines are differentiated as intras-
cutal formations; both arising from the prescutos-
cutal suture, the first in a more or less median
position and the second lateral. Two marginal lines
exist within the scutum, one that delimits the ante-
rolateral angle of the scutum, forming the suralare,
a sclerite that includes the anterior and anteme-
dian notal wing processes. The other marginal
3764
T Thorax of Hexapods

cle

e
ir a

e
tur

tur
pis ic sp
m

m
su

su
n
nu

nu

ron
ero
ral
c

ral
ter

ter
Me hora

e
m

leu
pim

im
ple

pis
otu

s
tap

tep
t

rcu
so
se

so

se

se
on
Me

Me

Me

Me

Me

Me

Ce
Pr
Compound eye

Antenna
Frons
Clypeus
Labrum
Labium
Coxa
Trochanter
Femur Metathoracic spiracle
Tibia
Pretarsus
Tarsus

Thorax of Hexapods, Figure 44  Lateral view of a dragonfly (Odonata: Libellulidae).

e
m) git
od le e
eu ter
l
(pr omin pirac
op ab
bd cic s

Scutum
tat m

Praescutum
1s hora
Ce llum
Me hrus
Me notu

Tegula
ute
nc

ta
ta

Prepectus
Sc

Mesothoracic spiracle
Lateral ocellus
Pronotum
Cercus
Propleuron
and cervical sclerites
Mandible
Maxillary palpus
Coxa
Tibia
Me
Me pist
Me pleu um
Me epim l su
Me iste n
se
so ern
s
tep ero ture
tep rn
im um
er
ra

on

Thorax of Hexapods, Figure 45  Lateral view of a sawfly (Hymenoptera: Tenthredinidae).

suture delimits the posterolateral angle of the
scutum, which includes the posterior notal wing
process. In primitive forms of certain orders a ter-
gal fissure is differentiated, which transversally
unites the sides of the scutum at the level of the
anterior or antemedian notal wing process. The
recurrent scutoscutellar suture originates from or
near the center of the posterior margin of the
scutellum, diverging toward the anterior part. The
last sclerite is the postnotum.
 Thorax of Hexapods
T 3765

pim um

lum
ron
llu
m

m
Me ister
Wi scutu

Me cute

tel
Me ase

Me cutu
e
Te ium

cu
b
la

s
tas
tas
tag

so

se
se
so
gu

ng
Pronotum

Me

Me
Pa
Mesothoracic spiracle
Antenna
Compound eye
Maxillary palpus
Galeae 1 2 3 4 5
6
Proepisternum 7
Proepimeron
Coxa
Femur

Me
Co ster
Me
Me
Me iste
Me
Ab ime
Epiphysis

do
xa nu
so

ro
tep
ro
tep
Trochanter 1

mi
23
45

na
rn

ro
ls
m

um

pir
Tarsus

a cle
1
Thorax of Hexapods, Figure 46  Lateral view of a moth (Lepidoptera: Sphingidae).

Metathoracic spiracle
Metapleural suture
Mesonotum Abdominal spiracle I
Mesopleural suture
Mesothoracic spiracle
Pronotum
Proepisternum

Coxa
Trochanter
Femur

Thorax of Hexapods, Figure 47  Lateral view of a scorpion fly (Mecoptera: Panorpidae).

The presence of the wings brings with it a
series of modifications in the lateral margins of
the tergum, differentiating a series of processes,
some of which have been mentioned previously.
Thus, the most anterior process is called the pre-
alar arm or branch, which in the majority of orders
is a prolongation of the prescutum, although in
others like the Hymenoptera it does not exist. Pos-
teriorly, five points of articulation with the wings
are differentiated, which are called notal wing pro-
cesses. From the anterior part to the posterior,
they are the anterior and antemedian (already
mentioned), median, postmedian, and posterior
(also mentioned). In the case where the five pro-
cesses are evident, the first four are joined with the
first axillary sclerite and the last with the third
axillary sclerite.
The notal region of the thorax can present dif-
ferent modifications. Among the most customary
and conspicuous is the prolongation of the meso-
thoracic scutellum, which in certain cases projects
toward the back, on top of the metanotum (for
example, Hemiptera: Scutelleridae), and in other
cases adapts to its conformation.
3766
T Thorax of Hexapods
The sternum, as already mentioned, corre-
sponds to the ventral zone. In generalized Diplura,
Archaeognatha and some Thysanura, five parts or
apotomes are distinguished, which from the ante-
rior to the posterior part are: the presternum, the
basisternum, the furcasternum, the spinasternum
and the poststernum. In principle, the question is
posed of whether the poststernum, instead of rep-
resenting the final portion of the sternum, consti-
tutes the more anterior of the following sternum
that would have been incorporated. In any case, the
different apotomes of the sternum of Aptergygota
have a relatively well-defined position, with the
poststernum being a posterior segmentary struc-
ture, although it does not appear in Ptergygota.
The association of the mentioned sclerites to
the sternum, and the reductions that occur during
evolution toward advanced hexapod groups, are jus-
tified through the study of endosternal formations.
In the Apterygota, a non-cuticular endoskeletal
complex is distinguished, in addition to spinasternal
processes in Diplura and pleural apodemes in
Archaeognatha. Cuticular formations are well de­­
fined in Ptergygota, corresponding to the furca and
the spina.
As a consequence of losses, modifications and
fusions of certain zones, the original division of the
sternum in Pterygota has suffered changes that do
not permit delimiting a clear position from its
apotomes. Thus, the lack of a presterno-basisternal
suture makes the differentiation of a presternum
very difficult. The posternum is lost in the
Pterygota, with this loss affecting the two anterior
apotomes (spinasternum and furcasternum). The
reduction affects, in the first place, the most pos-
terior apotome, which is the spinasternum, being
reduced in certain cases to the spine, as occurs in
the mesosternum of the Orthoptera. The spine is
also lost in more evolved groups like Coleoptera,
Diptera and Hymenoptera, causing reductions to
the furcasternum, which can reach the point of
disappearing. The anterior part of the metaster-
num then occupies its place, shifting toward the
front and situating itself close to the furcal bases.
When this occurs, obliteration is produced on the
ventral border between the meso and metathorax.
This obliteration, which exists in different levels
of development in advanced insects, appears to
directly affect the formation of a functional sub-
tagma, the pterothorax, to which reference has
already been made. In this process, a tendency for
the reduction of the anterior and posterior parts of
the sternum can be observed, always leaving a well-
developed apotome, the basisternum.
All the studies carried out on the origin of the
pleuron demonstrate that this zone of the thorax,
situated between the tergum (or notum) and the
sternum in Archeognatha, Thysanura (Zygentoma)
and Pterygota, consists of a ventral subcoxal area
and another dorsal or pleural area, which have
become indistinguishable because of the scleroti-
zation. In this sense, an evolutionary sequence can
be established from the pleuron of Archaeognatha
to that of the pterothorax, considering the increase
in sclerotization tied to the development of the
wings. In primitive Pterygota like Blattodea, the
sclerotization is not very pronounced, and the scler-
ites that surround the base of the coxa have not
been obliterated, so clear homologies can be estab-
lished with Archaeognatha.
If one considers the pleural formations exist-
ing in the segments of the pterothorax, there are
distinguished, in the first place, a pleural suture
and its corresponding internal costa. In principle,
this suture ought to present a vertical path as is
observed in certain orders like Neuroptera, with a
tendency to present an oblique path toward the
front. The most dorsal part constitutes the pleural
wing process. This suture has been obliterated in
some orders of advanced hemimetabolous insects
like Hemiptera (Heteroptera) while conserved in
secondarily apterous orders like Siphunculata,
Mallophaga and Siphonaptera, and in orders like
Psocoptera. Internally, it is distinguished by way
of a pleural branch that is united to the furca
through a tendinous structure or a muscle. This
pleural suture divides the pleuron into two
regions: an anterior one (episternal region or
episternum) and a posterior one (epimeral region
or epimeron).

Another important suture is the paracoxal,
which divides the pleuron into two rings, an external
anapleural ring, or anapleurite, and an internal
ketapleural ring, or katapleurite. Its presence in
Archaoegnatha indicates that it is a primitive suture.
Considering the two pleural sutures men-
tioned up to now, the pleuron remains divided
into four regions: anepisternum, katepisternum,
anepimeron and katepimeron. In species of cer-
tain orders like Neuroptera, Hemiptera and
Hymenoptera, another suture exists, named the
transepimeral, which is a continuation of the para-
coxal suture in the episternal part. The anepister-
num remains divided by the anapleural suture in
one part dorsally (the anepisternum proper), and
another part ventrally (the preepisternum). In spe-
cies of some orders like Psocoptera, the anapleural
suture is situated more ventrally, with another
suture being differentiated in those cases named
the transepimeral suture, which divides the anepis-
ternum proper into two portions (dorsal and ven-
tral). In primitive orders, beginning from the
anepisternum a small sclerite called the basalare is
differentiated, situated just in front of the pleural
wing process. When the area that surrounds the
basalare is membranous, it can extend posteriorly,
originating a basalar incision that in some orders
like Dermaptera forms the episternal suture.
Behind the pleural wing process the subalar scler-
ite is differentiated, which in reality is a sclerite dif-
ferentiated from the tergum.
Three bridges exist. The prealar bridge or
prealare, which has already been mentioned in
the section dedicated to the tergum. The precoxal
bridge or precoxale, which is formed by the
preepisternum uniting with the basisternum and,
are separated by the pleurosternal suture. This
suture is obvious in Apterygota and in the major-
ity of hemimetabolous Pterygota but does not
exist in certain holometabolous insects, in those
in which the preepisternum and basisternum are
fused. This fusion is not produced in other holo-
metabolous insects, since the preepisternum
extends forward, forming the lateral cervical
sclerite. The third bridge is the postalar bridge or
Thorax of Hexapods
T 3767
postalare, a structure similar to the prealare, but
formed by the connection between the dorsal
margin of the anepimeron and the lateral exten-
sion of the postnotum.
The trochantin is a sclerite differentiated from
the katepisternum, which can present four points of
articulation in Thysanura, one dorsal with the kata-
pleuron and three ventral with the coxa. In Ptergy-
gota, only the anterior coxal-trocantinal articulation
is conserved, with various modifications of the
­trochantin being observed. It can be isolated (pro-
thorax of Psocoptera), partially fused to the katepis-
ternum, conserving the anterior coxal-trocantinal
articulation (eutrochantin), and it can even be
undifferentiated due to the strong sclerotization of
the katepisternum, as occurs in advanced orders.
In the more primitive groups, in the posterior
zone of the katepisternum the sternopleurite is
found, which appears to correspond, according to
Matsuda (1970) to a part of the ventral zone of the
katapleuron. This ventral pleurite in holometabo-
lous insects is not appreciated, and it is possible
that it has been transformed in the ventral articu-
lation process of the coxa.
It can be concluded that the evolution of the
hexapod thorax has been a continual process,
between the thorax of the groups of Apterygota and
that of the Pterygota, a process based on the loss
and modifications of different structural elements.
 Wings of Insects
References
Bitsch J (1994) The morphological groundplan of Hexapoda:
critical review of recent concepts. Ann Soc Entomol Fr
30:103–129
Kristensen NP (1998) The groundplan and basal diversifica-
tion of hexapods. In: Fortney RA, Thomas RH (eds)
Arthropod relationships. Systematics Association, Spe-
cial Volume Series 55. Chapman and Hall, London,
281–293 pp
Manton SM (1977) The arthropoda. Habits, functional mor-
phology and evolution. Clarendon, Oxford
Matsuda R (1970) Morphology and evolution of the insect
thorax. Mem Entomol Soc Can 76:1–431
Snodgrass RE (1952) A textbook of arthropod anatomy.
Comstock, Ithaca, New York
3768
T Thripidae
Thripidae
A family of thrips (order Thysanoptera). They
commonly are known as common thrips.
 Thrips
Thrips-Parasitic Nematodes
Steven Arthurs
Texas A&M University College Station, TX, USA
Several species of nematodes belonging to the genus
Thripinema (=Howardula) (Tylenchida: Allantone-
matidae) are known to naturally parasitize thrips
(Thysanoptera).
Taxonomy, Host Range and
Distribution
The genus Thripinema was erected by Siddiqi in
1986 during a taxonomic revision of the species. To
date, there are five described species of Thripinema:
T. reniraoi, T. aptini, T. nicklewoodi, T. khrustalevi
and T. fuscum. Together these nematodes have been
recovered from twelve species among eight genera
of thrips: Thrips physapus L., T. trehernei Prisner,
T. physopus L., Aptinothrips rufus Gmelin, Franklin­
iella vaccinii Morgan, F. occidentalis Pergade, F. fusca
Hinds, Taeniothrips vaccinophilus, Stenothrips gram­
inium, Catinathrips vaccinophilus, Heliothrips sp.,
Megaluriothrips sp. The biogeographical range of
thrips parasitic nematodes is known to include the
UK, Germany, USA, Canada, Russia and India.
However, the extent of this distribution probably
reflects where surveys have been made. Given
Thripinema spp. hosts include introduced agricul-
tural pest species found worldwide, thrips-parasitic
nematodes are probably widely distributed.
Biology and Life Cycle
Unlike soil-dwelling nematodes of the family Rhab-
ditidae, Thripinema spp. are not mutually associated
with pathogenic bacteria and do not appear to kill
their host. Rather, Thripinema spp. have evolved a
parasitic lifestyle and develop through a single het-
erosexual generation in the live host. Although
infected thrips show no obvious physical signs of
the internal parasite, a consequence of infection is
that embryos do not develop and adult female thrips
are effectively sterile. The cause of host sterility is
unknown, but nematodes may deprive the host of
the protein required for oogenesis or secrete a toxin,
which damages the reproductive organs. Male
thrips are similarly parasitized, although the effect
of infection on male fertility is unknown. During
the infection stage, parasitic female nematodes pen-
etrate a thrips host through intersegmental mem-
branes. Following infection, the female nematode
swells to a sac-like organism in which her repro-
ductive organs become the only visible structure.
Nematode eggs are laid into the host hemocoel.
Upon hatching, the resulting vermiform juveniles
feed on fluids within the thrips’ abdominal cavity.
When mature, both male and female nematode
progeny penetrate into the lumen of the hosts’ gut,
and are continually released for the lifetime of infec-
tive thrips via the anus in the frass or via the ovi-
positor. Relatively little is known about the biology
of Thripinema spp. following its emergence from
the host. However, an intriguing aspect of the life
cycle of the free-living stage is that they appear to
attack their hosts in the above-ground parts of the
plant. While all free-living nematodes require high
humidity, Thripinema spp. appears to exploit the
moist microclimate found within a leaf gall, flower
perianth or developing foliage terminal. Since
mature thrips nematodes exit the host via the anus
or ovipositor, these free-living forms naturally accu-
mulate in and around thrips foraging sites where
defecation and oviposition are pronounced and
where susceptible hosts may be found. Fertilization
of parasitic female nematodes is thought to occur
outside the host despite the fact that survival of this
“free-living” stage may only be a few hours; thus the
cycle is complete.
Thripinema spp. are not currently mass pro-
duced commercially. However, the ability of these
 Thrips (Thysanoptera)
T 3769

nematodes to attack thrips in their preferred feed-
ing sites, areas that are often impenetrable to insec-
ticides and natural enemies, have led several
investigators to speculate that thrips parasitic
nematodes have potential for thrips management
in agriculture.
 Thrips (Thysanoptera)
 Nematode Parasites of Insects
Reference
Loomans AJM, Murai T, Greene ID (1997) Interactions with
hymenopterous parasitoids and parasitic nematodes. In:
Lewis T (ed) Thrips as crop pests. CAB International,
Wallingford, United Kingdom, 355–397 pp
Thrips (Thysanoptera)
Christopher Tipping
Delaware Valley College, Doylestown, PA, USA
The Thysanoptera, thrips, are a diverse insect order
with worldwide distribution (Table  11). There are
approximately 5,800 species described from nine
families. The order is divided into two distinct sub-
orders: Tubulifera and Terebrantia. These two
suborders can be distinguished by the shape of the
last abdominal segment of the adult stage which is
short and pointed in the Terebrantia, or long and
tubular in the Tubulifera. Nearly all described spe-
cies are less than 5 mm in length, and can be yellow,
green, black, or red colored. The name Thysanoptera,
derived from the Greek words, “thysanos” meaning
fringe and “ptera” meaning wings, refers to the two
pairs of slender wings which have few or no veins
and bear a dense fringe of long hairs (Figs. 48 and
49). These hairs allow for greater wing area and
increased flight efficiency. Thrips are thought to be
closely related to Hemiptera and Psocoptera.
Order: Thysanoptera
Suborder: Tubilifera
Family: Phlaeothripidae
Suborder: Terebrantia
Family: Aeolothripidae
Family: Merothripidae
Family: Heterothripidae
Family: Thripidae
Family: Melanthripidae
Family: Uzelothripidae
Family: Adeheterothripidae
Family: Fauriellidae
Thrips are holometabolous insects with com-
plete metamorphosis. Development includes the
egg, 2 larval instars, 2–3 pupal stages and the adult.
The pupal stages do not feed but are capable of
limited movement. Females of terebrantia have a
curved ovipositor which is used to insert eggs into

Thrips (Thysanoptera), Table 11  Some economically important thrips and their distribution
Common and species name Present geographic Native range
distribution
Western flower thrips Frankliniella World-wide; Mediterranean Central California
occidentalis (Pergande) climates, greenhouses in
coolerclimates
Tobacco thrips Frankliniella fusca North America, Mexico, and North America, Mexico, and
(Hinds) Puerto Rico Puerto Rico
Flower thrips Frankliniella tritici Eastern temperate North Eastern temperate North
(Fitch) ­America and Mexico America and Mexico
Melon thrips Thrips palmi Karney Tropics, southern Florida Southeast Asia
Onion thrips Thrips tabaci World-wide Mediterranean climates
(Lindeman)
3770
T Thrips (Thysanoptera)

Thrips (Thysanoptera), Table 11  Some economically important thrips and their distribution (Continued)

Common and species name Present geographic Native range

distribution
Cotton bud thrips Frankliniella World-wide Africa
schultzei (Trybom)
Florida flower thrips Frankliniella Southeastern U.S. Southeastern U.S.
bispinosa (Morgan)
Yellow tea thrips or chillie thrips Southeast Asia, India, Africa, Southeast Asia
Scirtothrips dorsalis Hood Australia
Thrips setosus Moulton No common Japan Japan
name
Frankliniella intonsa (Trybom) No Europe, Russia, Britain, Spain, Europe, Russia, Britain, Spain,
common name Mongolia, Japan, British Columbia, Mongolia, Japan,
USA (Washington state).

plant tissue. The antenna are short with 6–10 seg-

Antenna ments. Thrips have asymmetrical sucking mouth-
parts, possessing only the left mandible (Fig. 50).
Ocellus
Thrips are weak flyers and short directed flights
Pronotum are called thripping. Longer range dispersal is
Mesonotum dependent on wind currents. Within the same
Metanotum species, populations may have individuals with
Femur reduced wings (brachypterous) or no wings (apter-
Tibia ous) depending on environmental conditions such
as density, food quality, and season.
Thrips are important members of the ecosys-
tem as both herbivores and predators. Many
species live in leaf litter or dead wood and feed
nearly exclusively on fungus and will often sup-
Thrips (Thysanoptera), Figure 48  Diagram of a plement their diet with plant pollen. Other thrips
thrips, showing fringed wings. species are gall formers and display primitive
eusocial behavior. Predatory thrips are often
Femur beneficial species in agronomic situations and can
help regulate populations of mites and other
small insect pests including other thrips. Thrips
are often associated with disturbed growth areas
Tibia where large numbers can occur quickly on new
plant growth.
The vast majority of the described species of
Tarsus
Rudimentary claw thrips are herbivorous, with several being destruc-
tive pests of grain crops, fruits, vegetables and
Bladder ornamentals. Certain species are important pests
Thrips (Thysanoptera), Figure 49  Leg of a thrips; of plants grown in greenhouses. Feeding activi-
note that claws are not apparent. ties can result in plant deformities, scarring, loss

Maxilla
Maxillary palpus
Thrips head
Thrips (Thysanoptera), Figure 50  Head of a thrips; note lack of symmetry due to absence of the right
mandible.
of yield, and in some cases, transmission of plant
pathogens. Plant-feeding thrips pierce and suck
juices from the outer layer of cells, causing
stippling, or small scars, on leaves, flowers and
fruit. This feeding damage may result in stunting
of the plant, premature leaf drop and aborted
fruit. Flowers that have been damaged by thrips
feeding may be deformed and fail to open
properly. As many as 90 species of thrips are of
economic importance, including nine species
capable of vectoring plant viruses in the genus
Tospovirus. These viruses are the most important
disease of agronomic crops in many regions of
the world today.
References
Lewis T (1998) Thrips as crop pests. Oxford University Press,
Oxford
Moritz G, Mound L (2001) Thrips ID: pest thrips of the world.
Interactive CD. ACIAR, CSIRO, Collingwood, VIC,
Australia
Stannard LJ (1968) The thrips, or Thysanoptera of Illinois.
Illinois Natural History Survey, Urbana, IL
Thunberg, Carl Peter
T 3771
Antenna
Compound eye
Anterior tentorial pit
Transverse clypeal suture
Clypeus
Labrum
Labium
Labial palpus
Throscidae
A family of beetles (order Coleoptera). They com-
monly are known as false metallic wood-boring
beetles.
 Beetles
Thunberg, Carl Peter
Carl Thunberg was born at Joenkoepping, Prov-
ince of Smaaland, Sweden, on November 11, 1743.
He studied at the University of Uppsala under
Linnaeus, and served as a medical doctor in
South Africa for several years before returning to
Sweden. While in South Africa, he also visited the
Dutch colonies of the Far East, and was able to
investigate the fauna of Ceylon, Java and Japan. He
replaced Carl Linnaeus, Jr., at the University of
Uppsala, and transformed the Royal Gardens
into botanical gardens to honor Linnaeus.
Though known principally as a botanist, Thun-
berg published numerous entomological papers,
3772
T Thuringiensin

including some descriptions. A prolific publisher, Thyrididae

he authored over 150 scientific publications. He
died August 8, 1828. A family of moths (order Lepidoptera). They
commonly are known as picture-winged leaf
moths.
Reference  Picture-Winged Leaf Moths
 Butterflies and Moths
Papavero N (1971, 1973) Essays on the history of Neotropical
Dipterology with special reference to collectors
(1750–1905). Museu de Zoologia, Universidade de São
Paulo
Thysanoptera
An order of insects commonly are known as thrips.
Thuringiensin  Thrips

A soluble, heat-stable beta-exotoxin produced by

Bacillus thuringiensis during the vegetative growth
stage of the bacteria. It has several properties, Thysanura
including insecticidal, feeding deterrent, and tera-
tological effects. An apterygote order of insects. They commonly
 Bacillus thuringiensis are known as silverfish. This order is also known as
Zygentoma.
 Silverfish

Thyatiridae
A family of moths (order Lepidoptera). They com- Thysanuriform Larva
monly are known as false owlet moths.
 False Owlet Moths These are active, flattened, chitinous, free living,
 Butterflies and Moths and principally predaceous larvae. Subcate-
gories of thysanuriform larvae include campo-
deiform, caraboid, triunguloid, naupliiform and
planidiiform.
Thyreocoridae  Campodeiform
 Caraboid
A family of bugs (order Hemiptera). They some-  Triunguloid
times are called negro bugs.  Naupliiform
 Bugs  Planidiiform

Thyretidae Tibia (pl., Tibiae)

A family of moths (order Lepidoptera) also known The section of the insect leg between the femur
as African maiden moths. and the tarsus, usually one of the largest sections
 African Maiden Moths and often bearing spines or spurs (Fig. 51).
 Butterflies and Moths  Legs of Hexapods

Hidden true
segment
4
Coxa 5 at least 10 cases of human paralysis in children aged
Trochanter
Femur
Tibia
1 2 3
4 5
Pretarsus
Tarsus
Tibia (pl., Tibiae), Figure 51  Leg of a beetle
­(Coleoptera: Scarabaeidae) leg showing its
­component parts, and a close-up of one type of
beetle tarsus (foot).
Tick-Borne Encephalitis
Although encephalitis viruses usually are trans-
mitted by mosquitoes, ticks also can transmit some
types.
 Ticks
Tick Paralysis
Tim Lysyk
Agriculture and Agri-Food Canada, Lethbridge,
AB, Canada
Adult ticks inject considerable quantities of saliva
into the hosts during feeding. In some species of
ticks, proteins in the saliva can paralyze the verte-
brate host. At leas t 43 species of ticks have been
reported to cause paralysis, but some records are
doubtful. Paralysis caused by Dermacentor ander­
soni Stiles in North America and Ixodes holocyclus
Neumann in Australia have been studied most
extensively. Dermacentor andersoni, the Rocky
Mountain Wood Tick, causes paralysis in a variety
of hosts including sheep, cattle, horses, dogs and
humans. Paralysis has been reported in various
wildlife species, but this is rare and may be because
affected animals are not readily visible. Wood ticks
can paralyze cattle at doses of 25–83 mg tick per kg
Tick Paralysis
T 3773
1 host body weight, and in sheep at doses of 37–70 mg
tick per kg host. Increasing numbers of ticks per
2
host may increase the incidence of paralysis, but this
3
has only been demonstrated for laboratory animals.
Humans may be paralyzed by a single tick. There are
3–8 years that were caused by single ticks ranging in
weight from 60 to 300 mg.
Although D. andersoni is widely distributed in
western North America, paralysis is mainly associ-
ated with tick populations in a relatively small por-
tion of its range. Paralysis occurs in the interior of
British Columbia, and extends into Idaho, Oregon
and Montana. Paralysis is relatively rare in the prai-
rie regions of its distribution. Even though paralysis
is associated with a particular geographic location,
the ability of individual ticks to cause paralysis var-
ies considerably within areas that paralysis occurs.
Only a small proportion of ticks may be capable of
causing paralysis when placed singly on susceptible
laboratory animals.
Paralysis is typically associated with unmated
female ticks that have fed for at least 4–5 days on the
host. Males do not cause paralysis as they do not
engorge to the extent that females do, and not inject
the copious amounts of saliva into the host that
females do. Female ticks are most likely to cause
paralysis after they have attained a minimum weight
of 40 mg. Although paralysis will occur in humans
of all ages, it is less common in adults compared with
young children as adult humans are more likely to
detect and remove feeding ticks. In cattle, yearlings
are the most susceptible age class as older cattle may
develop immunity, and calves can have ticks removed
by maternal grooming. Paralysis typically occurs
in the early spring when adult ticks are actively
searching for hosts. Cattle placed on pasture in the
early spring are most at risk for paralysis (Fig. 52).
Tick paralysis is a progressive condition and
worsens the longer that ticks are attached. Regard-
less of the host, paralysis begins with loss of hind
limb function (posterior ataxia), proceeding to full
ataxia. The victims lose the ability to stand or sit.
Cattle will become sternally recumbent, and as
paralysis proceeds, will become laterally recumbent.
3774
T Tick Paralysis
Tick Paralysis, Figure 52  Cow immobilized by tick feeding.
If ticks are not removed, death due to respiratory
failure will occur. Prompt removal of ticks from
paralyzed animals can result in rapid recovery, even
as the ticks are being removed. The earlier ticks
are removed, the more rapid is the recovery. Paralysis
is most common in cattle. Several thousand cattle
have been reported paralyzed, with some occur-
rences involving entire herds of over 100 head.
Death rates vary, but may range upwards of over
20–25% of an affected herd. Several hundred cases
of human paralysis have occurred in the interior of
British Columbia since the early 1900s.
Tick paralysis is believed to be caused by a
toxin produced in the salivary glands and released
during feeding. Injection of artificially collected
saliva can cause paralysis. The rapid recovery of
the host following tick removal suggests that
infectious agents are not directly involved.
Increasing incidence of paralysis with increasing
doses of ticks further suggests that a toxin is
involved. To date, the nature and identity of the
toxin has not been identified. The mode of action
of the toxin is not well understood, but is associ-
ated with reduced nerve conduction, possibly by
attacking the nerve membrane. It is thought to
involve motor polyneuropathies, with only lim-
ited participation of the afferent pathways.
Paralysis caused by Ixodes holocyclus is similar
in some respects to that caused by D. andersoni,
and markedly different in others. Ixodes holocyclus
is among the most virulent of paralyzing ticks, and
is common in moist areas along the eastern coast
of Australia. Approximately 10 females can para-
lyze young calves 30–40  kg in weight, and 20–25
can paralyze calves 80–160 kg. The main hosts of
the tick are various species of bandicoots, but the
tick will cause paralysis in dogs, cats, domestic live-
stock and humans. Paralysis is associated with
feeding by the adult females, and these are active
from June through December. Toxins are secreted
by the tick after the third day of attachment, and
paralysis occurs after feeding for 4–5 days. Varia-
tion in virulence has not been found as has with
D. andersoni. Symptoms are similar to those caused
by D. andersoni, including an ascending flaccid
paralysis, however, the victim may become acutely
ill, and vomiting may occur. The symptoms may
worsen following removal of the tick, and symp-
tomatic treatment or administration of a canine
hyperimmune antiserum. Immunity to paralysis

can develop through previous exposure, through
mother’s milk, or by immunization.
The toxin produced by Ixodes holocyclus
appears to have a different mode of action ­compared
to other tick paralysis toxins, and may act to inhibit
acetylcholine release at the neuromuscular junc-
tion. Considerable research has been conducted to
isolate and identify the toxin produced by Ixodes
holocyclus. Initial work suggested the toxin was a
40–80 kDa protein, but more recent studies suggest
the toxin is of a lower molecular weight and related
to scorpion neurotoxins. Toxins from other tick
species, such as Rhipicephalus evertsi evertsi, are
approximately 68 kDa.
The evolutionary significance of the toxins
remains unclear. Toxins may have evolved to
reduce mortality caused by host grooming, may
have been con-served from an ancestor that used
venom to immobilize prey, or may have other
functions associated with tick-host interactions
and paralysis is accidental.
 Ticks
References
Gothe R (1981) Tick toxicoses of cattle. In: Ristic M, McIntyre I
(eds) Diseases of cattle in the tropics. Current topics in
veterinary medicine and animal science, vol. 6. Marti-
nus Nijhoff, The Hague, 587–598 pp
Gothe R, Kunze K, Hoogstraal H (1979) The mechanisms of
pathogenicity in the tick paralyses. J Med Entomol
16:357–369
Gregson JD (1973) Tick paralysis: an appraisal of natural and
experimental data. Monograph No. 9. Agriculture Canada
Stone BF, Doube BM, Binnington KC (1979) Toxins of
the  Australian paralysis tick Ixodes holocyclus. In:
Rodriguez JG (ed) Recent advances in acarology, vol. 1.
Academic, New York, 347–356 pp
Wilkinson PR (1982) Tick paralysis. In: Steele JH, Hillyer GV,
Hopla CE (eds) CRC handbook series in zoonoses.
CRC, Boca Raton, 275–282 pp
Ticks (Acari: Ixodida)
Lewis B. Coons, Marjorie Rothschild
The University of Memphis, Memphis, TN, USA
Ticks (Acari: Ixodida)
T 3775
Ticks are obligatory blood-feeding ectoparasites
of reptiles, birds and mammals. They belong to the
subclass Acari, order Ixodida. Ticks are the largest
mites, ranging in length from about 2  mm to
30 mm depending on the species and life stage. All
ticks pass through an egg and three active stages, a
six-legged larva also known as a “seed tick,” an
eight-legged nymph and an adult. Each active
stage molts into the next and, with few exceptions,
each requires a blood meal before molting. The
complex relationship of the tick to its vertebrate
host that may date back to the dinosaurs, and the
need for the tick to obtain a blood meal, have been
the principle driving forces for their evolution.
Classification of Ticks: The Order
Ixodida
About 850 species of ticks are arranged in three
families:
Class: Arachnida
Order: Ixodida
Family: Argasidae
Subfamily: Argasinae
Subfamily: Ornithodorinae
Subfamily: Otobinae
Subfamily: Antricolinae
Subfamily: Nothoaspinae
Family: Nuttallielinae
Family: Ixodidae
Subfamily: Ixodinae
Subfamily: Rhipicephalinae
Subfamily: Amblyomminae
Subfamily: Haemaphysalinae
Subfamily: Hyalomminae
Argasidae
The Argasidae with some 159 species is divided
into five subfamilies, each with one genus: Argasi-
nae (Argas with seven subgenera and 56 species),
Ornithodorinae (Ornithodoros with 100 species),
Otobinae (Otobius with two species), Antricolinae
(Antricola with about eight species), and Notho-
aspinae (Nothoaspis with one species) (Fig. 53).
3776
T Ticks (Acari: Ixodida)
Ticks (Acari: Ixodida), Figure 53  Adult of Argas persicus, the blue bug. The left side is a ventral view and the
right side is a dorsal view (from Marquardt et al. 2000, used with permission of Harcourt Academic Press).
Nuttallielidae
The Nuttallielidae has a single species Nuttalliella
namaqua known only from females and nymphs.
It is found in South Africa and Tanzania where it is
believed to be a parasite on small mammals such
as rodents and the rock hyrax. What little is known
about this species suggests that it has many char-
acteristics in common with both of the other two
tick families.
Ixodidae
The Ixodidae, with some 650 species, is divided
into five subfamilies. The subfamilies are grouped
into two divisions, the Prostriatia and the Metas-
triata. The Prostriata has a single subfamily, the
Ixodinae, with one genus, Ixodes, and some 245
species. The Metastriata contains four subfami-
lies. The largest of these, the Rhipicephalinae,
has eight genera, Dermacentor with 30 species,
Cosmiomma with one species, Nosomma with
one species, Rhipicephalus with 70 species,
Anomalohimalaya with three species, Rhipicen­
tor with two species, Boophilus with five species,
and Margaropus with five species. The other
three subfamilies are smaller: Amblyomminae
with two genera, Amblyomma with 102 species,
and Aponomma with 24 species; Haemaphysali-
nae has one genus, Haemaphysalis with 155 spe-
cies, and Hyalomminae has one genus, Hyalomma
with 30 species.
External Morphology of Ticks
Ticks have a typical acarine body, but one that has
been adapted to an ectoparasitic life. The body is
divided into a movable head region, the capitulum
or gnathosoma and the idiosoma, which makes up
the rest of the body. There is no visible segmenta-
tion. The small dorso-ventrally flattened body of
unfed ticks makes it difficult for the host to remove
them (Fig. 54).
The capitulum, or gnathosoma, consists of
the basis capituli, the palps, and the chelicerae,
and the hypostome. The gnathosoma is anteriorly
situated in the larvae of soft ticks and in all instars
of hard ticks. In postlarval instars of soft ticks, it
is not visible from above, being mostly hidden by
the overlapping anterior part of the idiosoma. The
gnathosoma is connected with the idiosoma by a
cavity, the emargination in hard ticks, or the cam-
erostome in soft ticks. The connection is via a soft
articulation membrane that allows the gnatho-
soma to be flexed or extended (Figs. 55 and 56).
The basis capituli, an integumental ring that
encircles the mouthparts, contains the shafts of
the chelicerae, the salivary ducts and the pharynx.
Its dorsum bears the area porosa in female hard
ticks. The paired palps have four segments, and
resemble legs in soft ticks, but have a more flat-
tened shape than legs in hard ticks. In soft ticks,
the terminal segment is normal in appearance but,
in hard ticks, it is much shorter and can be retracted
or protruded. The palps bear several types of seti-
form sensilla.
 Ticks (Acari: Ixodida)
T 3777

Hypothetical male and female ixodidae (Hard ticks)

with key characteristics labeled

Palpus Hypostome
Segment 4 Segment 4
Leg I Segment 3
Segment 2 Segment 3
Segment 1 Segment 2
Scapula Segment 1
Leg II
Basis capituli Basis capituli
Cornu
Cervical groove Genital aperature
Eye Internal shield
Trochanter
Lateral groove Genital groove
Leg III Ornate markings External spur
Spiracular Anus
Scutum plate
Dorsal prolongation Accessory shield
Femur Adanal shield
Festoon
Leg IV Tibia
Tarsus
Pulvillus
Claw
Metatarsus

Dorsum of male Venter of male

Porose area Coxa I

Cornu Internal spur
External spur
Punctations Coxa II
Scutum Coxa III
Ornate marking
Coxa IV
Anus
Spiracular plate
Anal groove

Dorsum of female Venter of female

Ticks (Acari: Ixodida), Figure 54  Diagrams illustrating the external anatomy of a hypothetical male and
female ixodid tick with key characteristics labeled. Note that the chelicerae have been removed (compare
to following figure) (from Marquardt et al. 2000, used with permission of Harcourt Academic Press).

The paired two-segmented chelicerae have
been modified as cutting organs that are unique
among the mites. Chelicerae consist of a bulbous
base, an elongated shaft, and the cutting digits, or
articles. In many species, a cheliceral hood covers
the articles. The cutting edges of the internal and
external articles are laterally oriented. The internal
article is moved from side to side by the tendons
attached to the powerful muscle masses in the
bulbous cheliceral bases. The external article
moves with it. This movement is used by the tick
to tear into the hosts skin prior to embedding its
mouthparts. Sensory structures occur on the
external and internal articles.
3778
T Ticks (Acari: Ixodida)
IV
Cheliceral sheath
III
Segments of the pedipalp
II
Cheliceral sheath
Basis capituli
First coxa
Ticks (Acari: Ixodida), Figure 55  Capitulum and mouthparts of a tick (from Marquardt et al. 2000, used
with permission of Harcourt Academic Press).
The hyopostome, located on the ventral gna-
thosoma, is a dorso-ventrally flattened protrusion
with recurved teeth on its ventral side, and a pre-
oral canal on its dorsal side. The preoral canal leads
to the mouth and the muscular pharynx. The
action of the pharynx sucks up blood through the
preoral canal. The preoral canal and the space
between the dorsal surface of the hypostome and
the ventral surfaces of the chelicerae are the com-
mon channels for blood intake and saliva outflow.
In hard ticks, the intake of blood alternates with
saliva flow with some pauses between the two
events. At the junction of the preoral canal with
the pharyngeal valve, a short and pointed flap-like
labrum exists.
The mouthparts of hard ticks vary in length.
Those species with longer mouthparts are referred
Dorsal view
Teeth of the chelicera
Basis capituli
Ventral view
Teeth
Hypostome
First coxa
to as longirostrate, and those with smaller mouth-
parts as brevirostrate.
The idiosoma is divided into the podosoma
which bears the walking legs and, in adults, the
genital opening, and the opisthosoma that lies
posterior to legs IV and bears the spiracular plate
and the anal opening. Some hard ticks have pat-
terns in the cuticle, usually in the scutum or the
dorum of the basis capituli, which are referred to
as markings or ornamentations.
The idiosoma of soft ticks is tough and leath-
ery and, with the exception of some larval forms,
has no sclerotized plates or shields. Eyes, when
present, are found laterally above the fourth pair
of legs in soft ticks and, in hard ticks, on the lateral
surface of the scutum. The cuticle of all Argasidae,
but Argas, have tiny ridges (mammillae) and

a b c d
Ticks (Acari: Ixodida), Figure 56  Capituli of the genera of hard ticks, family Ixodidae. (a) Rhipicephalus;
(b) Haemaphysalis; (c) Boophilus; (d) Dermacentor; (e) Ixodes; (f) Hyalomma; (g) Amblyomma (from
Marquardt et al. 2000, used with permission of Harcourt Academic Press).
depressions (discs) to which muscles attach. Some
hard ticks have grooves, or festoons, along por-
tions of the ventral posterior body margin.
The idiosoma of hard ticks bears several scle-
rotized plates or shields. In female hard ticks, an
anterior shield, the scutum, occurs on the dorsum.
The alloscutum covers the remainder of the idio-
soma. The alloscutum is not sclerotized and is
folded in unfed ticks. This allows the alloscutum
to greatly enlarge during feeding to accommodate
the large blood meal. Male hard ticks take small
blood meals, the alloscutum is lacking, and the
scutum covers the whole dorsum. Various shields
such as the accessory shield and adanal shield
occur only in male hard ticks. Sexual dimorphism
is well developed in hard ticks. Soft ticks are so-
called because they lack the scutum. There is little
visible external difference between males and
females in soft ticks, except the shape of the genital
opening.
The podosoma contains the walking legs.
Each leg is divided into six segments or podom-
eres, from proximal to distal: the coxa, trochanter,
femur, tibia, metatarsus and tarsus. Muscles,
hydrostatic pressure from hemolymph and bend-
ing stresses are used to produce movement. Mus-
cles and tendons run between the joints. Joints
between the body and the legs, between the
podomeres, and between the tarsus and the apo-
tele allow movement of the legs. The direction of
movement is determined by the type of articula-
tion, the extent of the flexible arthrodial mem-
branes, and the insertion points of the muscles
and the position of the tendons. The tarsus of each
Ticks (Acari: Ixodida)
T 3779
e f g
leg has an apotele, or pretarsus, which includes
the claws and, in hard ticks, only the pulvillus. The
pulvillus is a flap-like structure with a central
lumen containing lipid compounds that are
secreted onto the surface and may act as an adhe-
sive that allows the tick to walk on almost any
surface and to move vertically.
The opisthosoma contains the opening of the
respiratory tract and the anus. Adult and nymphal
ticks respire through tracheae, most larvae and all
eggs respire through their integument. However,
the larvae of some species of Argas and Orni­
thodoros have a simple tracheal system that opens
through minute apertures between coxae I and II.
Tracheae in other ticks open to the outside through
a complex structure, the stigmata (or spiracle).
This is associated with a sclerotized elevated region
of the cuticle, the spiracular plate. A pair of spi-
racular plates occur near coxae IV in all adult and
nymphal ticks. The spiracles of soft and hard ticks
are similar, although the spiracular plate is often
less conspicuous in the Argasidae. The exchange of
gases occur through pores that perforate the spi-
racular plate and lead to a labyrinth of chambers
that in turn lead to the trachea. Spiracular pores
help prevent dust and other debris from entering
the trachea. Pillars of cuticle (pedicles) run from
the floor to the top of these chambers. A valve-like
structure, the atrial valve, occurs beneath the spi-
racular plate. High carbon dioxide concentrations
stimulate the atrial valve to open.
The tick respiratory system is designed, in
part, to conserve water. Ticks that live in arid
­habitats have the most efficient spiracles to reduce
3780
T Ticks (Acari: Ixodida)

water loss. The pores and the elaborate labyrinth

system beneath the sieve plate function to reduce
water transpiration during respiration. When
stigmata remain open, loss of water increases,
which explains why a discontinuous ventilation
cycle exists in hard ticks. A discontinuous ventila-
tion cycle coupled with a low metabolic rate is
probably the reason unfed adults can survive long
periods of starvation and desiccation off the host.
Engorged hard ticks ventilate continuously with
little spiracular control.

Host Seeking and Tick Feeding

Most ticks are ambushers, seeking their hosts in a

passive manner. The exceptions are some species
of Hyalomma, which are active hunters that will
crawl several meters toward a host after perceiv-
ing their odors and movements. Ticks have
evolved specialized structures to sense the pres-
ence of a host. The most important of these is
Haller’s organ, a specialized area of the dorsal sur-
face of the first pair of legs found on all ticks.
Haller’s organ, along with other setae, can sense
CO2, ammonia found in sweat and urine, hydro-
gen sulfide found in the breath, belches or flatu-
lence, nearby movement, and a rapid rise in
temperature. When seeking a host ticks extend
their first pair of legs and assume a questing posi-
tion (Fig. 57). Ticks process sensory information
through their central nervous system, or syngan-
glion, which is described in the section on mites.
Host seeking behavior is rhythmic in some ticks.
Rhipicephalus appendiculatus, which mostly
infests cattle, has a bimodal diurnal periodicity,
that is, a peak of host seeking that occurs twice
during each day. The peaks shift depending on the
time of year.
Once on the host, a tick selects a feeding site
then embeds its mouthparts into the skin. First,
the tick uses its legs to elevate the body to a sharp
angle, then it cuts the skin with its chelicerae
and inserts the hypostome and chelicerae into
the wound using a rocking motion of the body.
Ticks (Acari: Ixodida), Figure 57  Female Ixodes
persulcatus in questing posture, waving its first
pair of legs (from Marquardt et al. 2000, used with
permission of Harcourt Academic Press).
The palps are splayed out on the surface of the
hosts skin. Ticks are pool feeders, that is, they feed
on blood that flows into a wound site in the case of
soft ticks, or a feeding lesion in the case of hard
ticks. Soft ticks create wounds by using their cheli-
cerae to tear into small blood vessels and capillar-
ies. Soft ticks are rapid feeders compared to hard
ticks, finishing their blood meal in 20–60  min
depending on the species. Exceptions to this rapid
feeding are the larvae of many species of Argas
and Ornithodoros, which require several days to
complete a blood meal.
After insertion of the hypostome, all hard
ticks, with the exception of some species of Ixodes,
secrete a substance from their salivary glands that
hardens into a cone-like structure. This “cement”

cone covers the mouthparts but not the palps. This
cone has multiple functions. It cements the tick
onto the host. It creates a feeding tube that make
the mouthparts more effective at taking up blood.
It limits contact with the host to a small opening at
the apex of the cone. Hard ticks do not create a
wound at the feeding site similar to that of soft
ticks. Instead, a specialized feeding lesion develops
beneath the cement cone. This lesion does not
develop without the host’s initial inflammatory
reaction. Both the bite wound of soft ticks, and the
feeding lesion of hard ticks are maintained by
saliva from the tick’s salivary glands (Fig. 58).
The paired salivary glands of ticks are com-
plex, multifunctional organs that are very impor-
tant in off-host physiology as well as feeding.
Salivary glands consist of grape-like acini con-
nected to a system of salivary ducts. The ducts lead
to a preoral cavity, the salivarium, which is isolated
by a trap door mechanism. When the salivarium is
opened, saliva flows into the host; when it is closed,
blood is sucked into the digestive system by the
Bc
P of preventing platelet activation at the tick feed-
SC
EP
Ch
C platelet activation that include at least five different
D
He
CD
FL Hy
Ticks (Acari: Ixodida), Figure 58  Diagram of the
feeding lesion that develops beneath the attached
female ixodid. The lesion is filled with blood and
inflammatory infiltrates. BC, basis capituli; C,
cement cone; CD, cheliceral digit; Ch, outer
cheliceral sheath; D, dermis of host skin; EP,
epidermis of host skin; FL, feeding lesion; He,
hemorrhage; Hy, hypostome; P, palps; SC, stratum
corneum of host skin (from Coons and Alberti
1999, used with permission of Wiley).
Ticks (Acari: Ixodida)
T 3781
action of the muscular pharynx. Both soft and
hard ticks alternate blood sucking with saliva pro-
duction. Acini contain specialized cells that pro-
duce the many bioactive compounds found in the
saliva. One type of acini produces a salt that takes
up atmospheric water when secreted on the
mouthparts of nonfeeding ticks. This is used to
replenish the water lost during the off host part of
the tick life cycle. The salivary glands of hard ticks
undergo a great developmental change during
feeding to become organs of osmoregulation that
return excess water and ions from the bloodmeal
back into the host via the saliva. Tick salivary
glands are innervated with a catecholaminergic-
like synapse.
Tick saliva compounds have anti-hemostatic,
anti-inflammatory and immunosuppressant prop-
erties. These compounds help the tick to obtain an
adequate bloodmeal and avoid rejection by the
host.
Antihemostatic compounds in tick saliva
inhibit platelet adhesion, activation and aggregation,
blood coagulation, and vasoconstriction. Some
compounds promote vasodilation. The importance
ing site is apparent by the number of compounds
that Ornithodoros moubata has evolved to prevent
compounds. Moubatin, a 17 kDa polypeptide, Tick
Adhesion Inhibitor, a 15  kDa polypeptide, and
disagregin, a 6  kDA peptide, prevent exposed
collagen on damaged blood vessel walls from acti-
vating platelets. Disagregin also prevents the for-
mation of fibrinogen and ADP. Apyrase, an enzyme
that hydrolyzes adenosine diphosphate (ADP) is
also present in the saliva of Ornithodoros moubata.
ADP can activate platelets and is released from
injured cells and activated platelets. Apyrase is
found in the saliva of a wide variety of ticks in
addition to O. moubata. An exception is Amby­
lomma americanum, which has no apyrase. In this
tick, inhibition of platelet aggregation is carried
out by high concentrations of prostaglandins
(PGE2 PGD2). Ixodes scapularis saliva also con-
tains high levels of prostaglandins (PGI2, PGE2).
3782
T Ticks (Acari: Ixodida)
The prostaglandins are the most powerful known
inhibitor of platelet aggregation known and can
actually cause desegregation of aggregated plate-
lets. Prostaglandins, PGI2, PGE2 and PG2, are also
potent vasodilators that can help increase blood
flow during feeding.
Blood coagulation is initiated by either the
extrinsic system or the intrinsic system. The extrin-
sic system is initiated by exposure of blood to sub-
endothelial components such as collagen, which
then activates tissue factor. The intrinsic system is
initiated by the release of tissue thromboplastin
from injured cells. Each system leads to a common
reaction that involves factor Xa (the Stuart factor),
catalyzing prothrombin to thrombin. Thrombin
catalyzes the conversion of soluble fibrinogen to
an insoluble fibrin mesh that forms a blood clot.
Most tick anticoagulants inhibit either the serine
protease factor Xa, or thrombin. An exception to
this is a compound from Dermacentor andersoni
saliva that inhibits the serine protease VIIa, and a
compound from Dermacentor variabilis salivary
glands that inhibits tissue factor.
The vertebrate host’s inflammatory and
immune systems are closely linked and many anti-
inflammatory compounds of tick saliva also inhibit
or suppress the host’s immune system. Compounds
in tick saliva can inhibit both the innate and the
acquired immune response of the vertebrate host.
Innate immune responses include those mounted
by the host immediately without the requirement
of previous contact with the foreign invader. These
include the process of inflammation and a series
of soluble proteins (complement) that can destroy
or damage foreign objects. Other components of
the innate response are natural killer cells and the
interferons. Studies have shown that some factors
in tick saliva can inhibit complement, suppress the
activity of natural killer cells and also suppress
the  anti-viral action of some interferons. This
includes the production of nitric oxide by host
macrophages, which is used to destroy foreign
objects. The acquired immune response is highly
specific and requires prior exposure to the foreign
object which must be antigenic. Acquired immunity
can be divided into humoral immunity carried out
by antibodies, which are bloodborne proteins of
the Immunogloblin superfamily manufactured by
B lymphocytes or B cells, and cell-mediated immu-
nity, which is carried out by T lymphocytes or T
cells. Compounds in tick saliva suppress antibody
production and responses of host T lymphocytes.
The cement cone, which is known to be antigenic,
binds host immune response factor IgG. This may
act as a molecular mask to prevent recognition of
the cement cone as a foreign object by the host’s
acquired immune response. A novel family of
immunoglobulin-binding proteins (IGBPs) may
also play an important role in evading the host’s
acquired immune response. IGBPs have been
found in all ixodid species studied to date, and
have been isolated from both saliva and hemo-
lymph. IGBPs secreted by males co-feeding with
their mates have been shown to enhance the
female’s ability to complete her blood meal and lay
a larger clutch of eggs.
After formation of the feeding lesion early
in feeding, hard ticks suppress the host’s inflam-
matory response. The high levels of prostaglan-
dins in tick saliva inhibit neutrophil function
and suppress the release of inflammatory media-
tors from mast cells. Bradykinin, an inflamma-
tory mediator of vertebrates that potentiates
pain, is deactivated by the saliva of Ixodes scapu­
laris. Histamine binding compounds and host
immunoglobulin binding compounds have been
identified in tick saliva. Histamine is an impor-
tant mediator of the inflammatory response, and
immunoglobulins mediate the host’s immune
response.
Tick drop-off from the host after feeding is
not uniform with respect to day/night cycles.
Completion of feeding at certain times has evolved
to ensure that ticks drop off into habitats that are
the most advantageous for their reproduction and
for the availability of hosts for the next life stage.
Photoperiod is the most common external factor
that affects drop-off timing. Individual ticks of the
same species feeding on the same host may finish
at different times.

Physiology of Ticks
Digestive System
Ticks have a typical acarine digestive system consist-
ing of a foregut, midgut and hindgut. The foregut is
divided into a mouth, a muscular pharynx that is
designed to suck up blood, and an esophagus. The
midgut is divided into a ventriculus, or stomach, and
several ceaca. Digestion takes place in the midgut,
which is the largest division of the digestive system.
A peritrophic membrane occurs in several species
of ticks. A short hindgut leads from the midgut to
the anal opening. Digestion starts when the blood-
meal is taken up by the midgut cells using receptor-
mediated endocytosis into coated vesicles. These are
sorted into endosomes that fuse with lysosomes. The
bloodmeal is digested in the lysosomal system in a
process termed heterophagy. The end products are
residual bodies that accumulate in the cell as diges-
tion proceeds. The products of digestion are released
into the hemolymph. A pulsating organ, the heart, is
located dorsally and helps circulate the hemolymph
throughout the body cavity. Soft ticks digest only a
portion of the bloodmeal as needed. This probably
contributes to their ability to live for relatively long
periods without an additional bloodmeal. Hard ticks
digest the entire bloodmeal, but do so in stages. The
first stage occurs before rapid engorgement. Cells in
the epithelial lining of the midgut fill up with resid-
ual bodies during the digestive process and are
sloughed off into the midgut lumen. They are
replaced by new cells that repeat the digestive pro-
cess, slough off and are replaced. The second stage of
digestion occurs during rapid engorgement. To enter
rapid engorgement, a female must be inseminated.
During rapid engorgement, midgut cells become
greatly distended and are filled with endosomes
containing the bloodmeal. At this time, digestion is
minimal. Following completion of the bloodmeal,
the female drops off the host and the third stage of
digestion occurs. During this time, all the bloodmeal
is utilized and the midgut cells fill up with residual
bodies. Cells do not slough off during second or
third stage of digestion.
Ticks (Acari: Ixodida)
T 3783
Osmoregulatory and Excretory Organs
Osmoregulatory organs are used to eliminate the
excess water and ions of the blood meal. In hard
ticks, salivary glands develop into osmoregulatory
organs and return water and ions to the host as
saliva. In soft ticks, coxal glands are the osmoregu-
latory organs and eliminate excess water and ions
to the outside through the coxal fluid, which
appears as a colorless drop between the base of
legs I and II during, or shortly after, feeding. Coxal
glands are absent in hard ticks. In hard and soft
ticks, paired Malpighian tubes accumulate gua-
nine, the end product of nitrogenous metabolism.
Malpighian tubes empty into the lower digestive
tract near the junction of the midgut and hindgut.
Guanine is then expelled through the anus as a
white paste-like substance along with the undi-
gested portion of the bloodmeal, which appears as
small red pellets.
Water Loss
Unfed ticks must prevent desiccation to survive.
This is accomplished by physical barriers and physi-
ological and behavioral adaptations. The most
important physical barriers are the impermeable
cuticle and a discontinuous respiratory cycle in
which the spiracle remains closed except during gas
exchange. Physiological adaptations include the
excretion of guanine which is a dry waste product,
and dry fecal material. An important behavioral
adaptation is that ticks move down close to the
ground into microenvironments with increased
humidity following questing. Here, the tick can
actively reabsorb water from the environment using
a salt solution secreted onto its mouthparts by the
salivary glands.
Reproduction
Male ticks inseminate their mates by transferr­
ing  packets of sperm in a structure termed a
3784
T Ticks (Acari: Ixodida)
s­ permatophore. Parthenogenesis is rare, but
occurs in both hard and soft ticks and involves
thelytoky where females produce only females. In
female ticks, a large amount of the blood meal is
converted to the female-specific glycolipoheme
protein vitellogenin, which is secreted into the
hemolymph and taken up by the eggs to become
vitellin. Vitellin is the yolk of the tick egg and
is  the main energy source of the developing
embryo.
Soft and hard ticks wax their eggs using Gene’s
organ which is located in the anterior body cavity.
The Gene’s organ turns inside out during oviposi-
tion. Unwaxed eggs dehydrate and do not develop.
In female hard ticks, secretions from the porous
area on the dorsal surface of the basis capituli are
also added to the eggs during waxing.
Semiochemicals
Semiochemicals are informational chemicals. Two
types of semiochemicals have been identified in
ticks. Pheromones regulate beneficial functions
between the same species, and allomones repel
predators. Four different types of pheromones
occur in ticks: assembly pheromones, aggregation-
attachment pheromones, sex pheromones and a
primer pheromone.
Assembly pheromones are common in many
species of soft and hard ticks and induce clustering of
ticks. These pheromones are interspecific and effect
all life stages. Perception of assembly pheromones
cause free living ticks to cluster. Guanine, the major
excretory product of nitrogenous metabolism in
ticks, acts by contact as a non-specific assembly
pheromone in the species of Argas, Ornithodoros,
Amblyomma, and Rhipicephalus.
Aggregation-attachment pheromones induce
attachment of ticks to areas where males are feed-
ing. They are produced by males of Amblyomma
and affect the behavior of adults and, in some cases,
nymphs. Females of A. maculatum, A. hebraeum,
A. variegatum, and A. marmoreum will not embed
in hosts unless feeding males are present.
Sex pheromones elicit behavior patterns that
lead to copulation. A pheromone in the coxal fluid
of female Ornithodoros, which is most active a few
days following feeding, elicits courtship behavior in
sexually active males. In all hard ticks except Ixodes,
there is a complex, but similar, courtship behavior.
Three different types of sex pheromones are involved.
A volatile attractant sex pheromone, 2,6-dichloro-
phenol, is produced by the foveal glands in most of
these species. These glands are located on the dorsal
alloscutum just posterior to the scutum in all metas-
triate ticks. After contact with the female, males must
identify a second pheromone, the mounting sex
pheromone, or they will abandon the female. A third
sex pheromone, the genital sex pheromone, must be
recognized by males of some species before a sper-
matophore is formed and copulation completed.
A primer pheromone, in this case the fecun-
dity reducing pheromone, has been identified in
Argas arboreus, where its effect is most noticeable
when ticks are crowded. The large wax glands of
Dermacent variabilis and Amblyomma america­
num secrete an allomone that repels predators.
Life Cycles and Habitats of Ticks
Many aspects of the life cycles and habitats of soft
and hard ticks differ. Differences also occur
between two divisions of hard ticks, the Prostriata
and Metastriata.
Postembryonic Development
The Argasidae have multiple nymphal stages with
different species having different numbers of
nymphal molts. Following a final blood meal, the
last instar nymph molts into the adult stage. The
Ixodidae have a single nymphal stage.
Feeding
Depending on the species, soft ticks feed on the
host once to many times in a given life stage.

Feeding is much shorter for soft ticks (15 min to
several hours) than for hard ticks, although some
larvae require several days to complete feeding.
Soft ticks ingest a relatively small amount of blood
compared to hard ticks. In a few species of soft
ticks, the larval stage molts to a nymph without
feeding. Hard ticks take a much larger blood meal
(up to or greater than 100 times their unfed body
weight in some species) than soft ticks, and feed
for a long time (9–13 days depending on the spe-
cies). Hard ticks feed only once in a given life
stage. Larvae complete feeding in the shortest
time, adult females in the longest time. Females
pass through a feeding stage known as rapid
engorgement, while the males do not. It is during
this feeding stage, which occurs 24–48 h prior to
the completion of feeding that most of the blood
meal is taken up. Depending on the species, each
ixodid tick can consume up to 15  ml of blood
during feeding. This is made possible by the tick
returning excess water and ions from the blood
meal to the host through its saliva. Compared to
females, males produce only about one-twentieth
the amount of saliva.
Mating and Reproductive Cycles
Ticks either mate on, or off, the host. Almost all
soft ticks mate off the host. Two exceptions are
Argas (Microargas) transversus, and Otobius meg­
nini. The former is a small tick that spends its
entire life on the Galapagos giant tortoise, and is
the only known tick to oviposit on its host. The
latter tick is the spinose ear tick, an economically
important species. A blood meal is not necessary
to initiate gametogenesis in species of Prostriata.
They can mate before feeding, and can mate on, or
off, the host depending on the species. In many of
the nidicolous (nest or burrow dwelling) species
of Ixodes, males cannot feed and do not occur on
hosts. Instead, they seek out females and usually
mate off the host. This life cycle may have evolved
in nidicolous, or nest dwelling species, to ensure
that females can survive long periods without
Ticks (Acari: Ixodida)
T 3785
feeding and still oviposit. An exception occurs in
the subgenus Ixodiopsis where, despite a nidi-
colous life, males feed. All species of Metastriata
mate on the host.
Soft and hard ticks have different reproduc-
tive cycles. Soft ticks go through multiple egg
laying (gonotrophic) cycles. Females lay a clutch
of eggs during each cycle. Each clutch of eggs is
usually progressively smaller. Autogeny, the abil-
ity to lay eggs without a bloodmeal, is obligatory
in genera where females have nonfunctional
mouthparts, i.e., Otobius, Antricola, and possibly
Nothoaspis; and facultative in Argas persicus,
and several species of Ornithodoros, including
O. lahorensis. Female hard ticks go through one
gonotrophic cycle, lay a single clutch of eggs,
then die.
Hosts
Ticks either have multiple hosts, or have a one-,
two-, or three-host life cycle. Almost all soft ticks
have multiple hosts although the hosts may be the
same species. Two exceptions are Argas transver­
sus, and Otobius megnini.
All species of ixodids have either a one, a
two- or a three-host life cycle. In a one-host life
cycle, ticks infest the host as larvae then remain
on the same host as nymphs and adults. Adults
mate following a blood meal. Mated females
drop off the host and lay eggs in a protected
niche such as a crack in the ground, or under
vegetation litter. About 12 species of metastriate
ticks have a one-host life cycle. In a two-host life
cycle, the larvae infest a host then remain on the
host to feed as nymphs after molting. Following
completion of feeding, the replete nymph drops
off to molt into an adult. The adult then infests a
second host to feed and mate, after which the
female drops off to oviposit. Only a dozen or so
species of metastriate ticks have a two-host life
cycle. Two examples are Hyalomma anatolicum
excavatum and Rhipicephalus evertsi. By far the
majority of metastriate ticks have a three-host
3786
T Ticks (Acari: Ixodida)
life cycle where each life stage infests a host. Usu-
ally, each host is a different species and each is
larger than the previous host. Molting from one
stage to another occurs off the host, and mating
occurs on the penultimate host then the replete
female drops off to oviposit.
In their preference of hosts, ticks are catego-
rized as either host-specific or opportunistic. Host-
specific ticks are less common, and are considered
specialists. An example is the cattle tick B. microplus.
These ticks respond dramatically to the odors of
cattle, but not to human odors. Opportunist ticks
are generalists and have a wide range of hosts. Two
examples are Ixodes scapularis, whose hosts include
a number of species of birds and mammals, and
Amblyomma americanum, whose host list includes
reptiles, birds and mammals.
Many species of ticks have repeated feeding
success on their natural hosts, but not on unnatu-
ral laboratory hosts. Repeated infestations of Der­
macentor variabilis on their natural hosts, such as
deer mice, results in successful feeding, but when
larvae and nymphs are fed on guinea-pigs, feeding
success is reduced. Successful molting to the next
stage by ticks that have completed feeding is also
reduced.
Habitats
Ticks can be divided into nidicolous and non-
nidicolous. Nidicolous ticks either live in, or in
close association with, the host’s dwelling. That
is, the host’s nest, burrow, cave or shelter. Non-
nidicolous ticks live throughout the host’s range.
Almost all species of Argasidae and many Pros-
triata are nidicolous. Most Metastriata are non-
nidicolous. The behavior of nidicolous ticks is
adapted to specialized niches. Such behavior can
include (i) the ability to survive for years in the
absence of a host, (ii) negative phototropism, an
avoidance of light, (iii) thigmotropism, a positive
reaction to contact with a solid object, so these
ticks prefer small cracks or crevices in their envi-
ronments that contact both surfaces of their
body, (iv) a narrow tolerance of temperature and
humidity, often the optima is that of the host’s
residence.
Non-nidicolous ticks live throughout the
host’s range, but most are not distributed in a uni-
form fashion throughout this range. Some are
found in several different habitats of their host’s
range, while others have a single preferred type of
habitat, for example a deciduous forest, where
most of their population is found. Important fac-
tors that determine this non-uniform type of dis-
tribution are climate, vegetation, availability of
hosts, presence or absence of diapause, and the
ability of the tick species to withstand adverse
environmental conditions. No single ecological
factor can account for this non-uniform type of
distribution.
The presence of diapause enables many tick
species to synchronize their populations with the
presence of hosts or with favorable climatic condi-
tions. Diapause is a state of low metabolic activity in
an arthropod that is mediated by neurohomone(s).
Two types exist in ticks, behavioral diapause, or
developmental diapause. Ticks in behavioral dia-
pause will not feed when offered hosts and often fail
to quest for hosts. Behavioral diapause is the most
common type. Developmental diapause involves
delayed completion of development in an egg, or
fed immature. Developmental diapause is often an
important regulator of the developmental cycle in
nidicolous ticks that use migratory birds or bats for
hosts. Usually this diapause occurs as delayed ovi-
position, which ensures that expansion of the tick
population is related to the presence of the host.
Great numbers of nidicolous ticks can occur in a
given nest or burrow. Bird nests can contain up to
20,000 ticks per square foot, and warthog burrows
have contained 250,000 ticks per burrow. In some
cases, seabirds have abandoned their nests and
fledglings due to the presence of large numbers of
ticks. Diapause has not been reported in nidicolous
ticks that have non-migratory hosts. Diapause is
widespread in non-nidicolous ticks. In Ixodes rinci­
nus, developmental diapause exists in the egg and
all active stages, which results in separate spring

and fall feeding populations. Delayed oviposition
(developmental diapause) occurs in Dermacentor
marginatus. Behavioral diapause occurs in Derma­
centor albipictus, Dermacentor andersoni and Der­
macentor variabilis to name a few species.
Dispersion
Ticks move slowly over short distances and must
rely on their hosts for dispersal. Most widespread
tick species have hosts that, in turn, are widely dis-
persed, or are migratory. An example is the brown
or red dog tick, Rhipicephalus sanguineus, which is
found throughout the world. Many ticks have at
least one life stage that infests migratory birds that
can carry them between continents. Using hosts as
mechanisms of dispersal has resulted in the spread
of tick transmitted diseases through large dis-
tances, and has made many of the diseases trans-
mitted by ticks multifocal.
Ticks of Medical and Veterinary
Importance
Three genera of soft ticks, Argas, Ornithodoros and
Otobius have species that are medical or veterinary
pests. The other genera, Antricola and Nothoaspis,
are parasites on bats.
The genus Argas is divided into seven subgen-
era, two of which, Argas and Persicargas infest birds.
The other subgenera are parasites on bats and small
mammals. Almost all species in the genus Argas are
nocturnal and occur in arid habitats with long dry
seasons. Argas (Persicargas) persicus, the fowl tick
or blue bug, is the most widespread soft tick on
poultry. Larvae of this tick feed on the host for
2–10 days depending on the situation. Fed larvae
drop off and molt in 4–16 days. Nymphs seek hosts
and complete feeding within 30  min. There are
three nymphal stages. Adults complete feeding
within 45  min. Females feed before laying each
clutch of eggs, and this cycle may occur daily.
­Several hundred eggs are laid in the early clutches,
Ticks (Acari: Ixodida)
T 3787
and only a couple of dozen in the later ones. Argas
(Persicargas) persicus originated in the Palearctic
region but, following domestic poultry, this tick has
spread throughout the world with the possible
exception of the Neotropical region. In addition to
domestic poultry, it is found on wild birds. The
fowl  tick transmits two diseases to poultry, fowl
spirochetosis and a rickettsial disease caused by
Aegyptianella pullorum. Three other closely related
ticks, Argas (Persicargas) walkerae, Argas (Persi­
cargas) persicus, and Argas (Persicargas) arboreus,
are also parasites on birds. In the southern U.S.A.,
Argas persicus, Argas sanchezi, and Argas radiatus
are parasites on poultry, but are not problems in
large commercial poultry houses.
Three species of Ornithodoros, Ornithodoros
moubata, Ornithodoros savignyi, and Ornithodoros
lahorensis, are important parasites of man and
domestic animals. The African tampan, or eyeless
tampan, Ornithodoros moubata, is a complex of at
least four species. Ornithodoros moubata sensu
strictu (in the narrow sense) occurs throughout
semi arid, or arid Africa from Kenya southward to
South Africa. The life cycle is relatively short, about
4 months from egg to adult. The larvae are non-
feeding and molt directly into a nymph. There are
three or more nymphal stages. Females deposit
several hundred eggs per batch. More than seven
clutches are laid, which can total over 2,500 eggs.
Large infestations of this tick can kill pigs. The tick
can become a parasite of humans that live in huts
or in dwellings with cracks. Ornithodoros moubata
is the vector of Borrelia duttoni, which causes
endemic relapsing fever. Other species in this
complex include Ornithodoros moubata porcinus,
found in Africa, Ornithodoros tholozani and Orni­
thodoros erraticus, found in the Middle East. Orni­
thodoros moubata porcinus, the African warthog
tick, and Ornithodoros erraticus, transmit the caus-
ative agent of African swine fever. The eyed tam-
pan, Ornithodoros savignyi, occurs in the arid
regions of Africa, the Middle East, India and Sri
Lanka where it is a parasite on domestic stock and
humans. It does not transmit disease, but heavy
infestations can cause severe damage. Ornithodoros
3788
T Ticks (Acari: Ixodida)
lahorensis is a parasite of domestic stock through-
out its range in Asia and the southern republics of
the former Soviet Union. Ornithodoros hermsi,
Ornithodoros turicata and Ornithodoros parkeri,
feed on humans along with other hosts, and can
vector Borrelia species that cause relapsing fever.
The spinose ear tick, Otobius megnini, is a par-
asite on cattle, horses and companion animals. It
occurs mostly in stables and in other animal shel-
ters. The spinose ear tick has spread from America
to southern Africa and India, and has been
reported from humans in the later region. The lar-
vae have a capitulum that is over one-third its
body length. Larvae invade the ear and feed for
5–10 days then molt to a nymph. Nymphs reattach
within the ear. The integument of the nymph has
numerous spines from which the tick gets its com-
mon name. The second stage nymph drops off the
host and seeks small, hidden areas such as cracks
where they molt to a fiddle-shaped adult. The adult
does not feed. Its hypostome is small and has no
teeth. Mated females lay up to 1,500 eggs in cracks
in the walls of the shelters at a height suitable for
transfer to a large host. Larval spinose ear ticks die
within 4 months, but adults can live up to 2 years
without hosts.
In the Ixodidae, the genus Ixodes has the larg-
est number of species. All are three-host ticks
without eyes and festoons. The capitulum is much
longer in the female than in the male. The most
important species group is the Ixodes ricinus-­
persulcatus complex which has a wide distribution
from North America south into Mexico, and in
Europe south to the Sahara, and in Asia south to
the Himalayas. This complex is important in vec-
toring pathogenic viruses of man, the Borrelia that
causes Lyme disease, and the protozoa that cause
piroplasmosis. Important species of this group are
the blacklegged tick, or American deer tick, Ixodes
scapularis (=dammini), found in North America,
the European sheep tick, or European castor bean
tick, Ixodes ricinus, and the tiaga tick, Ixodes per­
sulcatus. Ixodes scapularis occurs in North America.
Ixodes ricinus is found along the western parts of
the British Isles, and Norway southward to Iran
and Turkey, Bulgaria, Italy and the Pyrenes. Ixodes
persulcatus has a wide distribution from Japan
westward into Germany. All three are vectors of
the causative agent of Lyme disease. Ixodes persul­
catus is also the main vector of the virus that causes
Russian spring-summer encephalitis. This tick is
more tolerant of temperatures and is more cold
hardy than Ixodes ricinus. Two other species, the
Karoo paralysis tick Ixodes rubicundus in south-
ern Africa, and Ixodes holocyclus in Australia,
cause paralysis in mammals. Lyme disease is trans-
mitted by Ixodes rincinus in Europe, Ixodes scapu­
laris in the Eastern U.S. and Ixodes pacificus in the
Pacific coast states and intermountain west of the
U.S. Ixodes pacificus is a major cause of tick
paralysis.
The European sheep tick, Ixodes ricinus, is a
three-host tick with a 2- to 6-year life cycle depend-
ing on location. Immatures attack birds, but sheep
can be the hosts for all three life stages. This tick
has separate spring and fall feeding populations.
The larvae, seek a host in the spring or fall, feed for
3–6 days, then drop off and molt. After molting, the
larvae ascend grass and twigs to assume a questing
position but, here, they tend to lose body water
causing them to descend to a microclimate on or
near the ground where water is at or near satura-
tion. They rehydrate in this microclimate. The
nymphs seek a host the next spring or fall, engorge
for 3–5 days, then drop off the host and molt. The
adults seek a host the next spring or fall. Females
take from 5 to 14 days to complete feeding. Fertil-
ized females lay from 500 to 2,000 eggs that hatch
by late spring or late fall, but the larvae usually do
not feed until the following spring or fall.
Ixodes scapularis is found from Maine south
to Florida and west into central Texas and possibly
Mexico, and from Maine west into Minnesota and
Iowa. It is a small three-host tick that attacks a
wide variety of birds and mammals including man.
Larvae and nymphs attack small rodents especially
the white footed mouse Peromyscus leucopus.
Adults occur on larger animals with the white-
tailed deer Odocoileus virginianus being the most
common. A large population of deer is an important

factor in the presence of large populations of
Ixodes scapularis. Changes in agriculture and pat-
terns of human use in the eastern U.S. have resulted
in humans coming more into contact with areas
supporting populations of Ixodes scapularis. The
tick population in these areas has increased dra-
matically due to the increase in the deer popula-
tion. This tick is an important vector of the
causative agent of Lyme disease, human babesiosis
and human granulocytic ehrlichiosis. The Western
black legged tick, Ixodes pacificus, is found on the
pacific coast states and British Columbia. It is
closely related to Ixodes scapularis. Immatures of
Ixodes pacificus feed on small rodents and lizards,
the adults feed on deer, horses and man. Through-
out its range, this tick occurs in regions of higher
mositure. Ixodes pacificus transmits the causative
agent of Lyme disease and equine granulocytic
ehrlichiosis.
Species of Dermacentor are mostly large,
ornate, brevirostrate ticks with eyes and festoons.
This genus is most common in the New World.
Dermacentor marginatus transmits Siberian tick
typhus and Dermacentor reticulatus infests live-
stock. Both occur throughout Europe and Asia.
Dermacentor albipictus, the winter tick, occurs
from the west coast to the east coast of Canada
and far north to almost 60°N latitude. This one-
host tick does not feed during the summer. Heavy
infestations on large horned animals such as
moose can result in death. The Pacific Coast tick,
Dermacentor occidentalis, is found from Oregon to
California where it transmits anaplasmosis. This
species also causes paralysis in livestock and deer.
The American dog-tick, D. variabilis, occurs
in the central and eastern United States (U.S.)
northward into southern Canada and Nova Scotia.
The American dog tick vectors the Rickettsia bac-
teria that causes Rocky Mountain spotted fever,
the bacterium that causes tularemia and anaplas-
mosis. D. variabilis is an important pest of domestic
animals and man throughout its range. It can cause
canine paralysis. In the southern U.S., a life cycle
can be completed in 3  months under favorable
conditions. However, in the northern regions of its
Ticks (Acari: Ixodida)
T 3789
distribution, a life cycle can take 2 years. D. vari­
abilis has expanded its range in recent years. It is
found in the mid-western U.S. and Pacific states
where local populations have been established,
mostly along river valleys. Northward expansion
is probably limited by cold temperature because
the tick has not established breeding populations
beyond the mean winter (December–February)
0°C isotherm. Westward expansion is probably
limited by the lack of rainfall and deciduous for-
ests or brushy habitats. The American dog-tick
prefers field-forest ecotones. D. variabilis is a three-
host tick. Replete females drop from the host and,
within 4–10 days, lay a clutch of 4,000–6,500 eggs
preferably in cracks and crevices on the ground. In
the summer, the eggs begin to hatch in about
35 days depending on the temperature. The larvae
feed mostly on wild mice and voles for 3–12 days
then drop off and molt to nymphs. The nymphs
also prefer wild mice and voles as hosts. They feed
for 3–11 days then drop off to molt on the ground
and emerge as adults. The adults prefer dogs and
other larger mammals including man. The females
engorge in 6–13  days. Mating takes place on the
host. Unfed adults may live for more than 2 years.
The Rocky Mountain wood tick, D. andersoni,
occurs in the western U.S. and British Columbia. It
is a three-host tick with a similar life cycle to that
of D. variabilis. The adults prefer large mammals,
the nymphs smaller mammals and the larvae feed
mostly on wild mice. D. andersoni transmits the
causative agents of Rocky Mountain spotted fever,
Colorado tick fever and anaplasmosis. The tick
causes paralysis in mammals.
The genus Anocentor has a single species, the
Neotropical ear tick of horses, A. nitens, found in
the southern U.S. westward to Texas and south-
ward to Brazil. This one-host tick has no ornamen-
tation and the eyes are obsolescent. Some workers
place this tick in the genus Dermacentor.
Nosomma has a single species, N. monstrosum,
which has a wide range of hosts including cattle,
buffalo, humans, boar, bear, horses and dogs, with
the larvae infesting rodents. This three-host tick
occurs in India and Southeast Asia.
3790
T Ticks (Acari: Ixodida)
Species of Rhipicephalus are brevirostrate,
small, mostly inornate ticks. This genus is found in
the Old World, mainly in Africa south of the
Sahara and southern Arabia. One species, the
brown or red dog tick R. sanguineus, is now cos-
mopolitan with a greater geographical distribu-
tion than any other species of tick. R. sanguineus
has a wide host range preferring dogs and other
carnivores, some large herbivores, lagamorphs,
rodents, bats, reptiles, and some primates includ-
ing humans. This tick is a warm-climate species
that probably originated in Africa. Its ability to
colonize shelters in cold climates has significantly
contributed to its distribution. The brown dog tick
vectors Babesia canis and Rickettsia conorii. The
latter pathogen causes boutonneuse fever. In some
areas of Mexico, this tick transmits Rickettsia rick­
ettsii that causes Rocky Mountain spotted fever.
Other important species of Rhipicephalus on
domestic animals are the brown ear tick R. appen­
diculatus, R. evertsi and R. simus. R. appendiculatus
is a three-host tick that occurs in the eastern and
southern parts of Africa south of the equator. This
tick is found on goats and sheep but is mostly a
parasite of cattle. Its distribution reflects an inter-
action between climate, vegetation and hosts. It is
thought that the presence of cattle is necessary for
the tick to become established. Temperatures
around 4°C will kill all stages of engorged R. appen­
diculatus. A dry climate prevents eggs from hatch-
ing through desiccation. Under ideal conditions, a
life cycle in this tick can be completed in
3–4 months. The number of cycles per year depend
on the local conditions. In southern Africa, there
is one generation per year, but in Tanzania, two
generations per year can occur under optimal
conditions. R. appendiculatus vectors Theileria
parva which causes east coast fever in cattle, the
Nanovirus that causes Nairobi sheep disease, and
Babesia bigemina that causes babesiosis in cattle.
The two-host African red tick, R. evertsi,
infests domestic cattle, goats, sheep and wild ungu-
lates. The eggs of this tick hatch on the ground and
the larvae seek a host animal where they attach
to the inner surface of the ear. After feeding to
repletion, larvae detach and molt into nymphs that
attach in the same area of the ear and feed to reple-
tion then drop off the host to molt on the ground.
The adults seek a second host, attaching mostly in
the perianal region under the base of the tail or
less commonly on the teats, the base of the legs, or
the scrotum. Here they mate and females feed to
repletion then drop off to lay eggs on the ground.
All five species of Boophilus are brevostriate,
one-host ticks and all are parasites on large hoofed
mammals, especially cattle. No festoons, or eyes
are present. Three species are important vectors of
babesiosis to cattle: B. microplus, the cattle tick, is
found in the Neotropical, Afrotropical and Austra-
lian regions; B. decoloratus occurs in tropical
Africa; and B. annulatus is found in North Amer-
ica. The life cycle of B. microplus is completed in
about 5 weeks under favorable conditions and can
require up to several months under less favor-
able conditions. Females lay a single clutch of
2,000–3,000 eggs that hatch in about 2  weeks at
70% humidity. Larvae quest on the tips of grass
and twigs but do not move down to rehydrate in a
microenivronment. Larvae feed for about 4  days
on the host then molt into a nymph after a quies-
cent period of about 2  days. The nymphs may
move about the host before attaching. They feed
for about a week and then molt into an adult. This
molt is also preceded by a short quiescent period.
The adults mate on the host. The females take
about 3 weeks to feed to repletion, then drop off to
lay eggs. The oviposition period lasts some 10 days
and is preceded by a short preoviposition period
of several days. B. microplus must have a high rain-
fall, and cannot be found in dry areas with a low
humidity. This tick is widespread throughout the
warmer climates of the world. In the tropics,
B.  microplus are found on cattle throughout the
year. In subtropical regions, it has a seasonal cycle.
A commercial vaccine has been developed against
“concealed antigens” of the tick midgut. This vac-
cine has reduced tick fertility by as much as 70% in
some cases. Booster shots are necessary.
Some species of Margaropus, infest giraffes in
the Sudan and East Africa, but M. winthemi, the

winter horse tick, is a parasite on horses in south-
ern Africa. Margaropus are one-host ticks that are
considered relic boophilids.
Amblyomma are mostly large, highly orna-
mented, longirostrate ticks with eyes and festoons.
Most species occur in the tropics. All have a three-
host life cycle. Their long mouthparts are espe-
cially damaging to cattle hides. Species from the
southern U.S. are the only members of this genus
from the temperate region, although some nymphs
occur on migratory birds from Africa northward
through Europe and Asia. The African brown ear
tick, A. appendiculatus, and the tropical bont tick,
A. variegatum, transmit Cowdria ruminantium,
the causative agent of heartwater fever in cattle.
A.  nuttali has the distinction of producing the
largest clutch of eggs ever recorded from a single
tick, over 22,000.
The lone star tick, Amblyomma americanum,
is found across the southeastern U.S. from central
Texas to the Atlantic coast and north to New York.
It prefers a forested habitat. The questing activity
of this tick is most active from sundown to the late
evening hours when its principle host, white-tail
deer, forage. Large numbers of ticks occur in, or
near, the bedding of hosts. Active stages have no
host preference. Immatures are found on birds and
all sizes of mammals, but adults occur mostly on
medium to large mammals. All stages of this tick
attack man. Amblyomma americanum is well
adapted to forest communities. Two factors that
must be present to support large populations of
Amblyomma americanum are suitable hosts, and a
moist microenvironment to protect the ticks from
desiccation. An area with a forest canopy and lots
of vegetative ground cover is ideal habitat for
Amblyomma americanum. Male ticks are found on
deer all year. Engorgement of the females may be a
photoperiod response as there is a small drop-off
period that begins in May, and is over in late
August. The larvae first occur on deer in late June
and continue until mid-November. The nymphal
activity, which occurs from March to October, is
the longest of any stage. The lone star tick is a vec-
tor of Rocky Mountain spotted fever and Q fever.
Ticks (Acari: Ixodida)
T 3791
The Cayenne tick, Amblyomma cajennense, is
also found in the southwestern U.S. south through
Mexico and Central and South America and the
West Indies. It commonly attacks man and many
other animals. It transmits Rocky Mountain spot-
ted fever from Mexico south to Brazil. The Gulf
Coast tick, A. maculatum, is a parasite on deer and
cattle. The deer population has dramatically
increased, and this has resulted in an increase in
the population of A. maculatum.
Some or all species of Hyalomma are longiro-
strate, medium-sized ticks with eyes that may or
may not have festoons and scutal ornamentations.
This genus most likely originated in the dry des-
erts of Kazakhstan and Iran in the Palaearctic.
Some or all species of Hyalomma are hardy ticks.
Several economically important species exist. The
H. marginatum complex and H. anatolicum ana­
tolicum are major vectors of the arbovirus that
causes Crimean-Congo haemorrhagic fever. The
H. marginatum complex extends from India and
Indochina westward throughout southern and
southeastern Europe into the Near East and North
Africa. Populations are scattered throughout the
drier areas of Africa south of the Sahara from the
Red Sea to the Atlantic Ocean. Hosts of immature
ticks in this complex include wild birds, small
mammals, hedgehogs and hares. The adults attack
any domestic animal especially cattle, horses and
camels. Migrating birds are important in spread-
ing these ticks. A typical H. marginatum life cycle
is completed in 116 days at 18–19°C. All stages of
this tick complete feeding in about 6  days. The
females lay from 4,300 to 15,500 eggs in a single
clutch. Unfed adults can live for over a year.
Species of Haemaphysalis are small, inornate,
brevirostrate ticks. The genus is most common in
the tropics where it probably originated. H. punc­
tata in the Australian region, and H. longicornis in
the Oriental region, are important parasites of cat-
tle. The latter tick is also found on red deer in New
Zealand. H. leachi, the yellow dog tick of Africa, is
a common parasite of dogs and carnivores
throughout the tropics and subtropics of Asia and
Africa. It transmits the protozoan pathogen of
3792
T Ticks (Acari: Ixodida)
malignant jaundice in dogs. In the Oriental region,
H. spinigera transmits the arbovirus that causes
Kyasanur Forest Disease. Two species of Haema­
physalis occur in North America. The rabbit tick,
H. leporispalustris, occurs in the New World from
Alaska south to Argentina. It has a large host list
that includes horses, cats, dogs and birds. It rarely
attacks man, but is responsible for the transmis-
sion of Rocky Mountain spotted fever and tularemia
among wild animals. The bird tick H. chordelis,
is  common on upland game birds in North
America and is an important parasite of turkeys.
H. mageshimaenis is found in Japan, and is rare in
that it has both bisexual and parthenogenetic
reproduction.
Economic Importance of Ticks
Ticks are of great economic importance. Many
disorders are caused directly by the interaction of
the host to the tick. These can occur locally at the
tick bite area, but some are systemic such as toxic
reactions, or toxicoses and host paralysis produced
by tick toxins. Ticks have a high vector potential
and transmit more varieties of serious diseases to
vertebrates than any other blood feeding arthro-
pod. They are second behind mosquitoes in trans-
mitting diseases to humans, and first in veterinary
importance. Some species of ticks have a toxin in
their saliva that can cause death through paralysis.
Another of the many afflictions imposed on their
host has to do with blood loss through heavy tick
burdens. Large mammals can harbor enormous
numbers of ticks. A moose can have more than
50,000 ticks feeding on it at any given time, as can
a small giraffe. The record is probably a single cari-
bou found with more than 400,000 ticks. Heavy
tick infestations also occur in livestock and com-
panion animals where loss of blood can result in
the development of anemia, or in extreme cases,
death.
Several superficial local disorders such as der-
matosis, inflammation, itching, swelling and ulcer-
ation can occur at the tick feeding site. In some
individuals, tick feeding can produce a hypersen-
sitivity reaction that can be local, or in severe cases,
systemic, and can even result in anaphylactic
shock. These reactions usually occur early in the
course of tick feeding. The feeding site can become
a means of secondary infections from pathogens
not transmitted by the tick. The infestation of the
auditory canal by ticks, otocariasis, can cause seri-
ous secondary infections. Proper removal of ticks
is important to minimize secondary infections
because skin ulceration and lesions can result from
improper or partial removal of tick mouth parts.
Tick toxins introduced into the host through
the saliva cause paralysis or death in domestic ani-
mals, some wildlife, and humans. Tick paralysis
manifests itself as a motor paralysis that spreads
from the lower limbs to the upper limbs and head
region within hours. Paralysis rescinds following
removal of the tick, or ticks, except in the case of
Ixodes holocyclus, which is discussed below. Paral-
ysis is most likely to occur when a tick embeds on
the neck, especially near the base of the skull.
Many different ticks can cause paralysis, but five
species are notorious. These are Dermacentor
andersoni and Dermacentor variabilis in North
America; Ixodes rubicundus, Rhipicephalus evertsi
evertsi and Argas walkerae in South Africa; and the
Australian paralysis, or scrub tick, I. holocyclus in
Australia. The toxin of the latter tick, known as
holocyclotoxin, has been isolated, characterized
and an antitoxin developed. The scrub tick is the
most virulent paralysis tick in the world. Most
cases of paralysis are caused by females because
larvae and nymphs have much less toxin, and the
adult males feed only by inserting their mouth-
parts into females. Removal of I. holocyclus does
not rescind the paralysis, which must be treated by
an antitoxin given intravenously.
The high vector potential of ticks is a direct
result of the following characteristics: (i) Ticks are
persistent blood feeders that stay attached to the
host for long periods allowing ample time for the
transfer of pathogens. Hard ticks feed for 5–14 days
depending on the species. (ii) Ticks have great lon-
gevity that enhances the chances of acquiring and

transmitting pathogens. (iii) Ticks have a high
reproductive potential. Hard ticks lay a single
clutch of eggs that can number over 20,000
depending on the species. (iv) Ticks have few nat-
ural enemies due to heavy body sclerotization. (v)
Pathogens in ticks can persist through transovarial
transmission to the next generation, and from one
life stage to another through transstadial trans-
mission. (vi) Ticks transmit pathogens through
several routes. Most are transmitted through the
saliva, but some Borrelia are transmitted through
the coxal fluid. Stercoral transmission occurs
through the feces and requires pathogens that can
survive in the dry excrement of ticks, so this route
is uncommon. However, Coxiella burnetti and
Rickettsia conori are transmitted in this fashion.
(vii) Some pathogens are transmitted directly from
an infected tick to a non-infected tick while both
are feeding on the same host. This phenomena is
termed co-feeding and may be an important
means of maintaining tick-borne pathogens. Anti-
hemostatic, anti-inflammatory and immnuosup-
presant actions of tick saliva facilitate blood-feeding
and may indirectly enhance pathogen transmis-
sion. This is termed saliva-activated transmission
(SAT). In some diseases, such as tick-borne
encephalitis, uninfected ticks can acquire the
pathogen when co-feeding with infected ticks on
hosts that do not exhibit a viremia, or systematic
infection. This phenomenon is known as non-
viremic transmission and may be due to SAT. Bac-
terial pathogens may be acquired by continuing to
feed at a localized site where previously infected
ticks have fed.
Tick transmitted pathogens include arbovi-
ruses (arthropod-borne viruses), rickettsiae, other
bacteria, and protozoans. Most tick-borne dis-
eases are zoonoses, that is they occur in wild and
or domestic animals that act as a natural reservoir
of infection. Man is only an incidental host in
many of these diseases. Some zoonotic diseases
are transmitted within their natural reservoirs by
a species of tick that does not attack man. A dif-
ferent tick species then transmits the disease to
man. If the zoonoses includes a large wild animal
Ticks (Acari: Ixodida)
T 3793
reservoir with multiple vector species of ticks it
becomes difficult to control.
Tick-borne arboviruses are members of
three families, the Flaviviridae, the Bunyaviridae
and the Reoviridae. The Flaviviridae includes the
genus Flavivirus whose virons are spherical,
about 40–50 nm in diameter with a lipoprotein
envelope, and a genome that consists of a single
molecule of single-stranded RNA. The Bunya-
viridae includes the genus Nairovirus in which
all species are transmitted by ticks. The Nairovi­
rus are spherical in shape, 80–100 nm in diame-
ter, with a lipid envelope that has glycoprotein
projections. Their genome consists of three mol-
ecules of single-stranded RNA. The Reoviridae
contain the genus Orbivirus which causes Colo-
rado tick fever. This virus is icosahedral in shape,
60–80 nm in diameter, with an outer protein coat
and a genome of 12 pieces of RNA. All tick-
borne arboviruses replicate in intermediate ver-
tebrate hosts as well as in the tick. The major
arboviral diseases transmitted by ticks include
Tick-Borne Encephalitis, Louping Ill, Omsk
Hemorrhagic Fever, Kyasanur Forest Disease,
Powassan Encephalitis, Crimean-Congo Hem-
orrhagic Fever, Nairobi Sheep Disease, Colorado
Tick Fever and African Swine Fever. Other lesser
known tick-borne arboviral diseases occur in
birds, especially seabirds. Treatment for human
arbovirus diseases is often relegated to supportive
measures. Hospitalization can help especially if a
high fever or other symptoms can be treated.
Tick-Borne Encephalitis (TBE) is caused by a
Flavivirus and can affect humans, sheep, monkeys,
mice and hamsters. It is transmitted by species of
Ixodes. In Europe and Northern Asia, it is trans-
mitted mostly by Ixodes ricinus, and in areas of the
Far East by I. persulcatus. TBE can also be trans-
mitted through fresh milk or cheese from infected
goats or sheep. TBE is most common during spring
and summer. The disease is maintained in nature
by infections of small mammals such as rodents.
Agricultural and forest workers are most at risk
of infection, but urban residents that spend
time in the forests and countryside are also at risk.
3794
T Ticks (Acari: Ixodida)
Two subtypes of TBE are recognized, Russian
Spring-Summer encephalitis (RSSE), which is
found in Siberia, the southern republics of the for-
mer Soviet Union and in north-eastern China; and
Central European Encephalitis (CEE), which
occurs in Russia west of the Ural mountains and
Europe. RSEE is more serious than CEE. RSSE is a
life-threatening disease with a mortality rate of
from 8% to 54%. However, an effective vaccine
exists. RSSE is characterized by high fever, head-
ache, nausea followed by the symptoms of devel-
oping encephalitis, which include paralysis
especially in the upper body regions. Paralysis may
persist in some patients that have recovered. The
milder European form is biphasic with a brief
remission after 4–6  days of illness followed by
renewed fever. Brain dysfunction and meningeal
irritation are common. Mortality in the milder
CEE subtype is from 1% to 5%.
Louping Ill (LI) is caused by a Flavivirus and
is found in Great Britain where it has been known
for centuries among sheepherders in Scotland
and Ireland. LI infects a variety of mammals
including man, and some birds, especially upland
game birds. The virus is transmitted by I. ricinus.
Transstadial, but not transovarian, transmission
occurs. The disease is so named because it causes
an erratic “louping” gait in sheep. The mortality
in sheep is severe, often as high as 60%, and has
been known to reach 100%. LI causes a severe,
fatal encephalitis that often results in permanent
neurologic damage in animals that recover. In
humans, LI also produces an encephalitis that
can be severe and even result in death. Those at
risk include farmers, veterinarians, and animal
husbandry workers. A vaccine for sheep exists,
but sick animals are destroyed. Lambs are pro-
tected by a maternal antibody that disappears
after weaning.
Omsk Hemorrhagic Fever (OHF) is caused
by a Flavivirus and affects humans, rats, mice,
muskrats and wild rodents. OHF occurs in Siberia
and is transmitted by D. reticulatus and I. aprono­
phorus. Immature D. reticulatus ticks bite mostly
water voles, which are found in a forest-steppe
habitat. The cyclic nature of the vole population
can produce a huge population of ticks, many of
whom are infected with the virus. Adult D. reticu­
latus ticks infect several different large mammals
and humans. The tick is the reservoir, which is
maintained by transovarial transmission. I. apro­
nophorus does not transmit the virus to humans,
but is thought to help maintain the virus in nature
by feeding on many different small mammals
especially voles and muskrats. Muskrats have a
high incidence of infection (up to 30% of the
­population). Transmission of OHF to humans can
occur through handling infected muskrat car-
casses, or by drinking infected water contami-
nated by muskrats or voles. Muskrats are
amplifying hosts for the disease. Hunters of musk-
rats are at severe risk. The disease occurs during
the spring and summer seasons. OHF is charac-
terized by hemorrhagic symptoms. Mortality is
less than 5%. No vaccine is available, but some
cross-protection occurs with the Tick-Borne
Encephalitis vaccine.
Kyasanur Forest Disease (KFD), caused by
a Flavivirus affects humans and monkeys. KFD
occurs in the Kyasanur State Forest and a sur-
rounding area in India where it is transmitted
by H. spinigera. Increased human activity in the
forest has increased the opportunity of this tick
to attack humans. The pathogen is maintained
within a given tick by the transstadial route, but
is not transmitted transovarially. KFD has a
­sudden onset after a short incubation period
(2–7  days). Symptoms include coughing, diar-
rhea, vomiting, a severe fever for up to 12  days
and muscle pain. Mortality is 8–10%. Monkeys
are very susceptible to KFD. They are viremic for
days, during which time they have many ticks
feeding on them. In this fashion, monkeys act as
an amplifying host for the disease. Human cases
of this disease are increasing. Individuals work-
ing in the forest are especially at risk, however, an
effective vaccine exists.
Powassan Encephalitis (PE) is caused by a
Flavivirus. It occurs in Canada, Russia and
northeastern parts of the U.S. where it has been

isolated from a variety of vertebrates and causes
a sickness in humans, horses, and foxes. PE is
transmitted by several species of Ixodes, Derma­
centor and Haemaphysalis. I. cookei is an impor-
tant vector of PE in North America. No vaccine
for PE exists.
Crimean-Congo Hemorrhagic Fever (CCHF)
is caused by a Nairovirus that is transmitted by a
wide range of tick species. It was first described in
ad 1100. CCHF is widely distributed throughout
Europe, Asia and Africa, and is most common in
arid or semiarid regions of these areas. CCHF is
transmitted mostly by ticks of the genus Hyalomma,
or by contact with blood or tissues from human
patients or infected livestock. Person to person
spread can occur through respiratory secretions
and excreta, which can cause serious outbreaks of
the disease in hospitals. In Eurasia, Hyalomma
marginatum marginatum and D. marginatus are
the principal vectors. The clinical disease has been
found only in humans, but the virus occurs in a
wide variety of mammals. CCHF is found in iso-
lated enzootic foci throughout its range. An enzo-
otic disease occurs in a population of animals at
all times. Ground-feeding birds are important in
maintaining the disease and migratory birds are
important in its spread. Incubation of CCHF takes
from 3 to 7 days. The disease has a sudden onset
with fever, chills, photophobia and severe head-
ache. Muscle pain occurs mostly in the legs and
back. The hemorrhagic state of the disease involves
bleeding from the mucous membranes and the
appearance of a round red spot, which is due to
intradermal hemorrhage. Mortality is from 10% to
50%. Ticks are the reservoirs of CCHF. The rate of
infection in ticks is amplified by feeding on
infected mammalian hosts, and by transstadial
and transovarial transmission. A vaccine exists in
Russia and parts of Eastern Europe. Controlling
this disease is very difficult due to its widespread
distribution and the large number of different tick
species involved.
Nairobi Sheep Disease (NSD), also known as
Ganjam virus disease, is caused by a Nairovirus.
NSD is found in sheep, goats, and wild ruminants
Ticks (Acari: Ixodida)
T 3795
in East Africa. The principle tick vector is R. appen­
diculatus. There is no evidence for a wildlife reser-
voir. Onset of the disease is sudden with a dramatic
rise in temperature as high as 41°C. A nasal dis-
charge and diarrhea is common, along with
abdominal pain. Mortality is high. Humans
exposed to the virus develop an antibody, but no
symptoms, with the exception of one case. Treat-
ment of NSD involves destroying sick animals. In
areas of enzootic NSD, sheep are protected by a
maternal antibody. Epizootics, diseases that spread
rapidly through an animal population, are related
to large increases in the vector populations and
require the use of acaricides.
Colorado Tick Fever (CTF) is caused by an
Orbivirus, and is found in the Western U.S. where
it infects humans and many other mammals. The
principle vector to humans is Dermacentor ander­
soni. Transovarian transmission does not occur.
The disease is enzootic in wild rodents. Wherever
the principle vector occurs with infected reser-
voirs of wild rodents and humans, local outbreaks
will occur. CTF has a short incubation period in
humans of 1–4  days. A biphasic fever occurs in
about 50% of the cases. Symptoms include chills,
nausea, sore throat and retroorbital pain. Some-
times meningitis occurs, and leukopenia is com-
mon. However, mortality is low, less than 0.2%.
The peak incidence of CTF occurs from April to
July. Treatment is supportive and no vaccine exists.
Prevention of tick infestation in focal areas of the
disease is the best method of control.
African Swine Fever (ASF) occurs in Europe,
Africa, South America and the Caribbean. This
icosahedral-shaped virus is about 200 nm in diam-
eter with a lipoprotein coat and a single molecule
of double-stranded DNA. It is the only known
DNA virus to be transmitted by an arthropod.
Originally, it was placed in the family Iridoviridae,
but is now unassigned to any family. Wild swine,
including warthogs, harbor the virus. Domestic
pigs are at risk with the mortality being as high as
100% in herds. Several species of Ornithodoros
have been shown to be vector-competent in
the  laboratory, but the only natural vectors are
3796
T Ticks (Acari: Ixodida)
O.  erraticus and O. m. porcinus. Transstadial,
transovarial and sexual transmission of ASF has
been shown to exist in O. moubata. Many of the
vector-competent species exist outside the known
distribution of ASF suggesting that the disease
has a good possibility of spreading. ASF is charac-
terized by sporadic epizootics. Ticks are not the
only way of spreading the disease, direct contact
with animals is also a factor. Three forms of the
disease are known in domestic pigs – acute ASF,
subacute ASF and chronic ASF. Acute ASF causes
a high fever (up to 41°C) about 3 days following
infection. Then the fever subsides and the animal
dies. In the subacute form of ASF, the fever fol-
lows an irregular course for 3–4 weeks, then the
sick pigs either die, or recover and become carri-
ers of the virus. In chronic ASF, the main symp-
toms are stunted growth and emaciation. In
chronic ASF, sick pigs often remain carriers and
can live for a long time. They eventually die from
a secondary illness.
The Rickettsia are bacteria that are obligate,
intracellular parasites of vertebrates. Unlike viruses,
they have both DNA, RNA and bacterial cell walls.
During evolution, the Rickettsia have lost several
enzymes and cell components necessary to live
outside the cell. Some 15 genera of Rickettsia are
recognized, seven of which are transmitted by ticks:
Rickettsia, Coxiella, Ehrlichia, Cowdria, Anaplasma,
Aegyptianella, and Haemobartonella.
Rickettsia are divided into three groups, each
containing serologically related species. Two groups,
the Spotted Fever Group (SFG), and the Typhus
Group (TG) are transmitted by ticks. The third
group, the Scrub Typhus Group, is transmitted by
a mite. The only species of TG transmitted by ticks
is R. canada, which was first isolated from rabbit
ticks in Ontario. R. canada has not yet been shown
to cause a human disease despite a single case of
possible human infection where the patient pre-
sented with Rocky Mountain Fever-like symptoms.
The SFG is made up of the following species:
R. rickettsii, R. montana, R. belii, R. rhipicephali, R.
parkeri, R. conorii, R. australis, R. sibirica, R. slovaca,
R. helvetica, and R. akari. In general, species of the
SFG cause severe diseases characterized by head-
ache, chills and fever. These rickettsiae grow mainly
in the cytoplasm of the host’s cells, but can also grow
in the nucleus. Infected host cells are seldom killed
by SFG rickettsiae. They have an optimal growth
temperature of 32–34°C. They do not cause hemo-
lysis. The associated rash in humans is the result of
damage to capillaries that causes blood to leak out.
SFG rickettsia can cause collapse of the cardiovas-
cular system.
Several SFG rickettsiae are not associated
with human disease. Rickettsia parkeri occurs in A.
maculatum and Amblyomma americanum, from
Texas through Mississippi and Georgia. The prin-
ciple hosts are domestic animals. Rickettsia mon­
tana is found in D. andersoni and D. variabilis in at
least 13 states in the U.S. and is maintained natu-
rally by small mammals. Rickettsia rhipicephali is
found in R. sanguineus, D. andersoni, D. variabilis,
and D. occidentalis in the southeastern U.S., and is
maintained by small mammals. It is not patho-
genic in dogs. Rickettsia belii is found in D. ander­
soni, D. variabilis, D. occidentalis, D. albipictus,
H. leporispalustris, A. cooleyi, and O. concanensis in
eight states in the U.S. Again, it is maintained in
nature by small mammals.
A species of tick can harbor more than one
serotype of Rickettsia. However, experimental evi-
dence shows that a serotype present in a given tick
interferes with the establishment of another
serotype of Rickettsia. This phenomena is termed
rickettsial interference. Ticks are considered the
reservoir of infection in rickettsial diseases. This
is due to the fact that infected animals remain
rickettsemic for just several days and horizontal
transmission of rickettsiae from an infected
animal to a feeding tick is not as efficient as trans-
stadial and transovarial transmission. Venereal
transmission of rickettsiae in ticks during mating
does not occur.
Treatment of rickettesial diseases is greatly
dependent on the proper early diagnosis of the
disease. Several effective antibiotics exist includ-
ing tetracyclines, doxycyclines, chloramphenical,
chloromycetin and cotrimexazol.

The most severe disease caused by SFG rick-
ettsiae is Rocky Mountain Spotted fever (RMSF)
caused by R. rickettsii. This disease is covered in a
separate entry. The other human diseases caused
by SFG rickettsiae are discussed below.
Boutonneuse Fever (BF) (=Mediterranean
spotted fever, Fievre Boutonneuse, Marseilles
fever, Kenya tick typhus, South African tick bite
fever, Indian tick typhus) is caused by Rickettsia
conorii, which is closely related to R. rickettsii. BF
is widely distributed in Southern Europe, Africa,
Western and Central Asia and India. It can be
transmitted by many species of hard ticks. The
principle vector in the Mediterranean is R. san­
guineus, while in southern Africa, R. evertsi, A.
hebraeum, H. leachi and R. sanguineus transmit
the disease. In India, I. ricinus, H. leachi and R.
sanguineus are vectors. BF is maintained in nature
by a wide variety of smaller mammals. It is prin-
cipally a seasonal disease. Endemic areas exist in
Israel and throughout Africa. The disease is char-
acterized by chills, fever, lymphadenitis, headaches
and joint and muscle aches following a 5- to 7-day
incubation period. Fever can reach 40°C. A dis-
tinctive ulcer, known as a tache noire, is covered
with a black crust and appears at the site of the tick
bite. Untreated cases recover, but some virulent
strains can result in death. The pathology is simi-
lar to RMSF, but milder. Vaccines are not available.
Control of ticks on dogs is the most effective
method of preventing the disease.
North Asian Tick Typhus (NATT), is caused
by Rickettsia siberia, and is transmitted by species
of Dermacentor, Hyalomma and Haemaphysalis.
The most common are D. marginatus, D. silvarum,
D. reticulatus, D. nuttalli, Hy. asiaticum, Hy. japoni­
cum, H. punctata and H. concina. NATT occurs
from Siberia to Mongolia, and from Central Asia
to Eastern Europe. Natural foci of this diseases
exist in populations of small mammals. Ticks can
harbor R. siberia for long periods of time. The
pathogen is moved through the tick’s life cycle by
transstadial and transovarial transmission. In the
former Soviet Union, NATT most commonly
occurs in farm workers. It occurs from spring to
Ticks (Acari: Ixodida)
T 3797
fall. After an incubation period that lasts about a
week, the disease manifests as chills and a fever
that becomes intermittent after about a week. A
small lesion may develop at the tick bite. A rash
appears on the extremities and spreads to the
trunk.
Queensland Tick Typhus (QTT) is caused by
Rickettsia australis and transmitted by I. holocy­
clus, and possibly other species of this genus. The
disease occurs in Queensland, Australia, mostly in
a savanna habitat with intermittent rain forest. A
large population of rodents and marsupials is nec-
essary to support the tick population. QTT is a
mild disease. The incubation period varies from a
few days to over a week. QTT manifests as a gen-
eral malaise, headache and a mild fever pattern
that is often remittent. The tick bite site shows an
eschar, a lesion similar to that of the tache noire
seen in Boutenneuse fever. Nearby lymph nodes
are enlarged and painful. A variable rash appears.
Q-Fever (QF), also known as nine mile fever
or the Balkan grippe, is caused by the rickettsiae
Coxiella burnetii, and is transmitted by many spe-
cies of hard and soft ticks. The disease was first
recognized in Australia in 1936, where the Q in
Q-fever came from the word “Query.” The disease
is world wide in distribution, except in Antarctica.
The pathogen is found in small mammals, reptiles,
birds and domestic animals. Rickettsia are shed in
the feces of infected animals. Unlike other mem-
bers of the Rickettsia, C. burnetii can survive long
period outside the host cells. It is believed to be
able to survive up to 6  years in tick feces. This
hardiness may be due to the presence of a spore-
like cell in its life cycle. Coxiella burnetii is only
secondarily transmitted by ticks. Most commonly,
it is transmitted through airborne transmission,
consumption of infected milk, handling of con-
taminated wool or hides, infected animal feces,
animal bedding and contaminated clothing. The
most susceptible people are agriculture and labo-
ratory workers where sheep and goats are used for
scientific experiments. The pathogen can enter the
body through abrasions in the skin, inhalation in
the lungs, mucous membranes, the gastrointestinal
3798
T Ticks (Acari: Ixodida)
tract and possibly placental transfer. The disease
has an incubation period of about 20 days. It starts
with a sudden fever of 38–40°C which may last for
up to 2  weeks and can have a biphasic pattern.
Headache, diarrhea, sore throat, sweats and chills
also occur. A rash is usually absent, but when it
occurs, is found on the trunk and shoulders. Pneu-
monia can occur in some areas with acute Q-fever.
Mortality rates usually are less than 1%, and a vac-
cine exists.
Ehrlichia are obligate, intracellular parasites
of white blood cells, especially monocytes. They
cause ehrlichiosis, a serious and sometimes fatal
blood disease in animals and humans. Canine
ehrlichiosis, caused by Ehrlichia canis, and trans-
mitted by R. sanguineus, is found world wide. Fol-
lowing an incubation period of about 2 weeks, the
infected dog has a fever that can reach 40.5°C,
edema, anorexia, conjunctivitis and pancytopenia.
Dogs lose weight. In most breeds, the disease
has a mild form, but in German shepherds, it may
produce a severe hemorrhagic condition known
as tropical canine pancytopenia. Ehrlichiosis
can  persist in dogs for years without clinical
­symptoms. E. ewingii causes canine granulocytic
ehrlichiosis, a similar but less severe disease.
E.  (=Cytoecetes) phagocytophila, is transmitted to
cattle and to sheep by I. ricinus. The disease, known
as tickborne fever, manifests itself in weight loss,
reduced milk production and sometimes abortion.
It occurs in Ireland, Great Britain and is widely
distributed in Europe. This disease can make
young animals, especially lambs, susceptible to
other more serious diseases. E. chaffeensis causes
human ehrlichiosis. The pathogen is believed to be
transmitted by Amblyomma americanum and
D. variabilis, but the vector has not been proven.
The disease in man is similar to RMSF. However,
in human ehrlichiosis, a rash occurs in less than a
33% of patients, and a rash on the palms and feet
occurs in less than 5% of patients, which differs
from the rash found in RMSF. E. equi, which is
transmitted by I. pacificus, causes equine granulo-
cytic ehrlichiosis in horses and a wide variety of
other mammals in California. Several Ehrlichia
have unknown vectors, but all are assumed to be
transmitted by ticks. Examples are E. risticii, which
causes equine monocytic ehrlichiosis (=Potomac
horse fever); E. bovis, from cattle; E. platys, which
infects canine blood platelets; and E. senetsu, which
causes ehrlichiosis in humans in Japan.
Two important livestock diseases are heart-
water, which is caused by Cowdria ruminantium,
and anaplasmosis, which is caused by three species
of Anaplasma. Two other species of rickettsiae are
transmitted by ticks. Aegyptianella pullorumn is
transmitted by species of Argas, especially A. persi­
cus, and causes a disease of fowl that can be severe
in young chickens. Haemobartonella canis, trans-
mitted by R. sanguineus, is found in the red blood
cells of dogs, but is not associated with any pathol-
ogy. H. canis is widely distributed throughout the
world. It is transmitted by R. sanguineus.
Ticks transmit pathogens from four genera of
bacteria other than Rickettsia. These are Borrelia,
Francisella, Klebsiella and Staphylococcus. Borrelia
are helically coiled, Gram-negative, motile spiro-
chetes that cause Lyme disease, several types of
relapsing fever, epizootic bovine abortion, bovine
borreliosis and fowl (avian) spirochetosis. Borrelia
are similar to the spirochetes that cause syphilis
and Leptospirosis. Lyme disease is covered in a
separate entry.
Several species of Borrelia cause tick borne
relapsing fever, a disease known since ancient
times. Each of these species of Borrelia is transmit-
ted by a given species of soft tick. Some species of
Borrelia are transmitted in the coxal fluid of their
vectors, but other vector species do not produce
coxal fluid until they leave the host and, therefore,
transmission must follow a different route. Some
vectors, such as O. hermsi and O. turicata, transmit
the spirochetes in their saliva. In Africa south of
the Sahara, B. duttoni is transmitted by Orni­
thodoros moubata. In Spain, Portugal and north-
ern Africa exclusive of Egypt, B. hispanica is
transmitted by O. erraticus and causes Hispano-
African relapsing fever. In Morocco and Libya,
B.  crocidurae is transmitted by O. erraticus, and
causes North African relapsing fever. O. erraticus

also transmits B. merionesi in Egypt and Senegal,
B. microti in Kenya and Turkey, and B. dipodilli in
Iran. All cause relapsing fever. B. persica is trans-
mitted by O. tholozani, from China through India
and Iran to areas of the former USSR into Egypt. It
causes Asiatic-African relapsing fever. B. caucasica
is transmitted by O. verrucosus from the Caucasus
to Iraq, and causes Caucasian relapsing fever.
B. latyschewii is transmitted by O. tartakovskyi in
Iran and central Asia, and causes relapsing fever.
American tickborne relapsing fever is caused by at
least six different species of Borrelia: B. hermsii is
transmitted by O. hermsi in the Western U.S.;
B.  turicatae is transmitted by O. turicata in the
southwestern U.S.; B. parkeri is transmitted by
O. parkeri in the western U.S.; B. mazzotti is trans-
mitted by O. talaje in the southern U.S.; and B. ven­
ezuelensis is transmitted by O. rudis in Central and
South America. Relapsing fevers are zoonoses that
involve the circulation of the Borrelia between res-
ervoir hosts and vector species of Ornithodoros.
With one exception, the primary reservoir hosts of
all species of Borrelia that cause tick borne relaps-
ing fevers are species of rodents, chipmunks and
squirrels. The exception is B. duttoni, which has
humans as its primary reservoir host. This form of
relapsing fever is endemic in Kenya and other East
African countries because the vector O. moubata
has adapted to human dwellings, especially the
huts made of mud or straw. Studies on the DNA of
the relapsing fever Borrelia suggest that all species
are closely related.
All tick-borne relapsing fevers have similar
clinical features and pathology. Relapsing fever spi-
rochetes migrate rapidly from the bite site into the
hosts circulatory system. An incubation period
lasts from 2 to 18 days. Symptoms appear abruptly
and include headache, fatigue, chills and fever that
can be as high as 41°C. Subsequent periods of fever
are relapses. The first attack lasts about 3 days, fol-
lowed by another after 7  days, and one or more
attacks after that. The virulence of the disease abates
with secondary relapses, which tend to be shorter
and milder. Relapses are probably due to the patho-
gen’s change in its antigenicity thus evading the
Ticks (Acari: Ixodida)
T 3799
host’s immune system. Relapsing fevers are treated
with antibiotics. Because all Ornithodoros that
transmit relapsing fever Borrelia are nidicolous,
humans are incidental hosts and are not involved in
the zoonotic cycle. Relapsing fevers are enzootic
and occur in humans as scattered local outbreaks.
Epizootic bovine abortion is caused by B. cori­
acease, and is transmitted by O. coriaceus. It is a
serious problem in the western U.S. Bovine borre­
liosis, caused by B. theleri, is transmitted by the
Boophilis species and R. evertsi. Fowl or avian spi-
rochetosis is caused by B. anserine, and is trans-
mitted by A. persicus, A. reflexus, and A. miniatus.
All are species of the Argas subgenus Persicargas.
The disease is pathogenic for most domestic fowl,
but less so for guinea fowl and pigeons. It occurs
world wide mostly as an endemic disease.
Francisella tularensis causes tularemia, which
has a worldwide distribution. The most common
mammals with the disease are cottontail rabbits,
muskrats and rodents. Many species of ticks can
transmit the disease. The pathogen undergoes
transovarial transmission in ticks. In the U.S., the
disease is most commonly associated with rabbit
hunting. Transmission can occur in three ways:
through the skin, through inhalation of the patho-
gen and through contaminated water or meat.
Each method of transmission produces a distinct
form of the disease. Entry of the pathogen through
the skin from the bite of a tick results in the
ulceroglandular form of tularemia. Following a
2-day incubation period, the patient has a fever of
up to 41°C, accompanied by chills and shaking.
The fever plus enlarged lymph nodes (buboes)
and severe headache can last up to a month in
untreated patients. A vaccine exists, but must
be  administered every 3  years and is not always
protective. Streptomycin is effective. Klebsiella
paralytica, transmitted by D. albipictus, causes
moose disease in North America. The disease is of
limited importance. Staphylococcus aureus, trans-
mitted by I. ricinus, causes tick pyaemia in sheep
in Britain. This disease is not widespread or very
pathogenic, and ticks may not be necessary for its
transmission.
3800
T Ticks (Acari: Ixodida)
The protozoan class Piroplasmea contains the
genera Babesia and Theileria. All of whose species
are transmitted by ticks. These are parasites of ver-
tebrate blood cells and cause piroplasmosis such
as human babesiosis and east coast fever in cattle.
Control of Ticks
The high reproductive rate, host variability, wide
dispersion, secretive habits and longevity of many
ticks make control difficult. Strategies for tick con-
trol involve the reduction of transmitted diseases
and the reduction of numbers of ticks on animals
to an acceptable economic level. Surveillance of
ticks in a given area, which involves determining
the species, their population density and any
pathogens present, is an important part of any
control strategy. Control measures have included
one or more of the following: use of pesticides,
vaccination of susceptible animals, environmental
management, and protection of individual humans.
The latter, coupled with education about the spe-
cies of tick present and its life cycle, is probably the
most effective measure to prevent transmission of
tick-borne diseases to humans. Biological control,
which has proven valuable in controlling many
insect pests, has so far not been of much use in
controlling ticks. Some parasitic wasps have been
released in an attempt to control D. variabilis in
the northeastern U.S., but this has not proven
effective. Oxpeckers are natural agents of biologi-
cal control and, in Africa, consume large numbers
of ticks from ungulates. Likewise, fire ants will eat
ticks. How these natural enemies can be used by
man to control ticks is unclear.
Pesticides
Pesticides (=acaricides) are applied by spraying a
given area, or more commonly, by dipping or
spraying individual domestic animals. Other
methods of application use a systemic acaricide, or
involve controlled delivery systems such as collars
impregnated with a slow releasing acaricide. The
use of acaricide impregnated cotton fibers that are
taken by wild mice to their nests has been success-
ful in reducing populations of Ixodes scapularis; or
the use of baited stations that dispense the acari-
cide to the animal when it takes food from the
device has been successful in controlling tick pop-
ulations on domestic livestock in some regions
and on deer in the southwestern U.S. The develop-
ment of resistance to acaricides in recent years and
their adverse environmental effects have prompted
the use of other means such as vaccines and envi-
ronmental management to control ticks. Other
strategies use pheromones or CO2 to attract ticks
to stations containing pesticides.
Vaccines
Several commercial vaccines against ticks now
exist. These all take advantage of the fact that host
IgG in the midgut of the tick is immunologically
competent, and is transported through the midgut
as such into the hemolymph of the tick. The most
effective vaccines use concealed antigens. These
are antigens from the tick that the host has never
been exposed to before being vaccinated. Con-
cealed antigens usually require booster shots of
the vaccine.
Environmental Management
Ticks need a suitable habitat and suitable hosts for
an abundant population to develop. Habitat modifi-
cation involves controlled burning, use of herbicides,
mowing to destroy vegetation, and plastering to seal
cracks and crevices in human dwellings. The latter is
an effective control on some species of nidicolous
ticks such as Ornithodoros moubata. Indigenous
herdsman in Africa have used controlled burning
for centuries to limit ticks that attack cattle. In some
cases, removal of vegetative litter and opening up
the ground to intense sunlight by altering the forest
canopy has been effective. Reducing or denying

hosts is most effective when the target area is iso-
lated and has little possibility of their reintroduction.
If a wildlife host exists, control of ticks in an area is
very difficult, although fencing has been used with
some success to exclude large wildlife hosts such as
the Cervidae. It is possible to keep domestic animals
out of tick infested areas by rotating pastures.
Protecting Humans
Protecting humans against ticks involves prevention
of infestation, and proper removal of attached ticks.
Within the urban environment, measures to prevent
infestation include strategies to kill and repel ticks
inside the home and on companion animals. In the
home, foggers and sprays for the house and yard are
important. Topical repellants and sprays, anti-tick
collars and shampoos are effective means of killing
and repelling ticks on dogs and other companion
animals. Measures that prevent infestation outside
the urban environment involve avoidance of heavily
infested areas, especially during high tick activity. If
this is not possible, then tucking trousers into
exposed socks using some sticky tape and the use of
repellents to clothes and or exposed skin (follow the
directions on the label). Complete inspection of
one’s person immediately after leaving the area is
essential. Ticks prefer the area around the waist, the
axillary region, the genital and perianal region, the
neck and the head. It is important to know how to
remove ticks because improper removal can result
in secondary infections and, in some cases, the trans-
mission of pathogens from the tick to the person
removing the tick. Attached ticks should be removed
by placing tweezers between the tick and the skin of
the host and pulling slowly and gently up until the
tick is removed. Once removed, the tick should be
examined to make certain that the mouthparts are
not still in the host. Once removed, the tick should
be saved. Preserve the tick in a container with 70%
ethanol or rubbing alcohol. Preserved in this man-
ner, a physician or scientist can identify the tick, and
also determine if it is capable of transmitting a dis-
ease. Following removal, the bite area should be
Ticks as Vectors of Pathogens
T 3801
cleaned, an antiseptic applied and the area covered
with a small dressing.
 Mites
 Acaricides or Miticides
 Ticks as Vectors of Pathogens
 Tick Paralysis
References
Coons LB, Alberti G (1999) The Acari-ticks. In: Harrison FW,
Foelix R (eds) Microscopic anatomy of invertebrates.
Chelicerate Arthropoda, vol. 8B. Wiley-Liss, New York,
pp 267–514
Sonenshine DE (1991) Biology of ticks, vol. 1. Oxford Univer-
sity Press, New York, 447 pp
Sonenshine DE (1993) Biology of ticks, vol. 2. Oxford Univer-
sity Press, New York, 465 pp
Sonenshine DE, Mather TN (eds) (1994) Ecological dynamics
of tick-borne zoonoses. Oxford Unversity Press, New
York, 447 pp
Marquardt WC, Demaree RS, Grieve RB (2000) Parasitology
and vector biology, 2nd edn. Harcourt, New York, 702 pp
Ticks as Vectors of Pathogens
Sarah Randolph
University of Oxford, Oxford, United Kingdom
Worldwide, ticks transmit an exceptional number
and diversity of micro-parasites (viruses, bacteria,
rickettsia, protozoan parasites, even filarial worms)
that cause disease in humans and their livestock. In
temperate regions, ticks surpass insects in impor-
tance as vectors, and a number of “new” tick-borne
pathogens recently have been recognized as causing
human disease in the northern hemisphere. These
include the spirochete bacteria (Borrelia burgdorferi
s.l.) that cause Lyme disease and the rickettsia Erhli­
chia spp. In reality, however, the burden of these
infections pales into insignificance beside the medi-
cal and veterinary impact of ticks in the tropics.
Added to the ticks’ role as vectors, the direct dam-
age they do as parasites is a major brake on livestock
productivity. Together, this imposes huge economic
burdens where they can least be afforded.
3802
T Ticks as Vectors of Pathogens
Like most true vectors, ticks are blood feed-
ers, for which they are superbly designed; they cut
through the host’s skin with a pair of toothed che-
licerae and suck up body fluids from the sub-der-
mal lesion through a hypostome. Yet as vectors,
ticks appear to rather poorly designed, lacking the
high mobility and frequent feeding habits charac-
teristic of most insect vectors. Ticks have no wings,
nor do they jump. Nidiculous (nest-dwelling)
Argasid (soft) ticks live in semi-permanent, or
seasonally repeated, close association with their
hosts. Most Ixodid (hard) ticks are not nidiculous;
typically they climb to some vantage point on the
vegetation from where they contact a passing host,
a procedure that exposes them to considerable
moisture stress. Intermittently, they must return to
the ground where they can absorb water from the
moist air, but this is energetically expensive.
Ticks minimize the costs of achieving contact
with their host by taking very few, very large meals.
This is taken to extreme by Ixodid ticks, which feed
once per life stage, as larvae, nymphs and adults,
and reproduce once after the adult meal. Most ticks
drop to the ground after each meal, where they
develop to the next stage. Some species take both
the larval and nymphal meals from the same host,
and Boophilus ticks, worldwide vectors of cattle
1 Female
+1 male
~20% Survival
Vertebrate
host
10 Nymphs
Trans-stadlal
maintenance
Ticks as Vectors of Pathogens, Figure 59  Ixodes ricinus life cycle with typical reproduction and mortality
rates and pathogen transmission cycle.
babesias, take all three meals from the same indi-
vidual host before dropping back to the ground.
Each meal is enormous; even after concentrating
the blood by returning 30–70% of the imbibed fluid
to the host via salivary secretions, on average imma-
ture tick stages increase their body weight by about
one order of magnitude, and adult females by two
orders of magnitude. To accommodate such a large
volume of blood, ticks secrete new endocuticle dur-
ing a long phase of very slow blood intake, before
engorging rapidly toward the end of the meal that
typically takes from about 4 (immature stages) to 14
(adult females) days to complete. This prolonged
feeding itself incurs a cost as hosts mount strong
hemostatic and immunological defenses; in
response, tick saliva contains an impressive cocktail
of pharmacologically active components. At the
same time, the large volume of saliva can transport
large numbers of infective parasites, whose infectiv-
ity is enhanced by their entering the host at an
immuno-modulated site (Fig. 59).
To exploit as a vector an hematophage that
feeds only once per life stage, a parasite must survive
trans-stadially. It is acquired from an infected host
by a tick of one stage, maintained through the tick’s
development and moulting processes, and trans-
mitted to a new host by the following tick stage.
Trans-ovarial
transmission
2000 eggs
~10% Survival
100 Larvae
~10% Survival

The parasite’s transmission cycles are thus deter-
mined by the tick’s stage-specific host relationships
(larvae that acquire infections from one host spe-
cies may later feed as nymphs on hosts of a different
species) and rates of development, survival and
reproduction. An infection in one host acquired by
many feeding larvae may be retained and transmit-
ted to several new hosts by individuals of one or
both of the succeeding stages, nymphs and adults.
This achieves horizontal amplification between ver-
tebrate hosts, but as only about 10% of ticks survive
from one stage to the next, this route is more lim-
ited than it may at first appear. On the other hand,
those parasites that are passed trans-ovarially, from
females via the eggs to larvae of the next generation,
can exploit the tick’s impressive fecundity (several
thousand eggs) to achieve considerable potential
for vertical amplification of prevalence in addition
to any horizontal amplification. Even though trans-
ovarial transmission is usually inefficient, with less
than 20% of an infected tick’s larval progeny being
infected, nevertheless the abundance of larvae (typ-
ically 100 times more numerous than adult ticks
and 10 times more than nymphs) can make this
route quantitatively significant.
Due to these biological peculiarities of ticks, the
quantitative framework (i.e., model) for estimating
the transmission potential of tick-borne pathogens
differs from that for insect-borne pathogens. The
tick’s feeding pattern makes the concept of an indi-
vidual’s daily biting rate inappropriate, but, most
importantly, it introduces a long delay between
acquisition and transmission of an infection. The
off-host inter-stadial period, comprising both post-
engorgement development and questing for the next
host, is functionally equivalent to a very long extrin-
sic incubation period as the tick is not infective until
it is ready to feed again. This period is specific to the
vector rather than to the transmitted parasite, and
may last from one month to more than a year depend-
ing on the tick stage, the temperature-dependent
rate of development and whether diapause occurs.
Ticks are renowned for their longevity.
Engorged ticks must survive the long, temperature-
dependent inter-stadial development periods, and
Ticks as Vectors of Pathogens
T 3803
unfed ticks must survive the long period while they
quest for hosts, which may not always be available
just when and where the tick needs them. Unlike
insect vectors, however, a tick’s vectorial capacity
does not increase proportionally with a prolonged
life-span. This is because however long an individ-
ual tick survives, it does not feed on and infect more
than one host per life stage. Although tick longevity
(which may exceed that of smaller host species such
as rodents) ensures an enduring reservoir of infec-
tion, it slows the pace of transmission, because long
survival as any one life stage increases the delay
between acquisition and transmission of infection.
An important limiting factor on the transmis-
sion potential of any parasite is the period of host
infectivity, determined by rates of host mortality
and recovery from infection. If the transmitted
parasites are highly virulent, high daily mortality
rates of infected hosts may significantly reduce
transmission potential. If a host dies prematurely,
the feeding ticks will not complete their blood
meals. The risk of killing their hosts is avoided by
those tick-borne viruses that limit their infection
to a non-lethal, non-systemic form (i.e., limited to
certain parts of the host’s body) that is, neverthe-
less, highly transmissible to ticks over short peri-
ods of time. The quantitative impact of this
transmission route arises from the large numbers
of infectible ticks that co-feed with an infected tick
at sites of localized infection. This is a natural fea-
ture of tick-host interactions, as prolonged meals
taken on certain preferred parts of the host’s body
result in very large aggregations of ticks feeding
close together on some host individuals. The
immuno-modulatory effects of saliva secreted by
so many co-feeding ticks further facilitate this
transmission route. Although first recognized for
tick-borne viruses, this route has now been identi-
fied for B. burgdorferi s.l., and shown to be suffi-
cient to allow sheep to support natural cycles of
Lyme borreliosis in the absence of other, systemi-
cally infected hosts.
Whereas insect vectors are viewed as the
bridge between reservoir vertebrate hosts, the
identity of reservoir host and bridge is reversed for
3804
T Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)

the many parasites that survive in their long-lived Taxonomy

tick vectors rather than in vertebrates. A multitude
of specific parasite-vector-host interactions have
clearly evolved to allow many micro-parasites to
exploit the transmission potential offered by ticks,
even though ticks are not endowed with the fea-
tures we normally associate with insect vectors.
 Ticks
References
Nuttall PA (1998) Displaced tick-parasite interactions at the
host interface. Parasitology 116:S65–S72
Randolph SE (1998) Ticks are not insects: consequences of
contrasting vector biology for transmission potential.
Parasitol Today 14:186–192
Randolph SE, Gern L, Nuttall PA (1996) Co-feeding ticks: epi-
demiological significance for tick-borne pathogen
transmission. Parasitol Today 12:472–479
Sonenshine DE, Mather TN (eds) (1994) Ecological dynamics
of tick-borne diseases. Oxford University Press, Oxford,
447 pp
Most modern taxonomists believe that tiger beetles
should be considered a subfamily of the beetle fam-
ily Carabidae (ground beetles). Historically they
have been considered a family (Cicindelidae) sepa-
rate from other ground beetles, due largely to their
easily recognizable features and appeal with collec-
tors. Many workers have now accepted the close
relationship of this group to the ground beetle sub-
family Carabinae. This is in agreement with many
larval and adult structural characters. Throughout
the history of the classification of the group, this
close association has been maintained. It is more a
matter of personal opinion whether this group
should or shouldn’t be recognized as a separate fam-
ily. As there are no set rules for the determination of
family rank, their status remains a matter of opinion
pending further cladistic analyses (Fig. 60).
Tiger beetles are usually placed in the family
Cicindelidae Latreille, 1804, or as a subfamily of
the ground beetles, as Cicindelinae. Historically,

Tiger Beetles (Coleoptera:

Carabidae: Collyrinae and
Cicindelinae)

Paul M. Choate
University of Florida, Gainesville, FL, USA

Tiger beetles are very active, predaceous beetles.

Often brilliantly colored, they derive their com-
mon name from the fierce appearance of their large
mandibles and protruding eyes. Their popularity
among scientists and the general public stems from
their relatively large size, accessibility for observa-
tion and study, available literature for many parts
of the world, and a reasonably stable classification
system. An entire journal, CICINDELA, is devoted
to this group of beetles. Many web sites are devoted
to various aspects of these insects, and many color-
ful photographs have been posted for internet Tiger Beetles (Coleoptera: Carabidae: Collyrinae
viewing. Conservationists are using species of tiger and Cicindelinae), Figure 60  Head of Cicindela
beetles as bio-indicators, and more than a few spe- illustrating characters used to separate tiger
cies are now included on endangered species lists. beetles from other ground beetles.
 Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
T 3805

the following families were also proposed to
incorporate new taxa (currently considered tribes):
Collyridae Hope, 1838; Ctenostomidae Castelnau,
1835; Mantichoridae Castelnau, 1835; and Mega-
cephalidae Castelnau, 1835.
Tiger beetle suprageneric classification is
reasonably stable (tribes). Generic classification is
very unstable, however, due primarily to the 1954
splitting of Cicindela into many genera, based
solely on male genitalia characteristics. Thus,
many genera are not readily identifiable. Species
definition within each genus is oftentimes also
problematic. There are a great many subspecies
and color variants, most of which are named.
Their status and synonymy is confusing. Much
work must be done before all species can be
properly understood. However, in spite of the com-
plexity of their classification, many species groups
and regional faunas have been sufficiently studied
so that now it is possible to place names on most
forms (Fig. 61). As for generic identification, there
is no modern identification key that incorporates
all of the currently accepted genera. There is
presently only Willis’ 1969 translation of Horn’s
outdated key to the world genera of tiger beetles,
which does not reflect modern supraspecific
classification.
In 2002, K. Werner published the only com-
plete world checklist of tiger beetles. His classifi-
cation scheme is reproduced here. Tiger beetles
are divided into two subfamilies, Collyrinae and
Cicindelinae. Subfamily Collyrinae is divided
into two tribes, Ctenostomini with two genera
and Collyrini with six genera. The subfamily
Cicindelinae is divided into three tribes, Manti-
corini (two genera, African only), Megacephalini
(nine genera), and Cicindelini with many ill-
defined genera resulting from the splitting of
Cicindela. The approximate geographical distri-
bution for many genera is given here. Genera are
listed in phylogenetic order (related genera
close together) according to J. Wiesner’s 1992
checklist, along with their approximate world
distribution.

Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae), Figure 61  Males of Cicindela
scutellaris unicolor (left) and C. nigrior (right), once considered to be the same species.
3806
T Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)

Modern Classification of Tiger Heptodonta Hope (SE Asia, Philippines, China,

Beetles Nepal, India, Malaysia, Indonesia)
Dilatotarsa Dokhtouroff (Indonesia, Malaysia,
Order Coleoptera Philippines, Borneo)
Family Carabidae Pronyssa Bates (India)
Subfamily Collyrinae Pronyssiformia W. Horn (China)
Tribe Ctenostomini Calyptoglossa Jeannel (Madagascar)
Pogonostoma Klug (Madagascar) Peridexia Chaudoir (Madagascar)
Ctenostoma Klug (Mexico, Central America, Physodeutera Lacordaire (Madagascar)
South America) Walthornia Olsoufieff (Madagascar)
Tribe Collyrini Stenocosmia Rivalier (Madagascar)
Derocrania Chaudoir (India, Sri Lanka) Oxygoniola W. Horn (Indonesia)
Tricondyla Latreille (India, Sri Lanka, China, SE Darlingtonica Cassola (Papua New Guinea)
Asia, Indonesia, Malaysia, Borneo, Philippines) Caledonomorpha W. Horn (Papua New Guinea)
Collyris Fabricius (India, Sri Lanka, SE Asia, Vata Fauvel (New Caledonia)
Indonesia, Borneo) Caledonica Chaudoir (New Caledonia)
Taiwanocollyris Mandl (Taiwan) Odontocheila Castelnau (S America, Central
Protocollyris Mandl (Burma, Indonesia, America)
Philippines) Cenothyla Rivalier (S America)
Neocollyris W. Horn (India, Indonesia, SE Asia, Pentacomia Bates (S America, Mexico)
Japan, Philippines, Thailand, Taiwan, Vietnam, Phyllodroma Lacordaire (Brazil)
China, Nepal, Malaysia) Cheilonycha Lacordaire (Brazil, Argentina)
Subfamily Cicindelinae Prepusa Chaudoir (Paraguay, Brazil)
Tribe Manticorini (Africa only) Opisthencentrus W. Horn (Brazil)
Mantica Kolbe (Namibia) Oxygonia Mannerheim (S America, Central
Manticora Fabricius (Namibia, S Africa, Angola, America)
Botswana, Zaire) Metopon Fleutiaux (Brazil)
Tribe Megacephalini Eucallia Guerin (Ecuador, Colombia)
Platychile Macleay (Namibia, South Africa) Euprosopus Dejean (Brazil)
Picnochile Motschulsky (Chile) Iresia Dejean (S America, Central America)
Amblycheila Say (Mexico, SW USA) Distipsidera Westwood (Australia, Papua New
Omus Eschscholtz (Canada, W USA) Guinea, Indonesia)
Aniara Hope (Trinidad, S America) Rhysopleura Sloane (Australia)
Megacephala Latreille (widespread throughout Megalomma Westwood (Mauritius, Reunion)
world) Diastrophella Rivalier (Reunion)
Oxycheila Dejean (Mexico, S America) Rhytidophaena Bates (Bangladesh, India, Burma)
Pseudoxycheila Guerin (S America, Central Langea W. Horn (S America)
America) Nickerlea W. Horn (Australia)
Cheiloxya Guerin (S America) Baloghiella Mandl (New Caledonia)
Tribe Cicindelini Therates Latreille (Indonesia, SE Asia, India,
Prothyma W. Horn (Africa, Madagascar, India, Burma, Japan, Taiwan, China, Malaysia, Philip-
Indonesia, SE Asia, Philippines, China, Taiwan) pines)
Neochila Basilewsky (Tanzania, Africa) Bennigsenium W. Horn (Tanzania, Africa)
Euryarthron Guerin (Africa) Prothymidia Rivalier (Africa)
Dromica Dejean (Africa) Chaetotaxis Jeannel (Madagascar)
 Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
Ambalia Jeannel (Madagascar)
Cicindelina Jeannel (Madagascar)
Trichodela Rivalier (Africa)
Epitrichodes Rivalier (Africa)
Trichotaenia Rivalier (Africa)
Ophryodera Chaudoir (S Africa, Angola, Zaire,
Mozambique)
Bostrichophorus Thomson (Mozambique)
Elliptica Fairmaire (Africa)
Ropaloteres Guerin (Africa, China)
Hipparidium Jeannel (Africa, Indonesia, Mada-
gascar)
Calochroa Hope (Nepal, India, Burma, SE Asia,
Philippines, Nepal, Sri Lanka)
Cicindela Linnaeus (worldwide distribution)
Lophyridia Jeannel (Turkey, Iran, Iraq, China,
Afghanistan, Syria, Africa, Japan, India)
Cosmodela Rivalier (Afghanistan, India, Nepal,
China, SE Asia, Borneo)
Plutacia Rivalier (India)
Platydela Rivalier (Morocco, S Africa)
Lophyra Motschulsky (Africa, Iran, Pakistan, Sri
Lanka, Pakistan, India, Madagascar, Italy, Turkey,
SE Asia)
Habrodera Motschulsky (Madagascar, Africa)
Chaetodera Jeannel (Madagascar, Africa)
Neolaphyra Bedel (N Africa)
Jansenia Chaudoir (India, Sri Lanka)
Thopeutica Schaum (Indonesia, Philippines)
Wallacedeala Cassola (Indonesia)
Cephalota Dokhtouroff (Central Asia, Morocco,
Spain, Greece)
Cassolaia Wiesner (Algeria, Tunesia)
Homodela Rivalier (Turkey)
Naviauxella Cassola (Burma, Thailand)
Glomera Acciavatti & Pearson (India)
Setinteridenta Acciavatti (India)
Cylindera Westwood (Japan, China, Taiwan,
Europe, Central Asia, Korea, India)
Brasiella Rivalier* (Cuba, Mexico, Central
America, S. America)
Ellipsoptera Dokhtouroff*
Dromochorus Guerin*
Myriochile Motschulsky*
Cratohaerea Chaudoir*
T 3807
Microthylax Rivalier*
Eunota Rivalier*
Habroscelimorpha Dokhtouroff*
Opilidia Rivalier*
Salpingophora Rivalier (Iran, Pakistan)
Hypaetha LeConte (Iran, Yemen, India, Somalia,
Australia)
Abroscelis Hope (China, SE Asia, Indonesia,
Philippines, Taiwan)
Callytron Gistl (Pakistan, India, Iran, S Korea,
Taiwan, Japan, Malaysia, Burma, Philippines)
Enantiola Rivalier (Indonesia, Malaysia)
Notospira Rivalier (Burma)
Neocicindela Rivalier (New Zealand)
Euzona Rivalier (Australia)
Antennaria Dokhtouroff (Australia)
Marcfarlandia Sumlin (Australia)
Micromentignatha Sumlin (Australia)
Archidela Rivalier (Australia, Papua New
Guinea)
Grandopronotalia W. Horn (Australia)
Rivacindela Nidek (Australia)
Parapolyrhanis Rivalier (Fiji)
Polyrhanis Rivalier (Indonesia, Papua New
Guinea)
Oceanella Rivalier (Fiji)
Orthocindela Rivalier (Indonesia, Papua New
Guinea)
Guineica Rivalier (Indonesia)
Leptognatha Rivalier (Indonesia, Papua New
Guinea)
Eurymorpha Hope (Angola, Namibia, S Africa)
Apteroessa Hope (India)
(*genus treated as a subgenus of Cicindela by many
authors)
Description
Most species have conspicuous eyes, long legs,
and frequently display brilliant colors, a char-
acteristic shape, rapid locomotion, and nervous
behavior. The body is elongate or round, with a
large head and prominent eyes. Their size
3808
T Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)

ranges from 6  mm to over 70  mm (Manticora and other mouthparts also are large (Fig.  64).
latipennis – South Africa) in length (Fig.  62). The eyes vary from very small to very large and
Their color often includes iridescent markings, prominent.
though some genera are uniformly brown or The pronotum is variously shaped, but is
black (Omus, Amblycheila, Mantica, Manticora). narrower than the elytra, usually cylindrical,
Body hair is usually sparse, though sometimes and without lateral margins or (rarely) with lat-
with long, stout setae, especially on legs and eral margins. The legs are long and slender, and
mouthparts.
The head is variously shaped, prominent,
but not elongate. The antennae are filiform, long
and slender, with eleven segments (Fig. 63). The
mandibles are stout, toothed, sometimes very
large and prominent, much larger than the head,

Tiger Beetles (Coleoptera: Carabidae: Collyrinae and

Cicindelinae), Figure 62  Intrapopulation variation
in Cicindela dorsalis saulcyi from Carabelle Beach,
Florida, USA.

Tiger Beetles (Coleoptera: Carabidae:

Collyrinae and Cicindelinae), Figure 64  Face of
Tiger Beetles (Coleoptera: Carabidae: Collyrinae adult tiger beetles showing prominent
and Cicindelinae), Figure 63  Head of male toothed mandibles: (above) Megacephala
Manticora latipennis. carolina; (below) Cicindela marginata.
 Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
well suited for running. The tarsal segment
­formula is 5–5–5. Tiger beetles display typical
carabid-type wings; the elytra cover the abdo-
men, and sometimes are connate, rounded
behind, and sometimes possess lateral margins.
The wings may be present or absent.
The abdomen of tiger beetles is sometimes
narrow, with elytra covering the sides, with four
to six visible ventral sternites. Male genitalia are
highly modified, carabid-like tri-lobed parameres
with a separate pars basalis (unlike that found in
other ground beetles) entirely separate from the
base of the penis and forming a lateral connection
between the parameres at a mid-point. Larvae are
distinguished by two or three pairs of hooks pres-
ent on the tergum (top) of the fifth abdominal
segment (Fig. 65).
Tiger Beetles (Coleoptera: Carabidae: Collyrinae
and Cicindelinae), Figure 65  Tiger beetle larva.
T 3809
Members of Cicindelinae are separated from
other Carabidae by a combination of the following
characters: clypeus laterally extending beyond
antennal insertion, both spurs of protibiae apical,
and larvae with dorsal hooks on fifth abdominal
tergite (dorsal plate). Consistent treatment of the
families of beetles requires that these beetles be
placed within the rest of the ground beetles.
Species Numbers and Distribution
There are approximately 2,100 described species
found in all regions of the world except Hawaii,
Antarctica, Maldives Islands off the southern tip
of India, and Tasmania (Table 12). They occur at
elevations from −60 m to over 4,000 m. The Indian
subcontinent is home to the largest number of
species of tiger beetles.
Fossil Records
There are very few tiger beetle fossil records.
Some published records are suspect; their iden-
tity may not be correct, and there is even evi-
dence that more than one record may be a fraud.
The oldest known tiger beetle fossil (Oxycheilop­
sis cretacicus Cassola and Werner) was described
in 2003 from the Santana Formation of Nova
Olinda, Brazil, Mesozoic formation, dating
from the Lower Cretaceous, ca. 120 million
years ago. Other fossil records include Oligo-
cene Baltic Amber, Quaternary from USSR
and Trinidad, Pleistocene (California, Minne-
sota, and Washington, USA) United Kingdom
(Europe), and Ontario, Canada.
Reproduction
Males visually locate potential mates. It is not
uncommon to see males attempt to mount
other males, as well as other species trying to
mate. Frequent encounters between conspecific
3810
T Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)

Tiger Beetles (Coleoptera: Carabidae: Collyrinae Tiger Beetles (Coleoptera: Carabidae: Collyrinae
and Cicindelinae), Table 12  Number of species and Cicindelinae), Table 12  Number of species
of tiger beetles known from many countries of tiger beetles known from many countries of
of the world, as reported in 1992 by Pearson the world, as reported in 1992 by Pearson
and Cassola and Cassola (Continued)
Country No. species Country No. species
Algeria 15 Malaysia 95
Angola 69 Mali 16
Argentina 64 Mauritius Island 3
Australia 81 Mexico 116
Bangladesh 53 Mongolia 23
Bolivia 86 Morocco 14
Botswana 27 Mozambique 47
Brazil 184 Namibia 31
Burma (Myanmar) 93 Nepal 64
Cameroon 43 New Caledonia 17
Central African Republic 46 New Zealand 14
Chile 6 Pakistan 33
China 94 Panama 28
Colombia 42 Papua New Guinea 72
Costa Rica 38 Paraguay 38
Cuba 11 Peru 79
Ecuador 74 Philippines 94
El Salvador 17 Réunion Island 4
Ethiopia 51 Solomon Islands 20
Fiji 2 Somalia 31
Guatemala 23 South Africa 94
Guinea-Bissau 34 Spain 16
Guyanas 29 Sri Lanka 55
Hispaniola 9 Taiwan 26
Honduras 7 Tanzania 68
India 193 Thailand 102
Indonesia 217 Togo 24
Iran 30 Trinidad & Tobago 4
Italy 17 Tunisia 14
Ivory Coast 21 Turkey 25
Japan 22 U.S.S.R. (C.I.S.) 49
Kenya 53 Uganda 33
Laos 59 USA 111
Libya 6 Venezuela 51
Madagascar 176 Vietnam 93
 Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
Tiger Beetles (Coleoptera: Carabidae: Collyrinae
and Cicindelinae), Table 12  Number of species
of tiger beetles known from many countries of
the world, as reported in 1992 by Pearson
and Cassola (Continued)
Country No. species
Western Samoa 2
Yemen 10
Zaire 134
Zambia 53
Zimbabwe 53
males result in brief wrestling/aggressive
behavior. Once a male is successful at mating,
he will frequently be seen riding on the back of
a female after mating has occurred. This is
called mate guarding, and this behavior is
believed to be used to prevent other males from
mating the same female. There also are mor-
phological differences between species that act
as interspecific barriers. A mandible coupling
sulcus occurs in many species. A combination
of male mandible shape and thoracic sulcus
on females is believed to be a selection mecha-
nism to prevent interspecific breeding. The
mandible of conspecific males fits into the sul-
cus on the female. Males of other species have
mandibles that are not fitted for female sulci
(Fig. 66).
Karyology
Karyotypes are known for fewer than 100 species of
tiger beetles, which are among the organisms with
two to four multiple X sex chromosomes. These
multiple X chromosomes are unique among insects
because they do not form chiasmata, crossover
points which allow recombination during meiosis.
Another characteristic of male chromosomes is that
they do not align in parallel during meiosis, but
rather form a conspicuous sex particle, chromo-
somes linked at their ends, forming a circle.
T 3811
Tiger Beetles (Coleoptera: Carabidae: Collyrinae
and Cicindelinae), Figure 66  Mating pair of
Cicindela dorsalis.
Development
Tiger beetles undergo complete metamorphosis,
passing through the egg, larval, and pupal stages
before emerging as adults. Eggs are laid singly by
females. Hatching occurs from 9 to 38 days after
oviposition. Larvae undergo three instars. The
newly hatched larva forms a vertical burrow in
which it will remain through pupation. Larvae for
most known species live in vertical tunnels, hold-
ing themselves with the aid of dorsal hooks on the
fifth abdominal segment. If suitable prey comes
within range of a tunnel entrance, the larva seizes
it and drops down into the burrow to feed. The
abdominal hooks also serve to anchor the larva in
its tunnel if a prey is too large to subdue. Larvae of
the Ctenostomatini (Neocollyris and Ctenostoma)
are unusual in that they develop in rotting logs
and branches or standing vegetation rather than
in burrows in the ground.
Larvae of many species have been described.
A list and key to all known tiger beetle larvae was
published by Putchkov and Arndt. The entire life
cycle from egg to adult may take as long as 4 years.
Food availability seems to be a major factor in the
rate of larval development. Many species appear
to be able to endure long periods of fasting, enter-
ing into a quiescent stage which may last for
months. Adults normally live from 8 to 10 weeks,
but some may live for several years (Manticora).
3812
T Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
Survival from Heat and Flooding
Many species inhabit extremely hot regions, where
air temperatures during the day may easily exceed
37°C. Those species that are active during hot
times of the day may exhibit a behavior known as
“stilting,” where the individual stands with legs
fully extended, keeping the insect as far away as
possible from the hot soil (Fig. 67). They may also
seek out shaded structures, or hide under debris,
or hide in leaf litter. Larvae of riparian species are
able to survive long periods of anoxia (lack of oxy-
gen) during seasonal flooding of their sandbar
and bank habitats (Fig.  68). Larval burrows may
contain sufficient oxygen to allow their inhabit-
ants to survive weeks under flood waters. The salt
marsh-inhabiting species Cicindela togata is
reported to have larvae that can survive 5 days of
burrow immersion in salt water.
Activity
Tiger beetles often run very rapidly over the ground,
frequenting sandy banks of streams, along road-
ways and paths and other such sunny places. Many
species are rapid flyers. In spite of their often bril-
liant metallic colors they are often difficult to see
because of their quick movements. Unlike most
beetles, a net is often necessary to collect these
insects. Some desert-inhabiting species can be
Tiger Beetles (Coleoptera: Carabidae: Collyrinae
and Cicindelinae), Figure 67  Cicindela hirtilabris
displaying “stilting” behavior.
collected in abundance by hand. Pitfall trapping has
also proven a successful technique for some species.
Many species are more easily collected at night with
such attractors as UV black-light or mercury vapor
lights. The use of lights to collect many of the
more elusive species has led to the demise of some
populations due to overzealous collecting. Several
species are on the verge of extinction, with over-
collecting appearing to be as responsible as habitat
destruction.
The genera Manticha and Manticora inhabit
deserts and steppes of southern Africa. A few spe-
cies of Cicindela live in termite nests. The tropical
tribes Ctenostomini and Collyrini are arboreal,
searching out their prey among the branches of
trees and bushes.
Adults of Megacephala, Amblycheila, and
Omus are crepuscular/nocturnal and are most
effectively collected with pitfall traps. Some species
Tiger Beetles (Coleoptera: Carabidae: Collyrinae
and Cicindelinae), Figure 68  Cicindela blanda, a
river sandbar species from the southeastern USA.
 Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
T 3813

of Megacephala have been reported to be attracted

to electric lights, but are usually found beneath
stones, hiding in crevices in the earth, or under
almost any debris. Megacephala affinis was
reported to prey on dung beetles in Panama. Mega­
cephala fulgida was reported to appear at sound
traps being used to attract Scapteriscus mole crick-
ets. Individuals of Amblycheila have been reported
to become active soon after sunset. Adult Omus
have been reported to be predators on millipedes.
Species of Cicindela are both diurnal and
nocturnal. Many species prefer dry sunny areas,
but others are known to prefer semi-aquatic sites.
Some species, while active both during daytime
Tiger Beetles (Coleoptera: Carabidae: Collyrinae
and night, appear to accomplish most of their
and Cicindelinae), Figure 69  Clay bank at
mating at night. Many species are strong flyers,
Thomasville, Georgia, USA, with holes marking
but some have fused elytra and are incapable of
entrances to larval burrows.
flight. Others appear reluctant to fly even though
flight wings are present.

Predators and Parasites

Larvae have only a few methods of escaping preda-

tion and parasitism. They will either drop to the
bottom of their burrow when danger approaches,
or they may even leave the burrow and run to
another location. Since they are restricted to the
one vertical burrow during their development, par-
asites are able to locate and attack larvae with a fair
amount of success. Members of the hymenopteran
family Tiphiidae (Methoca, Karlissa, and Pterom­
bus) hunt for larvae, sting them, then deposit an
egg on the paralyzed larva. The burrow is then
closed by the wasp. The parasite larva develops,
killing the tiger beetle larva. A fly family (Bomby-
liidae) also is a parasite of tiger beetle larvae. These
flies flip eggs near or into the larval burrow. Eggs
fall to the bottom of the burrow, hatch, and the new
larva attaches to the tiger beetle larva, remaining
attached until the larva pupates (Fig. 69).
Adult tiger beetles will defend against such Tiger Beetles (Coleoptera: Carabidae: Collyrinae
predators as bats, mites, lizards, other tiger bee- and Cicindelinae), Figure 70  Natural enemies of
tles, flies (Asilidae), birds, dragonflies, and, of tiger beetles: (above) robber fly (Asilidae)
course, collectors (Fig. 70). Defensive strategies predator; (below) bee fly (Bombylidae) parasitoid.
3814
T Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
include running, hiding (camouflage and cryp-
tic coloration), flying (quick short flight or long
sustained flight), dropping from the canopy
(arboreal species), displaying a warning color-
ation such as bright orange abdomen, and
chemical defenses. Many (but not all) species of
tiger beetles produce the chemical benzalde-
hyde, a chemical known to be an effective pred-
ator deterrent.
Sound Production
Some species of tiger beetles have been found
to produce sounds through stridulation. The
mechanisms behind sound production are
being investigated, and only a few species have
been analyzed. Sound production may be use-
ful in predator avoidance, or it may be part of
intraspecific communication. Two different
types of sound production have been found in
tiger beetles. One method is the scraping of a
pars stridens found on the dorsal side of costal
and subcostal veins upon a plectrum on the
ventral apical area of the elytra. Others have
rings on the elytra which are rubbed by either
the hind tibia (Manticora) or hind femur (Oxy­
cheila and Cheiloxya).
Sound Detection
Tiger beetles are capable of detecting sound. It is
believed that some species have evolved a hear-
ing organ (tympanum) to detect the hunting
sounds of bats. Not all species of tiger beetles
have tympana. When present the tympanum has
been found to be located on the dorsal-lateral
side of the first abdominal segment. It is believed
that some species use night dispersal flights to
avoid daytime predators such as robber flies,
dragonflies, and birds. This exposed them to
predatory bats. Detection of the ultrasound cries
of bats results in the tiger beetle dropping out of
the air to the ground.
Defensive Behavior
Benzaldehyde and cyanide have been identified
as defensive secretions in M. virginica. Other spe-
cies are reported to have similar defensive secre-
tions, but of 89 species investigated, only 39
produced these compounds. Other defensive
behavior includes crypsis, aposematism, evasive
running, evasive flight, deception, roosting aggre-
gations, and release of noxious chemicals from
pygidial glands. While the principal predators of
tiger beetles are believed to be birds, lizards, spi-
ders, robber flies, and bats, birds are believed to
be the major force behind selection for defensive
coloration.
Phenotypic Variation
Intrapopulation color and extent of maculation
is common among tiger beetles. This variation
has resulted in many named subspecies. The tax-
onomic validity of many of these names has not
been resolved, and many of these most likely
represent variation of little taxonomic value
(Fig. 71).
Sexual Dimorphism
Many species exhibit sexual dimorphism in
extent of maculation, degree of hairiness of the
head, number of labrum teeth, overall color, pro-
tarsal pads, shape of the elytral apex, overall body
shape and size (Fig. 72). Females tend to be larger
and wider, while males are often smaller and
narrower. Males have many more erect setae
between their eyes, and the first four segments of
their protarsi have dilated pads that are used to
hold onto females during mating. In species that
have dimorphic coloring to their labrum, males
usually have a white or pale labrum, while females
may have a totally black or dark labrum. This may
aid in mate recognition, and reduce the number
of male/male encounters (Fig. 73).
 Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
T 3815

Tiger Beetles in Folklore and

Religion

Though there are relatively few references to

tiger beetles in religious literature, the African
genus Manticora is one that has been a part of
local legends and folklore. A recent revision of
Manticora described the folklore concerning
the derivation of the name Manticora, and the
beliefs surrounding the insects by native popu-
lations. The name Manticora was derived from
the mythological beast, the Manticore. The
Manticore was a beast that had the head of a
lion, the body of a serpent, and the tail of a
scorpion. The genus Manticora was proposed
for these beetles in 1792 by Johann Fabricius.
This name was taken from the Persian for a
man-eating monster. This may have been the
result of reports of these beetles feeding on
cadavers of warriors killed in native conflicts,
or from sighting of these beetles occasionally
emerging from skulls, presumably used as hid-
ing places to avoid the midday heat. According
to native legend in southern Africa, manticoras
cannot die, and are believed to be personifica-
tion of the Grim Reaper. They are thought to
bring nothing but ruin and destruction to
native tribes. They are so feared that it is
believed that if a manticora points its mandi-
bles in the direction of a person, that person
will die within 3 days. The natives try to sneak
up behind any manticora and crush it with their
feet before it can point its mandibles in their
direction. If a person is so unfortunate as to see
a manticora, that person must undergo a lengthy
religious purge ceremony to be saved from this
demon.

Tiger Beetles on Stamps

Tiger Beetles (Coleoptera: Carabidae: Collyrinae and A few countries have used images of tiger beetles
Cicindelinae), Figure 71  Male Manticora latipennis, on their stamps. Examples of these are shown here,
70 mm long, from South Africa. Members of this with insect species name and country where used
genus contain the largest species of tiger beetles. (Fig. 74):
3816
T Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)

Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae), Figure 72  Cicindela hirticollis (left,
male; right, female) showing increased maculation in female and narrower body shape of male.

·· Vietnam – Cicindela aunulenta, Cicindela tennipes,

Cicindela japonica
·· Senegal – Cicindela lunulata
·· Ethiopia – Cicindela petiti
·· North Korea – Cicindela chinensis
·· Albania – Cicindela hybrida
·· Portuguese Guinea – Cicindela brunet
·· East Germany – Cicindela campestris
·· Madagascar – Cicindela andriana
·· Republic of Equatorial Guinea – Cicindela
purpurea
·· Democratic Republic of Congo – Cicindela regalis
·· Niger – Cicindela cicindela
·· Vietnam – Collyris collyris
·· Republic of South Africa – Cicindela regalis
·· Japan – Cicindela japonica

Conservation

Tiger Beetles (Coleoptera: Carabidae: Collyrinae The attractive appearance of many tiger beetles
and Cicindelinae), Figure 73  Female Cicindela has been one of the reasons that collectors have
unicolor. Note the elongate middle tooth and sought out specimens, sometimes to the detriment
unicolorous black color of the labrum. of populations from over-zealous collecting.
 Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae)
T 3817

Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae), Figure 74  Examples of stamps
displaying tiger beetles: (top row, left to right – Cicindela japonica, Cicindela aunulenta, Cicindela
petiti, Cicindela cicindela; bottom row, left to right – Cicindela regalis, Cicindela purpurea,
Cicindela andriana).

The biology of many species is sufficiently well
known to permit estimates of their survival status.
As a result, several species of North American
tiger beetles have been elevated for protection
under the Endangered Species Act. Among USA
endangered species are Cicindela highlandensis
Choate (central Florida), Cicindela puritana G.H.
Horn (Maryland, Connecticut), C. ohlone Freitag
and Kavanaugh (California), C. dorsalis dorsalis
Say (northeastern seacoast), Cicindela nevadica
lincolniana Casey (Nebraska), and Cicindela lim­
bata albissima Rumpp (Utah). Many other species
are listed as “species of concern,” meaning that
they are potential candidates for endangered spe-
cies status in the future as their habitats disappear.
The following list (by state) includes most of the
U.S. species that are being monitored:
·· Minnesota – (Endangered) Cicindela fulgida fulg­
ida Say, Cicindela limbata nympha Casey; (Threat-
ened) Cicindela denikei W.J. Brown, Cicindela
fulgida westbournei Calder, Cicindela lepida
Dejean; (Special concern) Cicindela hirticollis
r­ hodensis Calder, Cicindela macra macra Leconte,
Cicindela patruela patruela Dejean, Cicindela
splendida cyanocephalata Eckhoff;
·· Washington – Cicindela columbica Hatch;
·· South Dakota – Amblycheila cylindriformis (Say);
·· Texas – Cicindela chlorocephala smythi E.D. Harris;
Cicindela cazieri Vogt, Cicindela hornii Schaupp,
Cicindela nevadica olmosa Vaurie, Cicindela nigroco­
erulea subtropica Vogt, Cicindela obsoleta neojuvenilis
Vogt, Cicindela politula barbarannae Sumlin;
Cicindela politula petrophila Sumlin;
·· Nebraska – Cicindela nevadica lincolniana Casey;
·· Vermont, New Hampshire – Cicindela margini­
pennis Dejean;
·· California, Santa Cruz Co. – Cicindela ohlone Fre-
itag and Kavanaugh;
·· Massachusetts – Cicindela rufiventris hentzii
Dejean, Cicindela dorsalis dorsalis Say, C. margini­
pennis Dejean, C. patruela Dejean, C. puritana
G.H. Horn;
·· Utah – Cicindela limbata albissima Rumpp, con-
fined to the Coral Pink Sand Dunes formation in
southern Utah;
3818
T Tiger Moths (Lepidoptera: Arctiidae)
·· Ohio – C. hirticollis Say, C. marginipennis Dejean.
·· While less well-studied, a few species elsewhere
are also candidates for protection. Among those
are the following:
·· Canada, British Columbia – Cicindela parowana
Wickham;
·· Spain – Cicindela (Cephalota) deserticoloides
(Codina), endemic to the few remaining salt
steppes of southeastern Spain;
·· South Africa – Dromica spp., all species; Manti­
cora spp., all species; Megacephala asperata
Waterhouse, Megacephala regalis Boheman,
Platychile pallida (Fabricius), Prothyma guttipennis
Boheman;
·· Japan – Lophyridia angulata (Fabricius), Abroscelis
anchoralis (Chevrolat), Cicindela lewisii Bates, and
Chaetodera laetescripta Motschulsky.
Habitat destruction from encroachment by recre-
ational vehicles, housing construction, damming
of rivers, and forest harvesting are risk factors that
may eventually lead to species extinction. Even
night-lights have been investigated as potential
risk factors in the life cycle of some tiger beetles
because they draw adults from their habitat and
interrupt their mating behavior.
 Ground Beetles (Coleoptera) Taxonomy
 Beetles
References
Freitag R (1999) Catalogue of the tiger beetles of Canada and
the United States. NRC Research Press, Ottawa, 195 pp
Mares J (2002) A monograph of the genus Manticora
(Coleoptera, Cicindelidae, Manticorini). Taita, Hradec
Kralove, 208 pp
Naviaux R, Pinratana A (2004) The tiger beetles of Thailand
(Coleoptera, Cicindelidae). Sunprinting, Bangkok, 177 pp
Pearson DL, Cassola F (1992) World-wide species richness
patterns of tiger beetles (Coleoptera: Cicindelidae).
Indicator taxon for biodiversity and conservation stud-
ies. Conserv Biol 6:376–391
Pearson DL, Knisley CB, Kazilek CJ (2006) A field guide to
the tiger beetles of the United States and Canada.
Identification, natural history, and distribution of
the Cicindelidae. Oxford University Press, New York,
227 pp
Pearson DL, Vogler AP (2001) Tiger beetles. The evolution,
ecology, and diversity of the Cicindelids. Cornell Uni-
versity Press, Ithaca, NY, 333 pp
Putchkov AV, Arndt E (1994) Preliminary list and key of
known tiger beetle larvae (Coleoptera, Cicindelidae) of
the world. Mitt Schweiz Entomol Ges 67:411–420
Werner K, (1999)The tiger beetles of Africa (Coleoptera:
Cicindelidae), vol. 1. Taita, Hradec Kralove, 191 pp
Werner K (2000) The tiger beetles of Africa (Coleoptera:
Cicindelidae), vol. 2. Taita, Hradec Kralove, 208 pp
Wiesner J (1992) Verzeichnis der Sandlaukäfer der Welt
[Checklist of the tiger beetles of the world (Coleoptera:
Cicindelidae)]. Erna Bauer, Keltern, 364 pp
Tiger Moths (Lepidoptera:
Arctiidae)
John B. Heppner
Florida State Collection of Arthropods, Gaines-
ville, FL, USA
Tiger moths, family Arctiidae (including flag moths
and wasp moths), total 11,155 species worldwide,
primarily Neotropical (about 6,000 sp.); actual
world fauna likely exceeds 14,000 species. The
family is in the superfamily Noctuoidea, in the section
Cossina, subsection Bombycina, of the division
Ditrysia. There are five subfamilies among three
groups: group Pericopinina (with Pericopinae),
group Arctiinina (for Lithosiinae and Arctiinae),
and group Ctenuchinina (for Ctenuchinae and Syn-
tominae). Various specialists use other classifica-
tions. Adults small to large (8–115  mm wingspan);
tympanal organs absent or vestigial in Syntominae;
hindwings greatly reduced in some groups (wasp
moths). Maculation extremely varied, but mostly
very colorful, especially among the wasp moths
(Ctenuchinae and the Old World Syntominae)
which mimic wasps in many cases. Adults mostly
nocturnal but many are crepuscular or diurnal (Per-
icopinae, Ctenuchinae, and Syntominae). Larvae are
leaf feeders. Host plants are varied among numerous
plant families, including mosses and lichens. A few
are economic. Among the largest adults are females
of Aglaomorpha histrio, from China, while the small-
est are some of the Lithosiinae (Fig. 75).

Tiger Moths (Lepidoptera: Arctiidae),
Figure 75  Example of tiger moths (Arctiidae),
Grammia virgo (Linnaeus) from USA.
References
Bryk F, Strand E, Zerny H (1912–37) Arctiidae. Lepidoptero-
rum Catalogus, 7:1–179 (1912); 22:1–416 (1912);
26:501–900 (1922); 45:1–57 (1931); 82:1–126 (1937). W.
Junk, Berlin
Fang CL (2000) Lepidoptera Arctiidae. In: Fauna Sinica
(Insecta), 19. Science, Beijing, 589 pp, 20 pl. (in Chinese)
Holloway JD (1998) Family Arctiidae. In: The moths of Bor-
neo, 6. Malayan Nature Society, Kuala Lumpur, 101 pp,
19 + 6 pl.; Malayan Nat J 42
Jacobson NL, Weller SJ (2001) A cladistic study of the Arctii-
dae (Lepidoptera) using characters of immatures and
adults. Thomas Say Monograph. Entomological Society
of America, Lanham, 130 pp
Marmet P, Schmid J (2000) Arctiidae-Bärenspinner. In:
Schmetterlinge und ihre Lebensräume: Arten-Gefähr-
dung-Schutz. Schweiz und angrenzenden Gebiete, 3:
581–744, pl. 26–34. Pro Natura-Schweizerische Bund
fuer Naturschutz, Basel
Seitz A (1909–34) Familie: Arctiidae. Die Gross-Schmetter-
linge der Erde, 2: 37–108, pl. 9–18 (1909–10); 2(suppl.):
53–94, 278–290, pl. 1–8 (1931–34); 6: 33–230, 293–455,
469–497, pl. 9–31, 38–67 (1915–25); 10: 61–92, 105–290,
pl. 10–30 (1912–15); 14: 41–122, pl. 3–5, 8–19 (1926). A.
Kernen, Stuttgart
Watson A, Goodger DT (1986) Catalogue of the Neotropical
tiger-moths. Occas Pap Syst Entomol 1:1–71 (4 pl.)
Tillyard, Robin John
Robin Tillyard was born January 31, 1881, at
Norwich, England. He was educated at Dover
College and Queen’s College, University of
Tillyard, Robin John
T 3819
Tillyard, Robin John, Figure 76  Robin Tillyard.
Cambridge, and received a Sc.D. in 1920. He
taught math and science in Sydney, Australia,
from 1905 to 1913, and began publishing on
dragonflies in 1905. He was named a lecturer in
zoology at the University of Sydney in 1917,
and received several honors from that University
and from the Linnean Society of London. He
also served as Chief of the Biological Depart-
ment of Cawthron Institute in New Zealand,
and Chief of the Division of Economic Ento-
mology, CSIRO, Canberra, Australia. Tillyard
published nearly 100 scientific papers, on many
aspects of entomology and most orders of insects,
but was especially interested in their evolution,
in fossil insects, and in dragonflies. He also pro-
vided numerous contributions to “The illustrated
Australian encyclopedia” (1925) and “The insects
of Australia and New Zealand” (1926). Tillyard
died in 1937 (Fig. 76).
Reference
Musgrave A (1932) Bibliography of Australian Entomology,
1775–1930. Royal Zoological Society of New South
Wales, Sydney, pp 316–321
3820
T Timema Walkingsticks
Timema Walkingsticks
A family of walkingsticks (Timemidae) in the
order Phasmatodea.
 Stick and Leaf Insects
Timemidae
A family of walkingsticks (order Phasmatodea).
They commonly are known as Timema
walkingsticks.
 Stick and Leaf Insects
Timarcha latreille (Coleoptera:
Chrysomelidae, Chrysomelinae)
Pierre Jolivet
Paris, France
The leaf-beetle genus Timarcha Latreille comprises
about four subgenera, 125 species and 30 subspe-
cies, spread in eastern North America and around
the Mediterranean basin. They are absent from
Syria, Lebanon, Israel, and Egypt, where very prob-
ably European and African species once met, but
were eradicated during the Pleistocene desertifica-
tion. In Libya, it survives along the coast on the
western side and in Cyrenaica, but also survives
on some oases, 80  km south. Timarcha does not
reach or survive in the central Sahara (Hoggar,
2,918 m) where some Chrysolina live.
Fossil Timarcha, before the Pleistocene, are
unknown, but Timarcha is a very old genus, per-
haps related to the Upper Jurassic Timarchopsis,
a  Siberian fossil. The genus Timarcha combines
plesiomorphic characters (very primitive nervous
system, primitive aedeagus and tegmen, etc.) with
apomorphic ones, like the welding of the elytra in
tenon and mortise and a complete aptery. How
long has the beetle been apterous? Probably very
early, during the Cretaceous, because it is found
with Meloe (Meloidae), one of the rare beetles that
is apterous at the pupal stage.Aptery and a ­subelytral
cavity are forms of protection against heat and
water loss in many tenebrionids living in desert
and semidesert areas. Such structures reduce tran-
spiration, act as a thermal buffer for heat flow and
allows the beetle to store the maximum amount of
water possible to compensate for the loss of liquid
through reflex bleeding. Lack of flight muscles and
shortening and widening of metasternum are a
direct consequence of aptery. Pimelia spp. (Tene-
brionidae), also totally apterous, often mimic the
Timarcha spp. and there seems to be a certain con-
cordance in northern Africa between the local
Timarcha and Pimelia species. It could be more
Müllerian mimicry than Batesian, however, because
Pimelia regurgitates liquid when disturbed.
The archaic characteristics of the adult, and
morphological structures of the larvae, probably
warrant for Timarcha a subfamily of its own, the
Timarchinae, situated between primitive ones
(Aulacoscelinae, Sagrinae) and more evolved ones
(Chrysomelinae). That status has already been pro-
posed by various authors, but many others remain
hesitant and prefer the status of tribe (Timarchini)
at the beginning of the Chrysomelinae. Timarchini
would be a monogeneric tribe with four subgenera.
All other genera formerly included among the
Timarchini are now listed among the Entomos-
celina, a subtribe. No other Chrysomelinae has a
ring piece around the aedeagus, divided at its base,
with a ciliated cap-piece on the top. Several rare
chrysomeline genera show a ring piece (tegmen)
devoid of any cap piece on the top. Normally Chry-
somelinae genera and species have a v or Y-shaped
tegmen, a more evolved form of aedeagus. Farrell’s
molecular analysis of the Chrysomelinae unfortu-
nately missed Timarcha, a key genus.
The genus Timarcha probably originated in
the steppes of Central Asia, from where it has been
eliminated by the Pleistocene glaciations. It adapted
through a complicated system of egg or adult dia-
pause to Middle Europe and North America,
including middle-sized mountains. It still does not
occupy areas that were glaciated in the Pleistocene
in the U.S. and Canada (except Vancouver island)
and in Europe (below Scotland, the Baltic States
 Timarcha latreille (Coleoptera: Chrysomelidae, Chrysomelinae)
and Denmark). Species of Timarcha can survive
moderate cold, but in Normandy, for instance, one
species (T. goettingensis (Linné)) becomes active in
February when the sun shines. Most of the species
are diurnal, but some can be crepuscular or entirely
nocturnal. Timarcha punctella Marseul in Tunisia
and Libya, and T. laevigata (L.) in Morocco, are
active during the day when other species in the
North African mountains are mostly crepuscular.
Through the Middle European mountains, adults
of the subgenus Metallotimarcha Motschulsky
(T.  metallica Laicharting, T. hummeli Faldeman,
etc.) seem to be mostly crepuscular or nocturnal in
activity. In the United States and southern Canada,
adults of the subgenus Americanotimarcha Jolivet
are entirely nocturnal. During the summer, they
climb over Rubus plants at around 9 p.m. and start
to go down around 5 a.m. to hide under the trash,
fallen leaves, and near the roots of brambles. They
do the same on strawberry plants. European and
African Timarcha show abundant reflex bleeding
(haemorrhage) around the mouth and between
femur and tibia. American species, being nocturnal
and in this way being protected from most of the
predators, show a very discrete bleeding. Not only
does Timarcha blood taste bitter, but it is toxic in its
contents (anthraquinones). Also, the purely noc-
turnal species of Timarcha (the American species,
and also some of the Metallotimarcha) do not have
the elytra fused. Probably, problems of water loss
are not acute during the night.
Timarcha species fed originally on Plantago
species (P. albicans L., P. maritima L., etc.) and this
choice is maintained with most of the African and
southern European species (no data are known on
Asian Timarcha). This host selection behavior is
absent among north European and North Ameri-
can species. However, the dual choice (Rubiaceae/
Plantaginaceae) is still shown along the French
Atlantic coast with Timarcha maritima Perris
which feeds alternatively on Galium arenarium
Lois and Plantago maritima L. Many Iberian or
Moroccan species have adapted to the same diet,
Rubiaceae/Plantaginaceae, related taxonomically
and chemically, but they eventually switch to other
T 3821
related plant families: Veronica (Scrophulariaceae),
Scabiosa (Dipsacaceae) or not related: Launaea
(Asteraceae), Carrichtera, Iberis, Alyssum (Brassi-
caceae). Southern species (Sicily, Spain, Morocco)
display such adaptations, but generally Rubiaceae
(Galium, Rubia, Crucianella, Asperula, Sherardia)
along with various species of Plantago form part of
the diet. There are also reports of Timarcha metal­
lica feeding on Vaccinium spp. (Ericaceae) and other
Ericaceae. The difference in food plants between
Old and New World stocks of Timarcha, and the big
difference in chromosome formula between the
two groups, indicate a long isolation, probably since
the separation of the northern land masses of the
Atlantic in the early Eocene period. American
Timarcha feed on Ericaceae and Rosaceae.
Timarcha is a K-strategist and lays few big eggs
protected by a primitive ootheca mostly made of
buccal secretions. Aptery and suppression of flight
muscles likely allows the female to increase its egg
production. Aptery is a serious handicap in case of
fragmentation of the habitat. Once Timarcha is
eliminated from a habitat, repopulation is unlikely.
Timarcha is distributed in middle and south-
ern Europe, northern Africa and western North
America, and new species are described from time
to time in Turkey, Italy and Corsica. However,
Timarcha has completely disappeared from central
Asia, and its ephemeral and possible existence in
Teneriffe, Japan and elsewhere (Iceland) seems to
be due to accidental introduction with forage not
followed by survival. Timarcha has survived in
some big islands (Corsica, Sardinia, Sicily, Mallorca,
Minorca) and small ones (Channel Islands, Chausey
archipelago, Aegades, small islands off the coast of
eastern Spain, etc.), but has disappeared or has never
existed in the eastern Mediterranean islands, includ-
ing Cyprus and Crete. Malta remains Timarcha free,
but probably lost the beetle due to intense urban-
ization since the Greek and Roman times. It was
connected with Sicily during the Cenozoic.
Stranger is the lack of Timarcha in three small
Balearic islands, perhaps due to geological history.
Timarcha has disappeared completely from the
eastern and central USA (Fig. 77), probably during
3822
T Timarcha latreille (Coleoptera: Chrysomelidae, Chrysomelinae)

Timarcha latreille (Coleoptera: Chrysomelidae, Chrysomelinae), Figure 77  Timarcha: (a) Distribution

of the genus Timarcha in the USA and Canada. Localities in Montana are not visible on the map;
(b) Timarcha (Metallotimarcha) metallica Laicharting from Belgium; (c) Timarcha
(Americanotimarcha) intricata Haldeman, Oregon, USA; (d) Timarcha (Americanotimarcha) cerdo
Stål, Oregon, USA.

the Pleistocene, though host plants are present in
the Apalachian Mountains and elsewhere. It is also
difficult to understand why the Timarcha did not
cross the Sahara when it was vegetated, and did not
colonize the Hoggar and the East African moun-
tains as Chrysolina did. In some ways, the original
distribution of Timarcha could have been similar
to that of Pimelia and Pimeliinae in the West
before the desertification of the Middle East, with
a wider distribution toward Mauritania and the
western Sahara, plus Egypt, Sudan, eastern Medi-
terranean and western Asia.
Being protected by their toxic fluid (by regur-
gitation) and prebuccal and tibio-femoral reflex
bleeding (by anthraquinones) and eventually
also by a nocturnal life, Timarcha spp. have few
parasites and parasitoids (Ichneumonidae and
Braconidae), mites under the subelytral cavity
(Canestriniidae) and microbial commensals:
gregarines. Practically no predators (birds, lizards)
feed on them. When resting during the cold
season in the Mediterranean, adults of Timarcha
often gather together under tufts of plants, showing
a tendency to gregarism.
American and European species of Timarcha
differ in number of chromosomes, the American
species having a much greater number. The basic
formula in Europe is: 2n  =  12 and in America:
2n = 44.
The black body color of Timarcha and the red
blood extruded abundantly likely have an apose-
matic effect because of the contrast with the green
background of the food plant. However, aposema-
tism is of no use for nocturnal species.
The size of Timarcha adults varies from
5–8  mm (T. cerdo) to 18–23  mm (T. tangeriana
Bechyne). Generally a size of 10–12 mm (T. goet­
tingensis (L.)) is common.
Conclusions
The genus Timarcha remains rather enigmatic. In
certain areas it seems to be evolving very quickly.
Isolated valleys and mountains, acting as islands,
Tineid Moths
T 3823
like the Pyrenees in France and Spain, and the
Atlas in Morocco, seem to be the focus of strong
variation. Along the Moroccan coast and in the
Pyrenees, small morphological differences, proba-
bly linked with interbreeding, sometimes show
small variations in food habits. In the Pyrenees,
each river, each valley seems to have a small
variation.
Separation of the genus between America and
the Old World has always puzzled entomo­logists.
Very few other cases are similar among the arthro-
pods. Transpacific migration remains a possibil-
ity, but the genus is absent in the Far East.
Extinction is caused by urbanization, frag-
mentation of the habitat, use of insecticides and
herbicides, general pollution and many other rea-
sons. The survival of many species is actually in
jeopardy in Europe and in the USA. Probably sev-
eral species will soon be extinct, and many more
are endangered.
References
Farrell BD (1998) “Inordinate fondness” explained: why are
there so many beetles? Science 281:555–559
Gomez-Zurita J, Juan C, Petitpierre E (2000) The evolutionary
history of the genus Timarcha (Col Chrys.). Inferred
from mitochondrial COII gene and partial 16S rDNA
sequences. Mol Phylogenet Evol 14:304–317
Jolivet P (1994) Remarks on the biology and biogeography of
Timarcha (Chrysomelidae Chrysomelinae). In: Furth DG
(ed) Proceedings 3rd International Symposium on Chry-
somelidae, Beijing, 1992. Backhuys, Leiden, 85–97 pp
Jolivet P (1995) A status report on the species of Timarcha
(Col. Chrys.). Insecta Mundi 9:153–154
Jolivet P, Petitpierre E (1973) lantes-hôtes connues des Timar­
cha Latreille (Col. Chrys.). Quelques considérations sur
les raisons possibles du trophisme sélectif. Bull Soc
Entomol Fr 78:9–25
Tineid Moths
Members of the family Tineidae (order
Lepidoptera).
 Fungus Moths
 Butterflies and Moths
3824
T Tineidae
Tineidae
A family of moths (order Lepidoptera). They
commonly are known as tineid moths, fungus
moths, or clothes moths.
 Fungus Moths
 Butterflies and Moths
Tineodidae
A family of moths (order Lepidoptera) also known
as false plume moths.
 False Plume Moths
 Butterflies and Moths
Tingidae
A family of bugs (order Hemiptera). They some-
times are called lace bugs.
 Lacebugs
 Bugs
Tiphiidae
A family of wasps (order Hymenoptera).
 Wasps, Ants, Bees, and Sawflies (Hymenoptera)
 Tiphiid Wasps (Hymenoptera: Tiphiidae)
Tiphiid Wasps (Hymenoptera:
Tiphiidae)
Michael E. Rogers, Daniel A. Potter
University of Kentucky, Lexington, KY, USA
The family Tiphiidae belongs to the informal
group (series) Aculeata, which includes all sting-
ing wasps, of the order Hymenoptera (ants,
wasps and bees). The Tiphiidae were previously
placed in the superfamily Scolioidea and later
Tiphioidea. The current classification of the
Hymenoptera which recognizes only three
a­ culeate superfamilies, Chrysidoidea, Apoidea
and Vespoidea, places the Tiphiidae in the super-
family Vespoidea.
Order: Hymenoptera
Suborder: Apocrita
Informal Group: Aculeata
Superfamily: Vespoidea
Family: Tiphiidae
Most members of the Tiphiidae are believed
to be parasitoids of the edaphic (soil inhabiting)
larval stage of certain beetles (Coleoptera). Primar-
ily a tropical family, the Tiphiidae are represented
worldwide by seven subfamilies containing about
1,500 species. These subfamilies are the Antho-
boscinae (six genera), Diamminae (one genus),
Thynninae (50 genera), Tiphiinae (nine genera),
Brachycistidinae (13 genera), Myzininae (12 gen-
era) and Methochinae (two genera). The Thynni-
nae is the largest subfamily of the Tiphiidae,
present mainly in the Neotropical regions and
Australia. The five subfamilies represented in
North America include the Tiphiinae, Myzininae,
Methochinae, Anthoboscinae and Brachycistidi-
nae. Of these subfamilies, the Tiphiinae is the largest
containing about 140 species in North America.
The most common group of Tiphiinae are the
members of the genus Tiphia, represented by about
100 North American species.
External Morphology
The adult Tiphiidae range from 5 to 30 mm in length.
The wasps are typically black but may have red, yel-
low or white markings. The antennae are 12-seg-
mented in females and 13-segmented in males. The
pronotum and mesonotum are separated by a suture
and not fused. The middle and hind legs are often
heavily spined. Sexual dimorphism ranges from
slight to pronounced and in some species, the wings
of the female are reduced or absent. Males often have
a modification of the eighth sternite (or hypopygid-
ium) forming an upward curved spine that may be
mistaken for a sting. Two morphological features
which help to distinguish the Tiphiidae from other

families are a mesosternum with two posterior lobes
and the separation of abdominal segments by well-
defined constrictions.
Life History and Habits
The Tiphiidae are all solitary wasps and develop as
ectoparasitoids on their soil-dwelling hosts. Most
tiphiids are parasitoids of larval Scarabaeidae, com-
monly referred to as white grubs. The Thynninae,
Tiphiinae and Myzininae contain species that, for
the most part, are parasitoids of white grubs. The
exception is the Myzininae, in which a few of the
species parasitize larval Tenebrionidae, Cicindelli-
dae or Cerambycidae (all Coleoptera). The biology
of the Anthoboscinae and Brachycistidinae has not
been studied but it is believed that members of
these two subfamilies are also parasitoids of scara-
baeid larvae. The Diamminae, an Australian group,
parasitizes mole crickets (Orthoptera: Gryllotalpi-
dae) and the Methochinae parasitize the larvae of
tiger-beetles (Coleoptera: Cicindellidae).
Adult Tiphiidae feed primarily either on hon-
eydew produced by other insects, or on the nectar
of flowering plants. Female wasps may also feed by
biting a paralyzed host during an oviposition event
and then imbibing the hemolymph exuding from
the wound. Females lay about 50 eggs over their
3- to 4-week lifespan, but in a few species may lay
as many as 100 eggs. As in most members of
Hymenoptera, fertilized eggs become females and
males are produced with unfertilized eggs. Females
control the sex of their offspring, with male eggs
placed on smaller hosts and female eggs placed on
larger hosts (Fig. 78).
The best-studied group of Tiphiidae is the
genus Tiphia. Tiphia are mostly host specific, i.e.,
each wasp species parasitizes larvae of only one
species of grub. In cases where more than one grub
species is parasitized, all host grub species are usu-
ally of the same genus. The emergence of adult
wasps is synchronized with the presence of the
third instar of grubs with a 1-year life cycle or the
second instar of grubs with a 2- or 3-year life cycle.
Tiphiid Wasps (Hymenoptera: Tiphiidae)
T 3825
After mating, the female burrows into the soil and
uses kairomones from grub frass (feces) and body
odor trails to locate a host. Once a host is found,
the wasp stings the grub ventrally between the first
and second thoracic segments causing temporary
paralysis. An egg is then laid on the host. The posi-
tion of the egg on the host differs among the spe-
cies of Tiphia. The larval Tiphia hatches from the
egg in 3–7  days. Upon hatching, the wasp larva
pierces its host’s cuticle with its mouthparts and
feeds on its body fluids. After a period of about
21 days, the fifth instar Tiphia devours the remain-
ing non-sclerotized body parts of its host and then
spins a silken cocoon. In temperate regions, Tiphia
have one generation per year and will overwinter
in the cocoon. Tropical species of Tiphia have mul-
tiple generations each year.
Predators and Parasites
The impact that natural enemies have on tiphiid
populations is not known. Bombyliid flies (Dip-
tera) and rhipiphorid beetles (Coleoptera) are
common parasites reared from the cocoons of
various Tiphiidae. Sphecid and mutillid wasps
(Hymenoptera) and nematodes are less commonly
observed as natural enemies of tiphiids.
Importance in Biological Control
During the 1920s and 1930s, 14 species of Tiphia
were introduced into the U.S. from Japan and
China to control the spread of the Japanese beetle,
Popillia japonica (Coleoptera: Scarabaeidae). Only
two of them, Tiphia popilliavora and T. vernalis,
became established. Only T. vernalis is known to
still be established throughout much of the range
of the Japanese beetle. Currently, efforts are under
way to move Tiphia vernalis to areas of the U.S.
where the Japanese beetle has recently spread but
Tiphia vernalis is not yet established. Of the
native Tiphiidae, Tiphia pygidialis and T. relativa
are common parasitoids of masked chafer,
3826
T Tipulidae

Tiphiid Wasps (Hymenoptera: Tiphiidae), Figure 78  Tiphiid wasps: (a) Adult female Tiphia pygidialis,
subfamily Tiphiinae, 12 mm long, North America. (b) Masked chafer, Cyclocephala sp. with egg
of T. pygidialis. (c) Fifth instar T. pygidialis devouring Cyclocephala sp. host. (d) Cocoon of T. pygidialis.

­ yclocephala spp., grubs and T. berbereti, T. inter­

C Kimsey LS (1991) Relationships among the tiphiid subfami-
media, T. tegulina, T. transversa and T. vulgaris
­parasitize June beetle, Phyllophaga spp., grubs.
 Wasps, Ants, Bees, and Sawflies (Hymenoptera)
References
Brothers DJ (1999) Phylogeny and evolution of wasps, ants
and bees (Hymenoptera, Chrysidoidea, Vespoidea and
Apoidea). Zool Scr 28:233–249
Clausen CP (1940) Entomophagous insects. McGraw-Hill,
London, 688 pp
Clausen CP, Jaynes HA, Gardner TR (1933) Further investiga-
tions of the parasites of Popillia japonica in the far east.
Technical Bulletin No. 366 United States Department of
Agriculture, Washington, DC
lies (Hymenoptera). Syst Entomol 16:427–438
King JL, Holloway JK (1930) Tiphia popilliavora Rohwer, a
parasite of the Japanese beetle. Circular No. 145. United
States Department of Agriculture, Washington, DC
Rogers ME, Potter DA (2002) Kairomones from scarabaeid
grubs and their frass as cues in below-ground host loca-
tion by the parasitoids Tiphia vernalis and Tiphia pygidi­
alis. Entomol Exp Appl 102:307–314
Tipulidae
A family of flies (order Diptera). They commonly
are known as crane flies.
 Flies
 Crane Flies (Tipulidae and Others)
Tomato Hornworm, Manduca quinquemaculata (Haworth) and Tobacco Hornworm, Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae)
T 3827

Tischeriidae Tomato Big Bud

A family of moths (order Lepidoptera). They A bacterial disease transmitted by leafhoppers.

commonly are known as trumpet leafminer  Transmission of Plant Diseases by Insects
moths.
 Trumpet Leafminer Moths
 Butterflies and Moths Tomato Hornworm, Manduca
quinquemaculata (Haworth) and
Tobacco Hornworm, Manduca
Toad Bugs sexta (Linnaeus) (Lepidoptera:
Sphingidae)
Members of the family Gelastocoridae (order
Hemiptera). John L. Capinera
 Bugs University of Florida, Gainesville, FL, USA

These species occur in North, Central and South

Tobacco America, and the Caribbean Islands. The tobacco
and tomato hornworms are very similar in appear-
ance, biology, and distribution, and are commonly
The source of nicotine, a natural product having confused. However, the tobacco hornworm is
insecticidal properties. more common in warmer climates, such as the
 Botanical Insecticides Gulf Coast States of the USA, whereas the tomato
hornworm is more common in cooler regions
such as the northern USA and Canada.
Toe Biters
Members of the family Belostomatidae (order Life History
Hemiptera).
 Bugs The number of annual generations ranges from
 Giant Water Bugs one in cool locations such as Canada to perhaps
four in warmer locations such as Florida, USA.
The proportion of insects that enter diapause
increases from about 5% in June to 95% in mid
Togossitidae August, as day length decreases. In northern Flor-
ida, the insects are active from April to November,
A family of beetles (order Coleoptera). They com- but they are abundant only for the first two gen-
monly are known as bark-gnawing beetles. erations because many pupae enter diapause. In
 Beetles North Carolina they occur from mid May to Octo-
ber, and evidence of a third generation is weak.
Throughout their range, hornworms overwinter in
Tolerance the pupal stage, and in the northernmost portions
of their range may not overwinter successfully,
The ability of a host to grow and reproduce nor- occurring only after dispersal northward during
mally while supporting an insect population that the summer. The life cycle can be completed in
would normally be damaging. 30–50 days, but often is considerably protracted.
3828
T Tomato Hornworm, Manduca quinquemaculata (Haworth) and Tobacco Hornworm, Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae)
The eggs are spherical to oval in shape, and
measure 1.25–1.50  mm in diameter. Eggs are
smooth and vary in color from light green or yel-
low when they are early in development, to white
at maturity. Eggs are deposited principally on the
lower surface of foliage, but also on the upper sur-
face. Mean fecundity is about 250–350 eggs, with
seasonal fluctuations and maximum egg produc-
tion at mid-season. However, with adequate adult
nutrition, fecundity of nearly 1,400 eggs per female
could be attained. Duration of the egg stage is
2–8 days, but averages 5 days.
The larva is cylindrical in form and bears five
pairs of prolegs in addition to three pairs of tho-
racic legs. The most striking feature of the larva is
a thick pointed structure or “horn” located dorsally
on the terminal abdominal segment. The horn is
as long as the body in newly hatched larvae, but
becomes relatively smaller as the larva matures.
Young larvae are yellowish white but during the
second instar become green with white lines later-
ally. The tobacco hornworm develops seven
straight oblique whitish lines laterally. The white
lines are edged with black on the upper borders,
and the horn is usually red in color. The tomato
hornworm is superficially similar, but instead of
the seven oblique lateral bands it bears eight whit-
ish or yellowish “V”-shaped marks laterally, and
pointing anteriorly. The V-shaped marks are not
edged in black (Figs. 79 and 80). Also, in tomato
hornworm the horn tends to be black in color. The
body of both species is usually light green in color,
but occasionally dark brown or blackish forms
occur; the larvae blend in very well with the foli-
age on which they feed. There normally are five
instars, but occasionally six are observed. The
mean head capsule width is 0.8, 1.2, 2.0, 3.0, and
5.0 mm for instars 1–5, respectively. Correspond-
ing mean larval body lengths are 6.7, 11.2, 23.4,
49.0, and 81.3  mm, respectively. Larval develop-
ment time averages about 20 days, but ranges from
13 to 44  days depending on temperature. Mean
development time for larvae reared under insec-
tary conditions in northern Florida is 3.4, 2.9, 3.0,
3.9, and 6.6 days for instars 1–5, respectively.
Tomato Hornworm, Manduca quinquemaculata
(Haworth) and Tobacco Hornworm, Manduca sexta
(Linnaeus) (Lepidoptera: Sphingidae),
Figure 79  Tomato hornworm larva.
Tomato Hornworm, Manduca quinquemaculata
(Haworth) and Tobacco Hornworm, Manduca
sexta (Linnaeus) (Lepidoptera: Sphingidae),
Figure 80  Tobacco hornworm larva.
Mature larvae drop to the soil at maturity and
burrow to a depth of 10–15 cm. There they form a
pupal cell measuring about 7 cm long and 4 cm wide,
and pupate within. The interval between entering
the soil and pupation is usually 4–8 days. The pupa
is large and elongate-oval in form, but pointed at
the posterior end. It measures 45–60 mm in length
and 13–14  mm in width. The pupa bears a pro-
nounced maxillary loop, a structure that encases
the mouthparts. The maxillary loop in tobacco
hornworm extends back about one-fourth the
length of the body, whereas in tomato hornworm
it is longer, usually extending for about one-third
the length of the body (Figs. 81 and 82). The color
of the pupa is brown or reddish brown. Duration
of the  pupal stage is protracted and variable.
Pupal duration often exceeds 100  days, even in
the ­summer generations, but may be as short as
15 days, and 21 days is about average. Overwinter-
ing pupae do not emerge synchronously, with
emergence spread from May to early August; a few
even diapause through two winters.
The adults of both species are large moths
with stout, narrow wings, and a wing span of
80–130 mm. The forewings are much longer than
Tomato Hornworm, Manduca quinquemaculata (Haworth) and Tobacco Hornworm, Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae)
T 3829

Tomato Hornworm, Manduca quinquemaculata Tomato Hornworm, Manduca quinquemaculata

(Haworth) and Tobacco Hornworm, Manduca sexta (Haworth) and Tobacco Hornworm, Manduca sexta
(Linnaeus) (Lepidoptera: Sphingidae), (Linnaeus) (Lepidoptera: Sphingidae),
Figure 81  Tomato hornworm pupa. Figure 82  Tobacco hornworm pupa.

the hind wings. The females are larger than the

males and can be differentiated from them by the
narrower antennae. Both species are dull grayish
or grayish brown in color, though the sides of the
abdomen usually are marked with six orange-­
yellow spots in tobacco hornworm and five spots
in tomato hornworm. The hind wings of both spe-
cies bear alternating light and dark bands (Figs. 83
and 84). Adults become active at sunset, when they Tomato Hornworm, Manduca quinquemaculata
can be observed feeding at flowers. Though some (Haworth) and Tobacco Hornworm, Manduca sexta
adults remain active throughout the night, most (Linnaeus) (Lepidoptera: Sphingidae),
activity occurs early in the evening and just before Figure 83  Tomato hornworm adult.
dawn. Both hornworm species likely produce sex
pheromone, but only that of the tobacco horn- These insects feed only on solanaceous plants,
worm has been identified. The preoviposition particularly tomato and tobacco. They are recorded
period of moths is about 2  days, and eggs are from other vegetables such as eggplant, pepper,
deposited for about 4–8 days. and potato, but such feeding is unusual. Several
3830
T Tomato Hornworm, Manduca quinquemaculata (Haworth) and Tobacco Hornworm, Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae)
Tomato Hornworm, Manduca quinquemaculata
(Haworth) and Tobacco Hornworm, Manduca sexta
(Linnaeus) (Lepidoptera: Sphingidae),
Figure 84  Tobacco hornworm adult.
solanaceous weeds are reported to serve as hosts,
including groundcherry, Physalis spp.; horsenettle,
Solanum carolinense; jimsonweed, Datura stramo­
nium; and nightshade, Solanum spp.; but wild
hosts are unimportant larval food sources relative
to crops. Adults imbibe nectar from flowers of a
number of plants such as catalpa, Catalpa speciosa;
daylily, Hemerocallis sp.; hollyhock, Althaea rosea;
jimsonweed; four o’clock, Mirabilis jalapa; mallow,
Hibiscus lasiocarpus; mimosa, Albissia julibrissin;
and tobacco.
A large number of natural enemies is known
from tobacco and tomato hornworm. Natural
enemies of the egg stage include Trichogramma sp.
(Hymenoptera: Trichogrammatidae) and Teleno­
mus sp. (Hymenoptera: Scelionidae), but these are
thought to be of little importance. Of greater impor-
tance is the stilt bug Jalysus spinosus (Say)
(Hemiptera: Berytidae) and other general predators
such as bigeyed bugs (Hemiptera: Lygaeidae) and
lacewings (Neuroptera: Chrysopidae).
Larvae often are parasitized by Apanteles con­
gregatus (Say) (Hymenoptera: Braconidae), and
larvae are sometimes seen bearing clusters of
white pupal cases formed by this wasp, attached to
their bodies. In North Carolina, 30–40% of horn-
worms may be parasitized by this wasp. In contrast
to this one species of wasp accounting for most of
the parasitism by Hymenoptera, a number of
insects in the order Diptera, particularly the
Tachinidae, attack tobacco and tomato hornworm.
Records of tachinid parasitism from tomato horn-
worm include Compsilura concinnata (Meigen),
Drino incompta (Wulp), D. rhoeo (Walker), Lespesia
frenchii (Williston), Winthemia leucanae (Kirkpat-
rick), and W. quadripustulata (Fabricius). Records
of tachinids from tobacco hornworm include
Carcelia spp., Drino incompta, D. rhoeo, Lespesia
spp., Metavoria orientalis Townsend, and Win­
themia quadripustulata. In North Carolina, the
proportion of hornworm larvae parasitized by
tachinids increases during the season, sometimes
attaining 100%. The number of tachinid eggs per
hornworm larva also increases seasonally, indi-
cating a greater abundance of flies. Also of great
significance as a mortality agent of larvae is Polistes
spp. (Hymenoptera: Vespidae). These wasps kill
and consume, or sometimes carry away to provi-
sion their nest, a very high proportion of larvae.
Apparently Polistes spp. is the most important larval
mortality factor in North Carolina.
Pathogens sometimes affect hornworms. A
bacterial disease that causes the larva to blacken
and droop is sometimes reported to kill larvae, but
this does not occur regularly, and is observed
mostly at very high larval densities. Larvae also are
susceptible to infection by the fungus Ento­
mophaga aulicae, but this disease also does not
occur widely.
Vertebrates may prey on the pupae. Skunks
and moles are particularly important. Tachinids
emerge from the prepupal and pupal stages, but
attack only the larvae.
Damage
Although these insects are common, they are not
serious pests in commercial agriculture because
they are easily killed by insecticides. In home
gardens they often cause considerable damage to
tomato.
Larvae are defoliators, usually attacking the
upper portion of plants initially. Rather than chew-
ing holes in the leaf, they usually consume the entire

leaf. Sometimes they attack green fruit. Because the
larvae of hornworms attain such a large size, they
are capable of high levels of defoliation. The con-
sumption of tobacco foliage by larvae is 5.2, 9.7, 33.5,
175.4, and 1,941.4 cm2 by instars 1–5, respectively,
for a total of 2,165 cm2. Note that about 90% of the
foliage consumption occurs during the final instar,
and although the exact value of foliage consumption
would differ on tomato, the pattern would be the
same. Larvae blend in with the foliage and are not
easy to detect. Thus, it is not surprising that they
often are not observed until they cause considerable
damage at the end of the larval period.
Management
Moths are attracted to light and can be captured in
light traps. Light traps have also been used to
attempt suppression of hornworm populations,
and although some reduction was noted, this
approach has not proved practical. Isoamyl salicy-
late is attractive to both species of hornworms.
Visual examination of foliage usually is recom-
mended for monitoring of larval populations.
Young larvae of tobacco hornworm tend to be
found in the upper regions of the plant, whereas
larvae of tomato hornworm tend to be lower; dif-
ferential flight and oviposition behavior between
the species is implicated.
Chemical insecticides or Bacillus thuringiensis
are applied to the foliage for larval suppression. The
mature caterpillars are more difficult to kill, so
young larvae should be targeted. The pupae are
large and not buried very deeply in the soil, so
greater than 90% mortality is caused by normal
soil tillage practices. Hand picking and destruction
of larvae is often practical in the home garden.
To take advantage of the preference of Polistes
wasps for hornworm larvae, wasp shelters or nesting
boxes have been placed in tobacco fields to encour-
age the wasps, and wasp colonies were relocated
into tobacco. Although wasp predation was inad-
equate to prevent damage to tobacco, this approach
might be satisfactory for tomato.
Tonic Receptors
T 3831
Tobacco and tomato hornworm thrive on
tobacco plants that are allowed to revegetate after
harvest of the leaves, leading to high populations
during the next year. Destruction of tobacco stalks,
or inhibition of sprouting by application of plant
growth regulators, greatly reduces hornworm
populations in subsequent seasons. Though not
documented, timely destruction of tomato crop
residue likely would have similar beneficial effects.
References
Bell RA, Joachim FG (1976) Techniques for rearing labora-
tory colonies of tobacco hornworms and pink boll-
worms. Ann Entomol Soc Am 69:365–373
Capinera JL (2001) Handbook of vegetable pests. Academic,
San Diego, 729 pp
Chamberlin FS, Tenhet JN (1926) The seasonal history and
food habits of the tobacco budworm, Heliothis virescens
Fab., in the southern tobacco-growing region. J Econ
Entomol 19:611–614
Madden AH, Chamberlin FS (1945) Biology of the tobacco
hornworm in the southern cigar-tobacco district. USDA
Technical Bulletin 896, 51 pp
Rabb RL (1969) Environmental manipulations as influencing
populations of tobacco hornworms. Proc Tall Timbers
Conf Ecol Anim Cont Habitat Manage 1:175–191
Tomato Rust Mite, Aculops
lycopersici (Massee) (Acari:
Eriophyidae)
This is a pest of solanaceus crops, especially tomato.
Tomoceridae
A family of springtails in the order Collembola.
 Springtails
Tonic Receptors
Sensory neurons that are slow to adapt to continu-
ing steady stimuli, with the receptor potential
remaining elevated (contrast with phasic
receptors).
3832
T Tooth-Necked Beetles

Tooth-Necked Beetles Tortoise Beetles

Members of the family Derodontidae (order Members of the subfamily Cassidinae of the beetle
Coleoptera). family Chrysomelidae. The lateral expansion of
 Beetles the pronotum and elytra hide the legs and head,
giving a tortoise-like appearance to the insect.
 Beetles
Tormogen Cell

An epidermal cell that forms a depression in the Tortoise Scales

integument and which contains a seta, often is a
flexible socket. It typically is innervated and has
sensory capabilities.
Torre-Bueno, José Rollin De La
Some members of the family Coccidae, superfam-
ily Coccoidae (order Hemiptera).
 Scale Insects and Mealybugs
 Bugs

José de la Torre-Bueno was born at Lima, Peru, on Tortricid Moths

October 6, 1871. At the age of 14 he and his family
moved to the United States. He attended Columbia Members of the family Tortricidae (order
University and graduated in 1894. He obtained Lepidoptera).
employment with the General Chemical Company  Leafroller Moths
of New York, where some of his principal responsi-  Butterflies and Moths
bilities involved editorial work. He was an active
member of the Brooklyn Entomological Society,
and helped revive the society’s publications as the Tortricidae
Bulletin of the Brooklyn Entomological Society,
New Series, and of Entomologica Americana, New A family of moths (order Lepidoptera). They com-
Series. He served as editor of both until he died. monly are known as leafroller moths or tortricid
Torre-Bueno was a hemipterist, and published moths.
“Synopsis of the North American Hemiptera Het-  Leafroller Moths
eroptera” in three parts (1939, 1941, 1946). In 1937  Butterflies and Moths
the Brooklyn Entomological Society published
Torre-Bueno’s “Glossary of Entomology.” Though
the “Glossary” was a revision of J.B Smith’s “An Torymidae
explanation of the terms used in entomology,” it
became a classic publication. It was updated in A family of wasps (order Hymenoptera).
1989 by S.W. Nichols. Torre-Bueno died in Tucson,  Wasps, Ants, Bees, and Sawflies
Arizona, on May 3, 1948.

Townes, Jr., Henry K

Reference
Henry Townes was born at Greenville, South
Mallis A (1971) American Entomologists. Rutgers University Carolina, USA, on January 20, 1913. He received
Press, New Brunswick, NJ, 549 pp B.S. and B.A. degrees from Furman University in
 Tracheal Gill
T 3833

1933, and then attended Cornell University where Toxicant

he attained the Ph.D. in 1937. He taught at Cor-
nell and Syracuse Universities until receiving a A toxic substance, often the active ingredient in
fellowship in 1940 to work at the Philadelphia pesticide formulations.
Academy of Natural Sciences in Philadelphia,  Insecticides
where he prepared a catalog on the Nearctic Ich-  Acaricides or Miticides
neumonidae. He also worked at the U.S. National
Museum, where he was employed by the United
States Department of Agriculture as a taxono-
mist. In 1949 he moved to North Carolina State
Toxicity
University, where he worked on tobacco pests,
The ability of a toxin to harm or kill an organism.
and traveled to the Philippines to advise the gov-
 Insecticide toxicity
ernment on pests of rice and corn. In 1956 he
moved to the University of Michigan to work on
Ichneumonidae. Henry and his wife Marjorie
founded the American Entomological Institute Toxicogenic Insects
in Ann Arbor, Michigan, in 1962 as an indepen-
dent, nonprofit research institute. Henry also Insects capable of producing disease in plants
worked briefly at Michigan State University and due to injection of saliva or other secretions, and
Carleton University during the early stages of the in the absence of microbial pathogens.
institute, but it soon became a mecca for parasitic
hymenopterists, and a full-time job. The Institute
relocated to Gainesville, Florida, in 1985. Henry
was passionate about the study of Ichneumoni-
Trachea (pl., Tracheae)
dae, became known as the world’s foremost
An internal tube that delivers air to tissues, and
authority, and amassed the world’s best collec-
part of a system of large and small tubes. The
tion. He published nearly 140 articles or books
external openings of the system are called spira-
during his career, of which nine were at least 500
cles, and the smaller tubes are called tracheoles.
pages long. Along with colleagues, he established
Air sacs, or dilated areas of trachea, are often found
a firm knowledge of this group, one of the larg-
in the system (Fig. 85).
est families of insects known. Henry Townes
 Tracheal System and Respiratory Gas Exchange
died at Gainesville, Florida, on May 2, 1990.

Reference Tracheal Gill

Buckingham GR, Gupta VK, Townes MC (1991) Henry K.
Townes, Jr. Am Entomol 37:252–253
Toxemia
A condition produced by the dissemination of
toxins in the blood, though the bacteria are con-
fined to the gut (e.g., brachytosis).
An extension of the insect’s body that contains
numerous tracheae and serves as a site for
oxygen extraction from water. The heavily tra-
cheated flaps or filaments of the body wall are
usually lateral or ventral expansions of the thorax
or abdomen, and gas exchange occurs across the
body surface.
 Tracheal System and Respiratory Gas
Exchange
3834
T Tracheal Mite, Acarapis woodi (Rennie) (Acariformes: Tarsonemidae)

Heart

Dorsal longitudinal
Dorsal diaphragm trunk

Gut Visceral trachea

Lateral longitudinal
Spiracle trunk

Visceral diaphragm
Nerve cord
Visceral longitudinal
trunk
Ventral commissure

Trachea (pl., Tracheae), Figure 85  Cross section of the abdomen of an insect, showing the principal
trachea and tracheal connections (adapted from Chapman 1998, The insects: structure and function).

Tracheal Mite, Acarapis woodi

(Rennie) (Acariformes:
Tarsonemidae)

Thomas C. Webster
Kentucky State University, Frankfort, KY, USA

The tracheal mite is an internal parasite of honey

bees. It feeds and reproduces inside the protho-
racic tracheae of the adult bee. If a bee is heavily
infested, its tracheae become scarred and filled
with mites. Bees from heavily infested colonies
may be seen crawling on the ground nearby,
unable to fly.
Young bees are more susceptible to infesta-
tion than older bees. The female mite enters the
tracheal tube at the spiracle, and lays eggs within
several days of entry. The egg is followed by a lar-
val and a pharate nymphal stage. The immature
stages last 11–12 days for males and 14–15 days
for the larger females. Immature and mature mites
feed by piercing the host bee’s tracheal wall with
stylet mouthparts, and consuming the hemo-
lymph. Male and female offspring mate in the tra-
chea. Only mated females exit the spiracle to find
another host bee (Fig. 86).
The means by which tracheal mites kill bees is
not entirely clear. Some bees found crawling near
infested hives have no mites or any apparent damage
Tracheal Mite, Acarapis woodi (Rennie)
(Acariformes: Tarsonemidae), Figure 86  Female
tracheal mite clinging to a bee hair, in wait for a
new host bee.
to their tracheae. Possibly, pathogen outbreaks in a
bee colony are stimulated or mediated by the mite.
Dispersal from bee to bee is most rapid in
winter when the bees cluster tightly. Since no bees
are reared during winter, the proportion of bees
which are infested rises considerably in winter.
Consequently, a heavy infestation is often discov-
ered on the first warm days of early spring, when
many bees are found crawling on the ground near
the hive. Tracheal mites spread from hive to hive
when infested bees drift to, or rob honey from,
other hives nearby.

An earlier name, the acarine mite, has been
abandoned because it is meaningless and redun-
dant. Two closely related mites, A. externus and
A. dorsalis, live externally on the bees. They are not
known to be harmful to their hosts.
History
The tracheal mite was first identified in 1919, when
it was found in Scotland. Originally the mite was
implicated in the “Isle of Wight disease,” which
had plagued the British Isles earlier in the century.
However, more recent studies suggest that the dis-
ease was not caused simply by mite infestations.
Since then, the mite has been discovered in
many other parts of the world. It is very well
adapted to life as a honey bee parasite and is not
found on hosts other than Apis species. Conse-
quently, the host-parasite relationship must be
very old.
Mexico was found to have the mite around
1980. In 1984 it was discovered in the United States,
having apparently entered Texas from Mexico.
Infestations were confirmed in Canada in 1986. By
the late 1980s many thousands of hives in the
United States and Canada were dying yearly. This
parasite was rapidly dispersed by the shipment of
queen and package bees, and migratory beekeep-
ing operations. By the late 1990s, however, tracheal
mite infestations had declined dramatically. Now
the mite continues to be endemic in North Amer-
ica, as it is elsewhere. The decline of tracheal mite
infestations is still not well understood.
Diagnosis and Control
Tracheal mites are identified by removing the
prothoracic tracheae alone, or within the anterior
portion of the bee’s thorax. Thoracic muscle tissue is
cleared with potassium hydroxide solution. Tracheal
mites and scarring of the tracheae are easily seen by
low power microscopy. Positive identification is not
possible for those without a microscope.
Tracheal System and Respiratory Gas Exchange
T 3835
Menthol, formic acid and chlorobenzilate
have been used effectively as fumigants to control
the mites inside the hive. Vegetable oil also has
been used with success, mixed with sugar and
placed inside the hive. Bees that walk over the oil
preparation acquire a fine coating which seems to
inhibit mite dispersal among bees in the hive.
Some bees groom themselves of mites. This
trait is heritable, so selection for grooming behav-
ior can be part of a breeding program for tracheal
mite resistance.
 Mites
 Apiculture
 Honey Bee
References
Bailey L, Ball BV (1991) Honey bee pathology, 2nd edn.
Academic, New York
Webster TC, Delaplane KS (eds) (2001) Mites of the honey
bee. Dadant, Hamilton, IL
Wilson WT, Pettis JS, Henderson CE, Morse RA (1997) ­Tracheal
mites. In: Morse RA, Flottum K (eds) Honey bee pests,
predators and diseases, 3rd edn. A.I. Root, Medina, OH
Tracheal System and Respiratory
Gas Exchange
James L. Nation
University of Florida, Gainesville, FL, USA
Insects breathe through a complex network of
tubules, the tracheae. Large tracheae connect to
spiracles opening at the surface of the body, where
air enters and carbon dioxide exits. Spiracles usu-
ally occur on the pleural surface of the body, typi-
cally one on each side of each segment, but
numerous variations have evolved. Airflow may be
tidal, in and out of the same spiracles, or directed
flow with inflow through anterior spiracles and
outflow through posterior abdominal ones. Inter-
connecting longitudinal and transverse tracheal
trunks make directed flow possible and more effi-
cient than tidal flow because the system is
3836
T Tracheal System and Respiratory Gas Exchange
c­ onstantly flushed and incoming air is not mixed
with used air. Larger tracheal tubes send off
branches that become smaller in diameter as they
ramify to all tissues. The smallest diameter trache-
oles (tubes 1 µm diameter or less) end blindly on
the surface of most cells and even indenting some
cells, like pushing a finger into a soft balloon, until
they terminate within a few µm of mitochondria
that actually use the oxygen. Tracheoles indented
into a cell are said to be intracellular, although in
reality they are not really within the interior of
the cell, for the tracheal epithelium cell layer
and the cell membrane separate the tracheole from
the cytoplasm of the cell. The chitinous lining
of tracheae are shed at each molt, but the lining of
tracheoles is not molted. Spiracular valves at the
body surface often can be closed to reduce water
loss from the system. Although all parts of the tra-
cheal system allow oxygen to diffuse out to the tis-
sues and carbon dioxide to enter, most of the gas
exchange occurs across the smaller tracheae and tra-
cheoles because they are the parts of the system in
intimate contact with cells. The extensive ramifica-
tion of tracheae and tracheoles and their relation-
ship to all cells are similar to the pattern of the
vertebrate circulatory system, with the exception
that tracheoles end blindly and vertebrate capillaries
do not. The tracheal system is remarkably efficient
Dorsal diaphragm
Gut
Spiracle
Nerve cord
Ventral commissure
Tracheal System and Respiratory Gas Exchange, Figure 87  Cross section of the abdomen of an insect,
showing the principal tracheae and tracheal connections (adapted from Chapman 1998, The insects:
structure and function).
for insects. Insects do not accumulate an oxygen
debt during vigorous activity, such as flight. In
some very small insects (smaller than a Drosophila
fly), simple diffusion of gases through the tracheae
may suffice, but most insects, large or small, actively
ventilate the system by rhythmic compression of
the abdomen. Muscular movements during flight
or other vigorous muscular and body movements
compress the tracheal system and act like a pump
to ventilate the system (Figs. 87, 88, and 89).
Tracheae develop from embryonic ectoder-
mal tissue, and all parts, including the smallest
tracheoles, have an epicuticular lining or intima
that is continuous with the external cuticle. In
some larger insects one can see larger tracheal
trunks that are pulled out and still attached to the
old exoskeleton at a molt. Larger tracheae may
contain a thicker endocuticle layer that gives more
strength to the tubular structure. The internal
surface of tracheae contains a hydrophobic sub-
stance that helps prevent water from entering the
tracheae, and reduces evaporative water loss from
the internal tracheal surfaces. Thickened, tight
spirals of the cuticular intima, the taenidia,
strengthen tracheae, provide elasticity, and help
the tubes resist compression and collapse. Even
tracheoles and air sacs show some evidence of
taenidial reinforcements, but thickenings usually
Heart
Dorsal longitudinal
trunk
Visceral trachea
Lateral longitudinal
trunk
Visceral diaphragm
Visceral longitudinal
trunk

Tracheal System and Respiratory Gas Exchange,
Figure 88  A view from inside a large trachea in a
mole cricket. This scanning electron micrograph
shows the branching of two smaller tracheae and
the taenidial windings that strengthen all tracheae
and keep them from collapsing.
are widely spaced apart so that these parts of the
system are more flexible.
Tracheae are not simply tubes and tubules;
every part of the system contains living cells. Tra-
cheal epithelial cells are thin and flattened, like
many small pieces of ribbon glued together and
wrapped around the tracheae. A tracheal epithelial
cell encloses a tracheole. New tracheae and trache-
oles develop as the insect grows. A new tracheole
develops as a tubule or cavity within a tracheal
epithelial cell that grows out, often in multiple fin-
ger-like shapes, from the surface of a larger tra-
chea. The tracheole unites with the larger tracheal
branch to which the parent tracheal cell is still
attached.
Air sacs, dilated portions of tracheae, occur
in many insects. They are variable in size, but
frequently are large in flying insects such as hon-
eybees, cicadas, many adult Diptera, and some
Tracheal System and Respiratory Gas Exchange
T 3837
Tracheal System and Respiratory Gas Exchange,
Figure 89  A scanning electron micrograph view
of a trachea (about 2 µm diameter) that branches
several times into smaller tracheae and tracheoles
that penetrate the salivary gland tissue of a male
Caribbean fruit fly, Anastrepha suspensa.
scarab and buprestid beetles. The rhythmical
squeezing action of working flight muscles pumps
air sacs like a bellows and increases the flow of air
through the system. Air sacs may collapse as grow-
ing tissues fill the body space, and by collapsing
they make room for the new tissue, with little
change in the general body shape. Air sacs serve a
hydrostatic function in some aquatic insects, and
allow more freedom in vibration of the tympanic
membrane in some sound-producing insects. By
taking up space and restricting hemolymph vol-
ume, air sacs increase solute concentration in the
hemolymph without increasing total solute.
Hemocytes, the circulating blood cells, are the
only cells in the body that do not have direct tra-
cheal connections. Recently, it was shown that
hemocytes tend to accumulate on very thin-walled
tufts of tracheae near the last pair of abdominal
spiracles and in the compartment at the tip of the
3838
T Tracheal System and Respiratory Gas Exchange
abdomen called the tokus. It seems as if the highly
branched tracheal system of the last segment and
the tokus are sites where the hemocytes can
become oxygenated; they probably pass their car-
bon dioxide directly into the hemolymph.
Discontinuous Breathing
Some insects regulate spiracle closing and open-
ing, and keep the spiracles tightly closed and/or
apparently closed for a high percentage of the
time. Gas exchange occurs in three periods named
the open, flutter, and closed periods (often desig-
nated as O, F, and C, respectively) because of the
action of spiracles over the duration of a cycle.
This functional pattern, variously known as dis-
continuous release of CO2, passive suction ventila-
tion, discontinuous ventilation cycle, and as the
discontinuous gas exchange cycle (DGC) has been
known in some insects for more than half a cen-
tury. The earliest studies were in diapausing pupae
of Lepidoptera, and initially DGC was thought to
be limited to quiescent insects in a depressed state
of metabolism. DGC patterns, however, have been
observed in a number of different insects in vari-
ous states of activity, including ants, the cockroach
Periplaneta americana, a number of adult tenebri-
onid beetles, the locust Schistocerca gregaria, the
lubber grasshopper Romalea guttata, and adults of
additional species. DGC behavior also occurs in
some arthropods other than insects. During DGC,
accumulated CO2 is discharged periodically in
bursts during brief intervals when spiracles are
open. After a burst, the spiracles are closed for
some period of time that varies from species to
species. During the closed interval, tissues use
oxygen and intratracheal oxygen tension falls.
Most insects that exhibit discontinuous gas
exchange allow the spiracular valve to flutter with
imperceptible amplitude to the unaided eye during
a portion of a cycle. The fluttering (F) phase allows
small amounts of O2 to be sucked into the tracheal
system by the slight negative pressure arising from
O2 consumption by the tissues. The F phase usually
is considered to involve convective transfer of O2.
This has given rise to the name “passive suction
ventilation” that sometimes is applied to the pro-
cess. The slight internal vacuum retards the out-
ward loss of water vapor and CO2 during the
fluttering phase, and the low influx of O2 length-
ens the time to full opening or “burst” of spiracles.
Tissues produce CO2 even when the spiracles are
closed. The high solubility of CO2 in aqueous solu-
tions enables insects to accumulate bicarbonate
ion, HCO3−, in the hemolymph. Buffering capacity
of hemolymph aids in solubilizing CO2 as bicar-
bonate, and this keeps gaseous CO2 from building
up rapidly in the tracheal system. At some point,
probably different for different insects, the rela-
tionship between gaseous O2 and CO2, and HCO3−
in solution reaches an equilibrium at which
tracheal tension of CO2 and O2, and/or pH change
in the hemolymph, trigger spiracle opening and
release of CO2 from the hemolymph as a gas. It
often has been assumed, but not proven, that the
functional benefit of discontinuous ventilation is
conservation of water. In diapausing pupae that
must pass a long winter under the soil, leaf litter, or
other pupation site, water conservation seems
quite necessary and a reasonable driving mecha-
nism for the evolution of discontinuous ventila-
tion, since the pupa is a closed (to food/water
intake) system. Most adult insects that exhibit dis-
continuous ventilation do so only intermittently,
and the rest of the time they ventilate the system
continuously. Surprisingly, some insects do not
show DGC respiration under conditions that
might be expected (based upon assumptions) to
promote the behavior. For example, the lubber
grasshopper Romalea guttata, which discontinu-
ously ventilates at times, tends to ventilate contin-
uously when dehydrated, a physiological condition
in when it presumably has a great need to conserve
water. No good explanation has been provided for
such behavior. The ant Camponotus vicinus, which
exhibits discontinuous gas exchange, actually loses
more water than CO2 during the period when the
spiracles are open. The harvester ant, Pogono­
myrmex rugosus, and similar desert ants have a

relatively high percentage (up to 13%) of body
water loss through the tracheal system, even
though they exhibit discontinuous ventilation at
times. Whether the higher rate of water loss from
the tracheal system in these ants is a significant
stress for them may depend upon how much of
the time the ants exhibit discontinuous gas
exchange, how much access they have to food with
high water content, and duration of exposure to
environmental extremes. Although it seems some-
what intuitive that water loss might be high from
the tracheal system, actual measurements in some
insects indicate that more than 90% of total body
water loss occurs through the cuticle, with only
2–5% typically lost from the tracheal system. In
summary, a definitive selection mechanism for
evolution of discontinuous gas exchange cycling is
not evident, but the mechanism is fairly wide-
spread in many insects including larvae, pupae,
and large and small adults. Water conservation,
ecological niche occupied by insects, and interac-
tions of sensory components may be important
factors.
Gas Exchange in Aquatic Insects
The tracheal system of most aquatic insects is struc-
turally the same as that of terrestrial insects, i.e.,
with open spiracles and an extensive network of
tracheae and tracheoles. These aquatic insects
breathe air by coming to the surface. Water is pre-
vented from entering the system by the hydropho-
bic surface of the tracheae, and in some cases, by
spiracles that can be closed. Many aquatic larvae
have a tracheal system with only one functional
pair  of spiracles near the tip of the abdomen.
When the insect comes to the surface, it does so
with the posterior end uppermost and only the tip
of the abdomen bearing the spiracles is held above
the surface. A large number of aquatic insects sub-
merge with a bubble or film of air around a spira-
cle. These gas bubbles or films of air are called gas
gills, and they may be temporary or permanent.
Temporary ones must be replenished periodically
Tracheal System and Respiratory Gas Exchange
T 3839
as the ­oxygen is used. Permanent gas gills are
called plastrons. They do not collapse and oxygen
can be extracted from water into the gill (if the
water is well aerated), allowing the insect to live
underwater. A plastron consists of an extensive
physical meshwork, either of fine hairs or setae, or
a meshwork of small pores and channels that can
hold a volume of air and can present a large water-
air interface. Plastrons are common in aquatic
insects and can take many physical forms. Some
aquatic insects are able to capture and utilize gas
bubbles of oxygen released by aquatic plants. Cer-
tain species of Diptera, Coleoptera, and Lepi-
doptera independently evolved modifications for
piercing aquatic plants for air.
Some aquatic insects have a closed tracheal
system without functional spiracles. The lack of
functional spiracles eliminates any chance that
water will enter the system, but oxygen must dif-
fuse into the tracheal system through the cuticle, a
breathing mechanism called cutaneous respira-
tion. Some aquatic insects have tracheal gills, thin
flaps of cuticle with many tracheoles just under
the cuticle. Larvae of Trichoptera, Plecoptera,
Odonata, and some Lepidoptera utilize cutaneous
respiration, facilitated by extensive elaboration of
thin hair-like or flap-like tracheal gills from the
body surface. Internally these insects still have an
extensive tracheal system, and gas transport
through the tracheae and tracheoles to internal
body tissues is the same as in terrestrial insects.
Movement of water over the gill and body surface
of aquatic insects is important in maintaining a
fresh supply of oxygenated water in contact with
the body, and most use undulations of the body
and/or movements of the gills themselves to create
ventilatory currents of water. Larvae of some drag-
onflies (Anisoptera) draw water into the rectum
by elastic expansion of the body as dorso-ventral
compressor muscles relax. Typically there are six
main gill folds of the cuticular intima in the ante-
rior part of the rectum with extensive tracheoles
just beneath the intima that extract O2 from the
water. The water is pumped out by dorso-ventral
compression of the abdomen. The rate of ventilation
3840
T Tracheal System and Respiratory Gas Exchange
varies with several factors including the O2 content
of the water. About 85% of the water in the rectum
is renewed during each pumping cycle, and 25–50
cycles/min have been recorded. Larvae also will
come to the surface and ventilate the rectum with
air when oxygen content of the water is very low.
Many hymenopterans and dipterans are para-
sitic on other insects, and have been little studied
with respect to respiration, perhaps for the obvi-
ous reasons that they are usually small and hidden
in the body of the host. Cutaneous respiration is
probably very important. Many chalcid wasps and
tachinid flies hatch from eggs laid on the surface
of the host insect and they eat their way into the
host. They orient the posterior pair of spiracles at
the body surface of the host so that they breathe
air directly. Bot fly larvae, Hypoderma spp., migrate
to the skin of the vertebrate host where they bore
a tiny opening to the surface through which gas
exchange occurs. Respiration is cutaneous in ear-
lier instars that are migrating through the body of
the host.
Respiratory pigments occur in only a few
insects. Chironomus spp. larvae have a small hemo-
globin molecule composed of two chains with a
MW of 31,400. The hemoglobin is not in the cells,
but occurs as a circulating hemolymph protein.
The molecule has extraordinarily high affinity for
oxygen and is 50% saturated at a pO2 of 0.6 mmHg
at 17°C. This means that it will not give up its oxy-
gen to tissues except under extremely low oxygen
tension. Its principal function may be to aid recov-
ery from anaerobic conditions and to provide lim-
ited O2 to some critical tissues, such as the nervous
system. Hemoglobin occurs in certain cells of Gas­
trophilus spp. (horse bots) and in larvae and adults
of some beetles (Family Notonectidae, certain spe-
cies of the genera Anisops and Buenoa). In contrast
to the situation in Chironomus larvae, the hemo-
globin of the beetle Anisops pellucens is only 50%
saturation at a pO2 of 28 mmHg at 24°C (i.e., it will
give up half of its oxygen at 28 mmHg, a pressure
that might occur in actively metabolizing tissues),
giving it much more functional potential. The bee-
tle may get up to 75% of the O2 consumed during
a normal dive from its hemoglobin. Increased
temperature also causes the hemoglobin to release
more oxygen, which could be important to actively
working tissues such as muscles.
The embryo developing inside the egg must
obtain sufficient oxygen for development. The
majority of aquatic and semi-aquatic insects lay
eggs with no special respiratory structures incor-
porated into the shell, while eggs of a majority of
terrestrial insects contain special structures for
respiration, including an extensive, inner chorionic
meshwork that can function as a plastron when the
egg is submerged in well aerated water. Gas exchange
in eggs with no special respiratory structure occurs
by simple diffusion through the egg shell.
Non-Respiratory Functions of the
Tracheal System
Tracheae serve some important functions other
than gaseous transport. Tracheae act as the con-
nective tissue of insects, helping to tie cells and
­tissues together. Tracheae are important as a struc-
tural base for at least two important endocrine tis-
sues (i) the prothoracic glands whose cells are
attached to the tracheae near the prothoracic spir-
acle in larvae of Lepidoptera, and (ii) cells of the
epitracheal glands attached to the surface of the
major ventrolateral tracheal trunk to each spiracle
in lepidopterous larvae. Air sacs lie behind sound
producing organs in insects and are important to
sound modulation. A large air sac backs up to the
tymbal located on each side of the first abdominal
segment of male cicadas. The size of the air sac
varies with different species, and its size and tun-
ing are partly responsible for the species-specific
quality of the sound produced by male cicadas.
The interconnected prothoracic tracheae extend-
ing across the prothorax and into the protho-
racic legs of crickets act as a resonator of sounds.
They aid the cricket in discriminating direction of
sounds reaching the tympanal membrane located
just below the joint of the femur with the tibia (i.e.,
the knee joint) on each prothoracic leg. Hissing

cockroaches produce a hissing sound by expelling
air forcefully from certain spiracles when they are
disturbed. Lubber grasshoppers, R. guttata, release
quinones from the tracheal system on the side of
the attack when an ant attacks, or when stimulated
by probing.
References
Chapman RF (1998) The insects: structure and function.
Cambridge University Press, Cambridge, 770 pp
Klowden MJ (2002) Physiological systems in insects. Aca-
demic, New York, 415 pp
Nation JL (2002) Insect physiology and biochemistry. CRC,
Boca Raton, 485 pp
Tracheole
A very narrow trachea (1 µm or less in diameter)
that serves as the actual site of gas exchange between
the tracheal system and the body tissues because
they penetrate organs and lie so close to the cells.
 Tracheal System and Respiratory Gas Exchange
Trachypachidae
A family of beetles (order Coleoptera). They com-
monly are known as false ground beetles.
 Beetles
Trade Name
The name given a product that is marketed by a
company. The same product may be marketed by
more than one company using different names.
Trail Pheromone
A pheromone that is deposited along the ground
or other substrate that allows insects to maintain
the group or to communicate to others in their
Transgenic Arthropods for Pest Management Programs
T 3841
group (usually nest- or tent-mates) directionality,
often to a feeding location.
 Pheromones
 Sociality of Insects
Transcript
A mRNA copy of a gene.
Transcription
The process of producing a mRNA copy of a
gene.
Transformation
The process of changing the genetic makeup of an
organism by introducing foreign DNA. Transfor-
mation may be transient or stable (transferred to
succeeding generations.)
Transgene
The DNA that is inserted into the genome of a cell
or organism by recombinant DNA methods.
Transgenic Arthropods for Pest
Management Programs
Marjorie A. Hoy
University of Florida, Gainesville, FL, USA
Transgenic organisms contain genes that have
been introduced into the genome using biotech-
nology (recombinant DNA) methods. Transgenic
plants (including corn, rice, cotton and squash)
have been developed using recombinant DNA
methods and currently are grown commercially.
Development of the tools to develop transgenic
insects and mites has lagged behind that of plants
3842
T Transgenic Arthropods for Pest Management Programs
and microorganisms, but genetic modification
using recombinant DNA methods have been used
to transform a number of pest and beneficial
insects and mites. The successful transformation
of the fruit fly Drosophila melanogaster by a genet-
ically modified transposable element called the P
element in 1982 stimulated subsequent research to
genetically modify other insects (and mites) using
similar methods. (See the entry on Transforma-
tion of Drosophila melanogaster by P elements for
details of this method.)
Domesticated and semidomesticated insects
have been modified by traditional breeding meth-
ods for hundreds of years. Genetic manipulation
has improved disease resistance and silk produc-
tion in silk moths, and disease resistance and pol-
lination attributes in honey bees. More recently,
natural enemies of insects and mites used in bio-
logical control programs in agriculture and for-
estry have been modified by traditional breeding
methods and by hybridization of different strains
to achieve hybrid vigor. A pesticide-resistant pred-
atory mite (Metaseiulus occidentalis), developed
with traditional breeding methods, was incorpo-
rated into a integrated mite management program
in almonds in California. These predators pro-
vided effective control of spider mites, reduced the
need for costly pesticides, reduced production
costs and saved almond growers approximately
$22 million per year, most of which was due to
fewer applications of pesticides to control the spi-
der mites. This project demonstrated that genetic
improvement of natural enemies could result in
improved pest management programs. Genetic
improvement of natural enemies for biological
control of pest insects and mites by traditional
genetic methods has involved selecting for resis-
tance to pesticides, lack of diapause, and increased
tolerance to temperature extremes, although mod-
ification of other traits, such as sex ratio, theoreti-
cally could result in improved biological control.
During the past 40  years, a number of pest
insects have been sterilized by irradiation or
chemicals for use in genetic control programs.
This approach to pest management has been called
the sterile insect release method (SIRM) or the
sterile insect technique (SIT). Male insects are
mass reared and sterilized, usually by irradiation,
and released in to control a number of serious
pests, including the Mediterranean and Caribbean
fruit flies, mosquitoes and the New World screw-
worm Cochliomyia hominivorax. The SIRM has
been used to eradicate pests or to reduce pest
populations.
Sex and the Sorted Insects: A
Case Study
Genetic control of pest insects represents an
attractive alternative to chemical control of some
pests in terms of safety, specificity and the limited
negative effect this control tactic has upon the
environment. The screwworm (Cochliomyia hom­
inivorax) eradication campaign demonstrates
what can be achieved with mass releases of males
sterilized by irradiation.
The genetic control method used to eradicate
the screwworm was called the “sterile insect release
method” (SIRM) or “sterile insect technique” (SIT),
and involves mass rearing, sterilization of males by
chemicals or irradiation, and their subsequent
release to mate with wild females. Because females
of the screwworm mate only once, any wild female
mating with a sterile male fails to contribute prog-
eny to the next generation. By releasing an excess
of sterile males (compared to the number of wild
males), populations decline in a predictable man-
ner, ultimately becoming extinct. Because absolute
population densities were often low in the USA,
the number of sterile males that had to be released
could be produced in “fly factories.”
The screwworm eradication program in the
USA was initiated in Florida with small scale trials
on Sanibel Island in 1951. The results were prom-
ising and the project was geared up to cover the
state of Florida and then the southeastern USA.
The screwworm was declared eradicated from the
southeastern USA in 1959, one year ahead of
schedule. Eradication was achieved in a surprisingly

short time due to the combined effects of a severe
winter in Florida during 1957–1958, which greatly
reduced the overwintering screwworm popula-
tion, and a 17-month eradication program begin-
ning in July 1958 that cost approximately $7 million
and involved the release of almost nine billion
sterile screwworm flies over an area of approxi-
mately 56,000 square miles.
Since 1959, the livestock industry of Florida
and adjacent states have saved at least $20 million
each year because the screwworm is no longer
present; actual benefits are even greater in today’s
dollars. Furthermore, the elimination of losses due
to the deaths of livestock and labor and control
costs are only part of the benefits; loss of wildlife
to screwworm attack also was eliminated.
The success of the SIRM program in the south-
eastern USA led the cattle growers of Texas to
mount, in collaboration with the state and the
USDA, a similar but much more ambitious program
in the southwestern USA in the 1960s. This program
required more time and effort because the area in
which the screwworm was to be eradicated bordered
on a front 2,400 km long, stretching from the Gulf of
Mexico to the Pacific Ocean. Despite this challenge,
and some setbacks with quality control and rein-
vasion of flies from Mexico, both Texas and New
Mexico were declared “screwworm free” in 1964.
The SIRM program was moved into Arizona
and California in 1965, and in 1966 the entire USA
was declared free of screwworms. To reduce the
likelihood that the screwworm would reinvade the
USA from Mexico, the program was expanded
into Mexico in 1972, with the goal of eradicating
the screwworm all the way south to the Isthmus of
Tehuantepec.
After successfully eliminating the pest in
Mexico, the SIRM program was expanded to cover
all of Central America. Screwworms were elimi-
nated from Guatemala between 1988 and 1994,
from Belize between 1988 and 1994, from El Sal-
vador between 1991 and 1995, from Honduras
between 1991 and 1996, from Nicaragua between
1992 and 1998, from Costa Rica between 1995 and
1999, and from Panama between 1997 and 2000.
Transgenic Arthropods for Pest Management Programs
T 3843
These eradication programs were carried out so
that a barrier zone could be set up at the Isthmus
of Panama, which is only 190  km wide as com-
pared to the 2,400  km border that the USA and
Mexico share. This barrier zone has been main-
tained by a combination of quarantines and mass
releases of sterile screwworms.
Benefits of this massive, and expensive, screw-
worm eradication program are large. In 1996, the
annual producer benefits in the USA, Mexico
and  Central America were estimated to be $796
­million, $292 million and $77.9 million, respec-
tively. These benefits were due to decreases in
deaths of livestock, reduced veterinary services,
medicines, insecticides, inspections, handling
costs, and increases in meat and milk production.
The estimated benefit to cost ratios for the eradica-
tion programs average 12.2:1 for Central America
to 18:1 for the USA and Mexico.
The principle of sterile insect releases has
been applied to other pest insect species, including
the Mediterranean fruit fly (Ceratitis capitata), tse-
tse flies (Glossina palpalis and G. morsitans), mos-
quitoes (Anopheles albimanus), codling moth
(Cydia pomonella) and ticks.
Sterile insect release programs usually require
only males, but both sexes must be reared. Not
only is it expensive to rear large numbers of “use-
less” females, but, in the case of species that vector
disease or annoy or bite humans or domestic ani-
mals, it is undesirable to release any females, ster-
ile or not! As a result, various genetic methods
have been used to develop “genetic sexing strains.”
Slight differences in size or color of pupae have
been used to sort out undesirable females during
mass rearing. Most genetic sexing strains are based
on maintaining the desired genes (such as white
pupa or a temperature sensitive lethal) within
translocations. However, because translocations
can undergo recombination in the region between
the translocation breakpoint and the sexing gene,
the strains are not completely stable. As a result, if
no practical means exist to remove the recombi-
nants, an increasing number of the undesirable
females will be reared and released.
3844
T Transgenic Arthropods for Pest Management Programs
Ideally, a genetic sexing method using recom-
binant DNA methods will become available that
could produce only males of high quality and
vigor to compete with wild males for female mates.
Since an all-male colony will be difficult to main-
tain (!), this character ideally would be a condi-
tional trait, perhaps dependent upon temperature
or some other environmental cue. Because the
released males would be sterile they could not per-
sist in the environment, which could reduce poten-
tial risks. Other potential improvements using
recombinant DNA methods could result in insects
containing a marker gene, such as green fluores-
cent protein, that would allow the released sterile
males to be identified readily in the traps used to
monitor progress in the program; because such
males would be sterile, risks associated with their
release would also be low. Finally, recombinant
DNA methods might be developed that would
allow the insects to be sterilized without radiation;
this could reduce the damage produced by irradia-
tion to the entire body and allow fewer insects to
Transgenic Arthropods for Pest Management Programs, Table 13  Pest management goals that might be
achieved with transgenic methods
Project type
Biological control of insect and mite pests
•   Improve survival of natural enemies in
   environment
•   Improve effectiveness of natural enemies
Disease control method 
•   Develop insects that introduce a vaccine into
their hosts when taking a blood meal
Improve domesticated and semi-domesticated insects 
•   Improve silk production in silkworms
(Bombyx mori, Philosamia, Anthaerea)
•   Improve honey bees, Apis mellifera
be reared and released, resulting in considerable
cost savings.
Why Use Transgenic Methods?
Traditional genetic methods have limitations, and
recombinant DNA methods offer new opportuni-
ties for improving pest management programs
(Table 13). For example, significant benefits could
accrue if recombinant DNA methods allowed
sterile insects to be produced without incurring
the negative effects of irradiation. During the ster-
ilization process, the insect’s whole body is irradi-
ated, which damages all tissues. As a result, the
SIRM requires rearing very large numbers of males
for release because the irradiated males are dam-
aged by the sterilization process. Commonly, pest
populations are first reduced by pesticide applica-
tions or through natural seasonal (winter) mortal-
ity to reduce the number of insects that have to be
released. The number of males released is usually a
Objective(s)
Enhance ability to control pests by introducing
resistance genes; modify diapause or temperature
tolerance traits
Alter traits such as sex ratio (more females), host/
prey specificity; restrict ability to fly
Provide low cost vaccination against widespread,
serious diseases such as malaria
Improve quantity, quality or type of silk, introduce
disease resistance genes, introduce silk genes from
spiders or other silk producing arthropods into
moths to produce special types of silk
Insert genes for resistance to bacterial, viral and
fungal pest resistance; introduce resistance to mite
(Varroa) pests; modify pollination behaviors, modify
aggressive behaviors

Transgenic Arthropods for Pest Management Programs, Table 13  Pest management goals that might be
achieved with transgenic methods (Continued)
Project type
Population control methods 
•   Population replacement
•   Insert useful/deleterious genes
Sterile insect release method (SIRM) 
•   Sterilize males by recombinant DNA methods to
reduce damage from radiation/chemosterilization
•   Mark released males with molecular such as
green fluorescent protein, that can be detected
in trapped dead males so that the effectiveness
of the SIRM program can be assessed
•   Develop genetic sexing method so that females
do not have to be reared, reducing program costs can be killed during the mass rearing program
multiple of the estimated density of wild males,
with a 100:1 ratio of sterile to wild males com-
monly used. Rearing such huge numbers of insects
is costly and difficult.
Recombinant DNA methods also could allow
unique molecular markers to be inserted into the
sterile insects, which would allow SIRM program
Transgenic Arthropods for Pest Management Programs
T 3845
Objective(s)
Eliminate traits that make a pest, such as make a
pest unable to transmit diseases such as malaria,
dengue, sleeping sickness or yellow fever, by
altering ability of the pathogen to pass gut or
salivary gland barriers; eliminate the need for a
blood meal by vector mosquitoes; alter behavior
so the vector feeds on only one host. Release
altered strain to replace the pest population.
Replacement will require some type of drive
mechanism or a way to select for the released
­population in the field.
Release genetically modified individuals to mate
with a “driver” such as wild individuals in correct
ratio to insert genes transposable elements or
Wolbachia into populations. Proposals include
releasing (introgression model) insects with active
transposable elements, lethal genes or genes
that cause sterility, with the goal of causing so
much genetic damage that the pest
population crashes (as laboratory populations
can do when a new transposable element
invades)
Introduce genes and regulatory sequences to cause
sterility that can be stimulated by light, diet or other
environmental cues during mass rearing, as needed,
allowing colony to be reared normally until the
transgene(s) is activated
Insert benign marker gene that is expressed or vis-
ible in dead insects
Introduce a conditional lethal gene so that females
when a particular cue is provided
managers to more easily discriminate between
released sterile males and wild fertile males caught
in the traps used in monitoring the progress of the
program. Current marking methods using fluores-
cent dusts are unsatisfactory because they can
reduce fitness of the insects and the dyes do not
always adhere, which could falsely indicate that the
3846
T Transgenic Arthropods for Pest Management Programs
program is not working well. Other significant
benefits could be obtained if recombinant DNA
methods make it possible to control the sex of
insects being reared in SIRM programs, to intro-
duce lethal genes or genetic loads into pest popula-
tions, or to produce vectors of human and animal
diseases that are unable to transmit diseases such as
malaria, dengue, yellow fever and sleeping sickness.
Recombinant DNA techniques could make
genetic improvement of beneficial insects, such as
silkworms (Bombyx mori), honey bees (Apis mellif­
era) or biological control agents, more efficient and
less expensive. Once a useful gene has been cloned,
it could be inserted into a number of beneficial spe-
cies in a relatively short time. Furthermore, recom-
binant DNA methods broaden the number and
type of genes potentially available for use; no longer
is a project dependent upon the intrinsic genetic
variability of the species under study.
Many have speculated about the role that
recombinant DNA methods could play in the
genetic control of insects that serve as the vectors of
human and animal diseases or pests of agricultural
crops. Some consider transgenic technology to be a
new and vitally important pest management tool for
the control of serious pests that cannot be controlled
by any other means. Others have expressed reserva-
tions about the goals and methods suggested.
There are limitations to transgenic methods at
present. For example, traits primarily determined by
single major genes are most appropriate for manip-
ulating insects by recombinant DNA techniques.
Methods for manipulating and stabilizing traits that
are determined by complex genetic mechanisms are
not yet feasible with insects, although such methods
could be developed using procedures similar to
those developed by plant molecular geneticists.
Components of a Genetic
Manipulation Project
Genetic manipulation with recombinant DNA
methods requires methods for efficient and stable
insertion of foreign genes into the genome of the
target insect or mite, and the availability of useful
genes and appropriate promoters and other regu-
latory elements to obtain effective expression of
the inserted gene in the appropriate tissue at the
appropriate time. Inserting cloned DNA into
insects can be accomplished using several differ-
ent techniques. If the inserted DNA is incorpo-
rated into the chromosomes in the cells that give
rise to the ovaries and testes, the foreign gene(s) or
transgenes could be transmitted faithfully and
indefinitely to successive generations (stable ger-
mline transformation).
Initial research on stable transformation
methods was accomplished with Drosophila
melanogaster when it was discovered that the P
element could be genetically manipulated to serve
as a vector to carry foreign genes into the chromo-
somes of germ line cells. In molecular genetics,
vectors are self-replicating DNA molecules that
transfer a DNA segment between host cells.
P-­element vectors were investigated as possible
gene vectors for insects other than Drosophila, but
failed to function in other insects. Other trans-
posable element vectors such as mariner, piggy­
Bac, Hermes and hobo have been isolated from
insects and genetically modified for use as vectors
to transform insects other than D. melanogaster.
Another approach to genetic modification invo­
lves the genetic engineering of insect gut symbi-
onts. For example, a bacterial symbiont of the
Chagas disease vector Rhodnius prolixus lives in
the insect’s gut lumen and is transmitted from
adult to progeny by contamination of egg shells
or of food with infected feces. The symbionts have
been genetically engineered and transmitted to
hosts lacking any symbionts. The goal is to reduce
the ability of Rhodnius to transmit pathogens
when it takes a blood meal, perhaps by infecting
the bugs with gut bacteria that produce antibiotics
that kill the Chagas disease agent. Likewise, gut
symbionts of tsetse flies (Glossina species), which
are vectors of both animal and human African
sleeping sickness, also have been transformed.
Proposals have been made to release tsetse flies
carrying transgenic symbionts so the released flies

could replace or out-compete native populations,
but fail to transmit the disease.
The ability to introduce cloned genes into the
germ line at a predictable chromosomal site is
especially desirable, as it reduces the likelihood of
“position effects” on gene expression. Genes intro-
duced by transposable element and viral vectors
insert more or less randomly into the chromo-
somes, making it difficult to predict how well the
transgene will be expressed. One method for
accomplishing precise insertion is based on a sys-
tem found in the yeast Saccharomyces cerevisiae. A
gene for yeast recombinase, called FLP recombi-
nase, and two inverted recombination target sites
(FRTs) that are specifically recognized by the FLP
enzyme have been cloned. The FLP-FRT system
has been modified to insert DNA into a specific
site in a Drosophila chromosome. If the FRT sites
can be inserted into other insects, the system could
reduce concerns about unstable transformation
that may be elicited by the use of transposable ele-
ment vectors.
A few experiments have delivered linear or
circular plasmid DNA into the genome of insects
without using a specific vector. This approach has
the advantage of eliminating potential risks of
introducing vector sequences into the insect
genome, which could result in increased stability
of the inserted genes in the genome. This approach
assumes that the inserted gene is no more likely
than any other gene to be moved by “wild” trans-
posable elements or viruses.
A variety of methods have been evaluated
for delivering genes into insects in order to
achieve transformation. These include microin-
jection of transposable element vectors and other
vectors into dechorionated insect eggs, microin-
jection of plasmids directly into the abdomen of
female mites or insects (maternal microinjec-
tion), soaking eggs in DNA, using sperm to carry
foreign DNA into eggs of the honey bee, using
microprojectiles (gene gun technology) to insert
DNA into insect eggs, electroporation of DNA
into insect eggs, transplanting nuclei and cells,
and transformation of an insect microbial gut
Transgenic Arthropods for Pest Management Programs
T 3847
symbiont (which has been called paratrans-
genesis because the insect genome has not been
modified).
What Genes are Available to
Insert?
Cloned DNA can be isolated from the same or
other species. It is technically feasible to insert
genes from microorganisms into arthropods and
have the DNA transcribed and translated, although
coding sequences isolated from microorganisms
must be attached to promoters (controlling ele-
ments) and other regulatory sequences derived
from a higher organism so that the gene can be
expressed in insects. The regulatory sequences
determine when a gene will be transcribed, at what
level, in what tissues, and how long the messenger
RNA can be used for translation. Considerable
research is under way to identify regulatory
sequences that regulate genes in specific insect tis-
sues, such as the salivary glands and gut. It also may
be possible to isolate a gene from the species being
manipulated, alter it, and reinsert it into the germ
line, although this approach has not yet been
attempted in insects other than Drosophila to date.
Project goals will dictate what type of regula-
tory sequences might be most useful to regulate
transgene expression. In some cases, a low level
constitutive production of transgenic proteins will
be useful, while in other cases high levels of protein
production will be required after inducement by a
specific cue. Researchers may have to evaluate the
trade-offs between high levels of protein produc-
tion and the subsequent negative effects these could
have on fitness of the transgenic arthropod strain
based on the specific goals of each program.
After inserting the desired genes and regula-
tory elements, the next issue is how to detect
whether the gene has in fact been incorporated
into the germ line. Because transformation meth-
ods are relatively inefficient, a screening method is
needed to identify transformed individuals. This
process is relatively simple in Drosophila, where
3848
T Transgenic Arthropods for Pest Management Programs
there is a wealth of genetic information and visible
markers can be used to identify transgenic indi-
viduals. Most pest or beneficial arthropods lack
such extensive genetic information or markers.
Identifying transformed individuals could be
achieved using a pesticide resistance gene as the
selectable marker. However, the release of pesti-
cide-resistant pests into the environment would
create concerns about risk. Another option is to
use antibiotic resistance genes as selectable
markers to identify transgenic insects. However,
horizontal movement of resistance genes into
microbes in the environment could result in
increased levels of antibiotic resistance; the likeli-
hood of this potential risk has not been quantified.
Antibiotic resistance gene markers are no longer
considered safe for release into the environment in
transgenic crops, and methods have been devel-
oped for their removal. Another potential marker
is the β-galactosidase gene (lacZ) isolated from
E. coli, which can be detected by an assay that pro-
duces a blue color in the transformed insects and
mites. This construct has been present in a num-
ber of released organisms and it has been con-
cluded that risks associated with their release are
low. Eye color and green fluorescent protein (GFP)
genes also are considered to be safe selectable
markers if transgenic insects are to released into
the environment. Unfortunately, transgenic insects
with mutant eye colors may exhibit abnormal
behavior, which could reduce their effectiveness in
the field. The effects of GFP on vision could be
important when the GFP gene is expressed in
the eyes of insects. Normal behavior often is
crucial to the function of released insects in pest
management programs. It is probably desirable to
eliminate unneeded marker genes from trans-
genic insect strains prior to their release into the
environment.
Once transgenic strains have been produced,
they should be contained in the laboratory using
effective procedures and containment facilities
until permits have been obtained from the appro-
priate governmental agencies that would allow
the transgenic arthropods to be released into the
environment in a pest management program.
Transgenic strains must be evaluated for fitness
and the expression of the desired traits should be
stable in the laboratory. However, efficacy of the
transgenic strain for the intended purpose will
have to be evaluated eventually under field condi-
tions. At present, transgenic strains are first evaluated
in greenhouses, field cages, or some other con-
tained environment to be sure that they perform
as expected and do not exhibit unintended traits.
Purposeful permanent releases of transgenic
insects or mites have, as of winter 2004, not been
requested.
Risk Assessments of Transgenic
Arthropods
Risk equals the potential for damage and the like-
lihood of its occurrence. Risk estimates may be
different for pest versus beneficial insects and
may depend on whether the insect is expected to
persist in the environment or is unable to repro-
duce and cannot persist. Risks also will vary with
the specific transgene(s) inserted. At present, it is
easier to identify potential types of harm than to
quantify the likelihood of its occurrence.
Relative Risks
The least risky transgenic insects could be the
domesticated silkworm (B. mori), which is unable
to survive on its own in the wild. Transgenic
B. mori are unlikely to have a negative effect on
the environment because they should not be able
to persist even if they were accidentally released.
Also, transgenic pest or beneficial insects that are
sterile and unable to reproduce should pose lower
risk than insects that are able to reproduce and
persist in the environment. Transgenic pest or
beneficial insects that are unable to persist because
the environment is unsuitable during a portion of
the year also are likely to pose a lower risk. Honey
bees, Apis mellifera, are only semi-domesticated

and thus can escape human management to sur-
vive in the wild. Transgenic honey bees could pose
a greater environmental risk than the domesti-
cated silkworm for this reason.
Evaluating the risks associated with releasing
insects and mites that have been manipulated with
recombinant DNA techniques will likely change as
we learn more about risk assessment procedures
and gain experience. Current concerns can be
summarized as:
·· Is the transgenic population stable?
·· Has its host or prey range has been altered?
·· Does it have the potential to persist in the
environment?
·· Will the transgenic strain will have unintended
effects on other species or environmental processes?
Another question we may need to ask is how
far and how quickly can the transgenic strain dis-
perse from the experimental release site? Less is
known about dispersal behavior of many insects
than might be needed. The first three questions are
relatively easy to answer with a variety of labora-
tory experiments. The last issue is much more dif-
ficult to answer. For the near future, releases of
transgenic arthropods in the USA will be evalu-
ated by regulatory agencies on a case-by-case basis.
Initial permits for releases will be for short term
releases in controlled situations so that unexpected
outcomes might be mitigated.
Horizontal Gene Transfer
One risk issue that is unusually difficult to quan-
tify is the risk of horizontal transfer of transgenes
or transposable elements, or of drive elements
such as Wolbachia, to other organisms. Our knowl-
edge of horizontal transfer and transposable ele-
ments only began in the 1950s when Barbara
McClintock discovered transposable elements in
maize. Horizontal gene transfer results in the
movement of genes or transposable elements or
drive elements from one insect population to
Transgenic Arthropods for Pest Management Programs
T 3849
another of the same species, from one insect
species to another, or to other organisms in the
environment. It is difficult to quantify this risk
because we lack fundamental information on the
frequencies and mechanisms of horizontal gene
transfer; furthermore, the specific genes trans-
ferred will be important in determining potential
harm as will the site into which the transgene or
transposable element inserts. If the insertion is
into noncoding DNA in the chromosome, no
harm may occur to the recipient. If the insertion is
into functional and essential gene(s), then the
recipient may be harmed or killed. If the insertion
is into somatic cells the effect, if any, may be minimal
but if the insertion is into germ line cells then the
unintended genetic modification could be trans-
mitted to future generations. The whole topic of
horizontal gene transfer in insects has received
limited scientific attention until relatively recently.
We do know that horizontal transfer of genes
may occur between insect species by movement of
naturally occurring transposable elements. Hori-
zontal transfer is thought to be rare, yet more than
one such transfer has been observed within histori-
cal times in D. melanogaster and may have been
missed in other species because no one was look-
ing. The P element appears to have invaded D. mel­
anogaster populations within the last 50  years,
perhaps from a species in the D. willistoni group.
Controversy exists as to whether P elements were
transferred between Drosophila species by the semi-
parasitic mite Proctolaelaps regalis. Another trans-
posable element, hobo, appears to have invaded
natural populations of D. melanogaster around the
1960s, representing the second invasion of this well-
studied insect in the past 40–50 years.
Transfer of transposable element vectors from
insects to other organisms, including humans, is
potentially feasible, although these transfers would
be expected to occur very rarely. Recall that risk is
determined by frequency of occurrence and the
damage that might occur. In this case, the fre-
quency is expected to be very low if natural inva-
sions represent a realistic estimate of frequency
in the case of purposeful releases of active
3850
T Transgenic Arthropods for Pest Management Programs
t­ ransposable elements as drive mechanisms or
of conversion of inactive transposable element
vectors into active ones.
We are still discovering new aspects of the
biology and ecology of transposable elements and
this lack of knowledge makes it difficult to predict
what would happen if insects were released that
contained either active or inactive transposable
element vectors. The safest course might be to
remove any introduced transposable element vec-
tor sequences from a transgenic insect strain prior
to its permanent release into the environment to
reduce the probability that the transgene will
move, either within the strain or horizontally
between different populations or species.
Some questions to answer: When developing
a genetic manipulation project if it is to be deployed
successfully
PHASE I. Defining the problem and planning
the project:
·· What genetic trait(s) limit effectiveness of benefi-
cial species or might reduce damage caused by the
pest?
• Do we know enough about the biology,
behavior, genetics and ecology of the target
species to answer this question?
• Is the potential trait determined by single or
multiple genes?
·· Can alternative control tactics be made to work
more effectively and inexpensively than genetic
manipulation projects, and are they more environ-
mentally friendly?
• The costs of genetic manipulation projects
are high and the time to develop a functional
program can be quite long
• Transgenic technology may not be appropri-
ate if traditional genetic or other control
methods can be used because issues sur-
rounding risk assessment of releasing trans-
genic arthropods into the environment for
permanent establishment have not been
resolved.
·· How will the genetically-manipulated strain be
deployed?
• Will releases be inoculative and some type of
selection or drive system used to replace the
wild strain?
• Will the desired genes be introgressed (intro-
duced) into the wild population?
• What selection mechanism will be used?
• Will augmentative releases of very large num-
bers be required?
• Will multiple releases be required over many
years?
·· What risk issues, especially of transgenic strains,
should be considered in planning?
• If pesticide resistance genes are used as a
selectable marker for beneficial species is
there a possibility of the resistance gene mov-
ing to a pest?
• What is known about the potential for hori-
zontal gene transfer?
• If transposable element or viral vectors are
used in the transformation process, what
risks might they pose if the transgenic strain
is released into the environment?
• What health or other hazards might be
imposed on human subjects if the transgenic
strain were released?
·· What advice do the relevant regulatory authorities
give regarding your plans to develop a transgenic
strain?
• Which agencies are relevent to consult for
your project?
PHASE II. Developing the genetically-manip-
ulated strain and evaluating it in the laboratory:
·· Where will you get your gene(s)?
• Should the transgene(s) sequence be modified
to optimize expression in the target species if it
is from a species with a different codon bias?
·· Is it important to obtain a high level of expression
in particular tissues or life stages?
• Where can you get the appropriate regulatory
sequences?
·· How can you maintain or restore genetic variabil-
ity in your transgenic strain?
• Because both artificial selection and trans-
genic methods typically involve substantial
inbreeding to obtain pure lines, how will you

outcross the manipulated strain with a field
population to improve its adaptation to the
field or otherwise increase genetic variability.
·· What methods can you use to evaluate “fitness” in
artificial laboratory conditions that will best
predict effectiveness in the field?
• Have life table analyses and laboratory studies
of the stability of the trait under no selection
been correlated with efficacy in the field?
• Is it possible to carry out competitive popula-
tion cage studies?
·· Do you have adequate containment methods to
prevent premature release of the transgenic strain
into the environment?
• Have these containment methods been
reviewed by appropriate regulatory
authorities?
·· Do you have adequate rearing methods developed
for carrying out field tests?
• Are artificial diets available to reduce rearing
costs?
• Are quality control methods available to
maintain quality during mass rearing?
·· What release rate will be required to obtain the
goals you have set?
• Do you have an estimate of the absolute pop-
ulation density of the target species in your
field test?
• What release model are you applying: inun-
dative, inoculative, introgressioin, complete
population replacement?
·· Have you tested for mating biases, partial repro-
ductive incompatibilities or other population
genetic problems?
·· If the strain is transgenic, have you obtained approval
from the appropriate regulatory authorities to release
the strain into the greenhouse or small plot?
• Can you contain it in the release site?
• Can you retrieve it from the release site at the
end of the experiment?
• Can you mitigate if unexpected problems arise?
·· How will you measure effectiveness of the modi-
fied strain in the field trials?
PHASE III. Field evaluation and eventual
deployment in practical pest management project:
Transgenic Arthropods for Pest Management Programs
T 3851
·· If the small-scale field trial results were promising,
what questions remain to be asked prior to the
deployment of the manipulated strain?
• Are mass rearing methods adequate?
• Is the quality control program in place?
• Is the release model feasible?
• Were there unexpected reproductive incom-
patibilities between the released and wild
populations?
·· If permanent releases are planned, have relevant
risk issues been evaluated?
·· How will the program be evaluated for
effectiveness?
·· Will the program be implemented by the public or
private secto?
·· What did the program cost and what are the
benefits?
·· What inputs will be required to maintain the effec-
tiveness of the program over time?
(Modified from Hoy 2000.)
Steps in Developing a Transgenic
Arthropod
The above description indicates that a number of
steps are involved in a program designed to con-
trol pest insects through transgenic methods. The
target species probably should be identified as a
significant pest for which conventional control
tactics are ineffective because genetic manipula-
tion is usually more expensive and difficult than
other pest management approaches. Furthermore,
genetic manipulation with recombinant DNA
techniques may generate concerns about risk,
requiring additional time and resources.
How best might our knowledge about the pest
species’ physiology, ecology, or behavior be used
against it? How will the transgenic strain be
deployed in a pest management program?
Once a target trait has been identified, it must
be genetically altered using appropriate genes and
genetic regulatory sequences to ensure that the
new trait is expressed at the appropriate time and
in appropriate tissues. After a modified strain has
3852
T Transgenic Arthropods for Pest Management Programs
been developed, it must be evaluated in the labora-
tory for fitness and stability. If ultimate deploy-
ment requires mass rearing of very large numbers
of high quality insects, mass rearing and release
models will need to be developed. Eventually the
manipulated strain must be released into green-
houses or small field plots in the field for
evaluation.
Permission to release a transgenic insect will
have to be obtained from (several) regulatory
agencies. Short term releases initially will be made
into small plots, perhaps in cages. Initial releases
of transgenic insects into the environment in the
USA are intended to be short term experiments,
and current regulation of such releases by the U.S.
Department of Agriculture require the researcher
to retrieve all transgenic insects from the environ-
ment at the end of the experiment.
If the transgenic insect strain(s) perform well
and risk assessments are completed satisfactorily,
permanent releases into the environment may be
allowed, but the guidelines for such releases are
lacking as of spring 2002. Many pest management
programs, especially those involving replacement
of pest populations by the transgenic population,
will require permanent establishment in the envi-
ronment. The use of several “drive mechanisms”
have been proposed for replacement. Analysis of
the potential risks of such drive mechanisms has
not been carried out.
Could “Gene Silencing” Reduce
Program Effectiveness?
There is always the risk that a transgenic insect pop-
ulation could be released into the field and fail to
function as expected due to a phenomenon called
“gene silencing.” Transgenic plants and mammals
have been shown to be able to inactivate (silence)
transgenes that overexpress proteins or are other-
wise novel. Gene silencing is thought to be due to
genetic systems that evolved as a means to prevent
high levels of expression of transposable elements
or viruses that can cause genetic damage when
they invade new hosts. In fungi and plants, gene
silencing is associated with several mechanisms,
including methylation of the DNA or posttran-
scriptional or transcriptional processes. Multiple
mechanisms of transgene silencing also occurs in
Drosophila melanogaster. Thus, methods may have
to be developed to eliminate transgene silencing in
insects or this phenomenon could reduce the effec-
tiveness of a pest management program. The use of
genetic sequences called insulators or boundary
elements may limit gene silencing.
Gene silencing might be turned into a posi-
tive attribute if specific genes in insects could be
turned off. Gene silencing has purposefully
induced in D. melanogaster by introducing a
sequence that codes for an extended hairpin-loop
RNA by P-mediated transformation. Perhaps
endogenous gene expression and developmental
processes could be modified in other insects by a
similar genetic process.
The ultimate utility of transgenic insects and
mites for pest management programs remains to
be resolved in the coming years. Research on
improved transformation methods, isolation of
additional useful genes and regulatory elements
and development of improved risk assessment
methods based on an international consensus
must be achieved before transgenic arthropods
are widely used in pest management programs.
 Genetic Modification of Drosophila
melanogaster by P Elements
 Sterile Insect Technique
References
Atkinson PW, Pinkerton AC, O’Brochta DA (2001) Genetic
transformation systems in insects. Annu Rev Entomol
46:317–346
Handler AM, James AA (eds) (2000) Insect transgenesis
methods and applications. CRC, Boca Raton
Hoy MA (2000) Transgenic arthropods for pest manage-
ment programs: risks and realities. Exp Appl Acarol
24:463–495
Letourneau DK, Burrows BE (eds) (2002) Genetically engi-
neered organisms. Assessing environmental and human
health effects. CRC, Boca Raton

U.S. Department of Agriculture, Animal and Plant Health
Inspection Service (2001) The regulation of transgenic
arthropods. http://www.aphis.usda.gov:80/bbep/bp/
arthropod/#tgenadoc
Transgenic Organism
An organism whose genome contains genetic
material originally derived from an organism (not
its parents) or from a different species. The
transgene(s) can be transmitted to subsequent
generations (stable transformation) or can be lost
subsequently (unstable transformation).
Translocation
A type of mutation in which a section of a chro-
mosome breaks off and moves to a new position in
that or a different chromosome.
Transmission of Plant Diseases by
Insects
George N. Agrios
University of Florida, Gainesville, FL, USA
Plant diseases appear as necrotic areas, usually
spots of various shapes and sizes on leaves, shoots,
and fruit; as cankers on stems; as blights, wilts, and
necrosis of shoots, branches and entire plants; as
discolorations, malformations, galls, and root rots,
etc. Regardless of their appearance, plant diseases
interfere with one or more of the physiological
functions of the plant (absorption and transloca-
tion of water and nutrients from the soil, photo-
synthesis, etc.), and thereby reduce the ability of
the plant to grow and produce the product for
which it is cultivated. Plant diseases are generally
caused by microscopic organisms such as fungi,
bacteria, nematodes, protozoa, and parasitic green
algae, that penetrate, infect, and feed off one or
more types of host plants; submicroscopic organ-
isms such as viruses and viroids that enter, infect,
Transmission of Plant Diseases by Insects
T 3853
spread systemically and affect the growth of their
host plants; parasitic higher plants which range
from about an inch to several feet in size and pen-
etrate and feed off their host plants. Plant diseases
are also caused by abiotic, environmental factors
such as nutrient deficiencies, extremes in tempera-
ture and soil moisture, etc. that affect the normal
growth and survival of affected plants.
Of the aforementioned causes of disease,
many of the microscopic organisms and of the
viruses are transmitted by insects either acciden-
tally (several fungi and bacteria) or by a specific
insect vector on which the pathogenic organism
(some fungi, some bacteria, some nematodes, all
protozoa causing disease in plants, and many
viruses) depends on for transmission from one
plant to another, and on which some pathogens
depend on for survival (Fig. 90).
The importance of insect transmission of plant
diseases has generally been overlooked and greatly
underestimated. Many plant diseases in the field or
in harvested plant produce become much more
serious and damaging in the presence of specific or
non-specific insect vectors that spread the patho-
gen to new hosts. Many insects facilitate the entry
of a pathogen into its host through the wounds the
insects make on aboveground or belowground
plant organs. In some cases, insects help the survival
of the pathogen by allowing it to overseason in the
body of the insect. Finally, in many cases, insects
make possible the existence of a plant disease by
obtaining, carrying, and delivering into host plants
pathogens that, in the absence of the insect, would
have been unable to spread, and thereby unable to
cause disease. It is offered as a guess that 30–40% of
the damage and losses caused by plant diseases is
due to the direct or indirect effects of transmission
and facilitation of pathogens by insects.
Insects and related organisms, such as mites, are
frequently involved in the transmission of plant
pathogens from one plant organ, or one plant, to
another on which then the pathogens cause disease.
Equally important is that insects can and do trans-
mit pathogens among plants from one field to another,
in many cases even when the fields are several to
3854
T Transmission of Plant Diseases by Insects

Types of plant diseases

Proteins synthesized

Vitamins and
hormones formed
Shoot blight
Leaf blight
Reproduction and
storage of starch,
proteins and fats

Transpiration
Fruit spot

Fruit rot

Leaf spot

Carbon
Light dioxide Canker

Translocation
of water
and
minerals

Wilt
Food
translocation
Vascular
Photosynthesis wilt
(Food manufacture)
Crown gall

Sugars and nitrogen

form amino acids
Root rot

Uptake of water
and minerals Protein
synthesized

Transmission of Plant Diseases by Insects, Figure 90  Schematic representation of the basic functions in
a plant (left) and the interference with these functions (right) caused by some common types of plant
diseases (from Agrios 1997).

many miles apart. Almost all types of pathogens, externally on their legs, mouthparts, and bodies.
that is, fungi, bacteria, viruses, nematodes, and pro- Almost all plant pathogenic viruses, all phytoplas-
tozoa, can be transmitted by insects. Insects transmit mas, xylem- and phloem-inhabiting fungi and bac-
pathogens, such as many fungi and bacteria, mostly teria, some protozoa, and some nematodes are also
 Transmission of Plant Diseases by Insects
T 3855

transmitted by insects, and they are usually carried
by the insect internally. The insects that transmit
fungi and bacteria externally on their bodies and
legs belong to many orders of insects. On the con-
trary, the insects that transmit the other pathogens
listed above internally are very specialized and spe-
cific for the pathogen they transmit and belong to a
certain species or genus of insects (Fig. 91).
Insects transmit pathogens in three main ways.
(i) Many insects transmit bacteria and fungal spores
passively by feeding in or walking through an
infected plant area that has on its surface plant
pathogenic bacteria or fungal spores as a result of
the infection. The bacteria and spores are often
sticky, cling to the insect as it moves about, and
are carried by it to other plants or parts of the
same plant where they may start a new infection.
(ii) Some insects transmit certain bacteria, fungi,
and viruses by feeding on infected plant tissues and
carrying the pathogen on their mouthparts as they

Protozoon
5µ

3 Head of
nematode
2

0
Beet yellows virus
Tobacco mosaic virus
Wheat striate mosaic virus Fungus
Cucumber mosaic virus (mycelium)
Tobacco necrosis satellite virus
Hemoglobin molecule

Viroids

Mollicutes

Nucleus
Cell wall
Bacterium
Nucleolus

Transmission of Plant Diseases by Insects, Figure 91  Schematic diagram of the shapes and sizes of
certain plant pathogens in relation to a plant cell (from Agrios 1997).
3856
T Transmission of Plant Diseases by Insects

visit and feed on other plants or plant parts.
(iii) Several insects transmit specific viruses, phyto-
plasmas, protozoa, nematodes, and xylem- and
phloem-inhabiting bacteria by ingesting (sucking)
the pathogen with the plant sap they eat. Subse-
quently, the pathogen circulates through the body
of the insect until, with or without further multipli-
cation in the insect, the pathogen reaches the
salivary glands and the mouthparts of the insect
through which it is injected into the next plant on
which the insect feeds (Fig. 92).
Role of Insects in Bacterial
Diseases of Plants
In most plant diseases caused by plant pathogenic
bacteria (especially in those that cause spots, cankers,
blights, galls, or soft rots, bacteria), which are pro-
duced within or between plant cells, escape to the
surface of their host plants as droplets or masses of
sticky exudates (ooze). The bacteria exudates are
released through cracks or wounds in the infected
area, or through natural openings such as stomata,
nectarthodes, hydathodes, and sometimes through
lenticells, present in the infected area. Such bacte-
ria are then likely to stick on the legs and bodies of
all sorts of insects, such as flies, aphids, ants, beetles,
whiteflies, etc., that land on the plant and come in
contact with the bacterial exudates. Many of these
insects are actually attracted by the sugars con-
tained in the bacterial exudate and feed on it,
thereby further smearing their body and mouth-
parts with the bacteria-containing exudate. When
such bacteria-smeared insects move to other parts
of the plant or to other susceptible host plants, they

Fungi

Plasmodium Spore
Types of mycelium Colony Spores

Bacteria

Morphology and flagellation Fission Streptomyces

Mollicutes

Morphology Multiplication Spiroplasma

Parasitic
higher
plants

Dodder Witchweed Dwarf mistletoe Broomrapes

Viruses
Morphology Viroids

Nematodes

Adults Egg Juvenile Protozoa (Flagellates)

Transmission of Plant Diseases by Insects, Figure 92  Morphology and multiplication of some of the
groups of plant pathogens (from Agrios 1997).

carry on their body numerous bacteria. If the
insects happen to land on a fresh wound or on an
open natural opening, and there is enough mois-
ture on the plant surface, the bacteria may multiply,
move into the plant, and begin a new infection. The
same happens if the insects happen to create a fresh
wound on the plant.
The type of insect transmission of bacteria is
probably quite common and widespread among
bacterial diseases of plants, but it is passive and hap-
hazard, depending a great deal on the availability of
wounds or moisture on the plant surface. In any
case, there are few data on how frequently such
transmission occurs, and many conclusions about it
are the result of conjecture. A further point that has
been made is that insects which, whether above or
below ground, wound the host plant organs (roots,
shoots, fruit, etc.) by feeding or by ovipositing in
them, increase the probability of transmission of
plant pathogenic bacteria. This occurs because such
insects place the bacteria, with their mouthparts or
the ovipositor, in or around wounded plant cells,
where they are surrounded by a suspension of
nutrients (plant cell sap) in the absence of active
host defenses and where they can multiply rapidly
and subsequently infect adjacent healthy tissues.
Numerous plant diseases could be listed among
those in which bacteria are spread by insects pas-
sively as described above, for example, the bacterial
bean blights, fire blight of apple and pear, citrus
canker, cotton boll rot, crown gal, bacterial spot and
canker of stone fruits, etc. In several bacterial dis-
eases, however, the causal bacterium has developed
a special symbiotic relationship with one or a few
specific types of insects and depends a great deal on
these insects for its spread from infected to healthy
host plants. Some of the better known bacterium –
insect associations are described briefly below.
Bacterial Soft Rots
Bacterial soft rots cause tremendous losses world-
wide, particularly in the warmer climates and
the tropics. They are caused primarily by the
Transmission of Plant Diseases by Insects
T 3857
bacterium Erwinia carotovora pv. carotovora, to
some extent by Pseudomonas fluorescens and
Ps. chrysanthemi, and, occasionally, by species of
Bacillus and Clostridium. The last two genera of
bacteria cause rotting of potatoes and of cut fleshy
leaves in storage while Pseudomonas fluorescens
and Ps. chrysanthemi cause soft rots of many fleshy
fruits and fleshy vegetables. The species E. c. pv.
carotovora causes the vast majority of soft rots on
fleshy plant organs of any type (leave, blossoms,
fruit, stems, or roots), especially in storage and
under cover or in plastic bags. Affected fleshy fruits
are, for example, strawberries and other berries,
cantaloupes, peaches, pears, etc.; vegetables, for
example, tomatoes, potatoes, spinach, celery,
onions, cabbage, etc.; and ornamentals, for exam-
ple, cyclamen, iris, lily, etc. Nearly all fleshy vegeta-
bles are subject to bacterial soft rots. The soft rot
bacteria enter the plant organ through a wound,
sometimes in the field but more commonly during
storage, and there they multiply rapidly, secrete
enzymes that separate the cells from each other
and macerate the plant cell walls, which causes the
tissues to become soft and to rot. In many cases,
these bacteria are accompanied in the rotting tissues
by other saprophytic bacteria that further degrade
the softened plant tissue and cause it to give off a
foul odor. In all cases, rotting tissues become soft
and watery, and slimy masses of bacteria ooze out
from cracks in the tissues.
The soft rotting bacteria survive in infected
fleshy organs in storage and in the field, in plant
debris, in infected roots and other plant parts of
their hosts, in ponds and streams from where
irrigation water is obtained, and to some extent
in the soil and in the pupae of several insects. The
seedcorn maggot, Delia platura (Meigen) (Dip-
tera: Anthomyiidae), was shown to play an
important role in the dissemination and develop-
ment of bacterial soft rot in potatoes both in stor-
age and in the field. The soft rot bacteria are
usually introduced into a potato field on infected
or contaminated seed pieces but they can also
live in all stages of the insect, including the pupae,
and there they may survive cold or dry weather
3858
T Transmission of Plant Diseases by Insects
conditions. The insect larvae become contami-
nated with the bacteria as they feed in, or crawl
about on, infected seed pieces; they also carry the
bacteria to healthy plants and there they deposit
them into wounds they create. Even when the
plants or storage organs are resistant to soft rot
bacteria and can normally stop the advance of
the bacteria by developing a barrier of cork lay-
ers, the maggots destroy the cork layers as fast as
they are formed and the soft rot continues to
spread. Some other related flies, for example, the
bean seed maggot Delia florilega (Zetterstedt),
Drosophila busckii Coquillett (Diptera: Droso-
philidae), and probably others, seem to have
analogous relationship to the soft rot of potato
and other fleshy organs. It has also been shown
that several other flies have similar relationships
with soft rot bacteria and the host plants on
which they prefer to feed. Such relationships, for
example, exist between the cabbage maggot, Delia
radicium (Linnaeus) and soft rot in the Brassi-
caceae; the onion maggot, Delia antiqua (Mei-
gen), the onion black fly, Tritoxa flexa (Weidman)
(Diptera: Otitidae), the seedcorn maggot, and the
onion bulb fly, Eumerus strigatus (Fallen) (Dip-
tera: Syrphidae) and the soft rot of onion; and the
iris borer, Macronoctua onusta (Grote) (Lepi-
doptera: Noctuidae) and soft rot of iris.
The exact relationship between soft rot in
each host and each specific insect found to pos-
sibly be involved in the transmission of soft rot
bacteria from one organ or plant to another is
not clear. There is little doubt, however, that insect
transmission of soft rot bacteria does occur, that
insects help introduce the bacteria into wounds
they open, and that the presence of insects in
soft-rotting tissues inhibits the defense reaction
of the plants against the bacteria. The insects
also, by carrying the soft rot bacteria internally in
their bodies, help the bacteria survive adverse
environmental conditions. On the other hand,
the bacteria seem to help their insect vectors by
preparing for them a more nutritive substrate
through partial maceration of the host plant
tissues.
Bacterial Wilts of Plants
In several bacterial diseases of plants, the bacteria
enter the xylem conductive system of the plant and
there they move, multiply, and clog up the vessels.
The clogging of the xylem vessels is further
increased by substances released from cell walls by
bacterial enzymes and interferes with the translo-
cation of water through the stems to the shoots of
the plant. As a result of insufficient water, the leaves
and shoots loose turgor, wilt, and eventually turn
brown and die. In some bacterial wilts, the bacteria
destroy and dissolve parts of the xylem walls and
move into the adjacent tissues where they form
pockets full of bacteria from which the bacteria
ooze out onto the plant surface through cracks or
natural openings. In other bacterial wilts, the bac-
teria remain confined in the xylem and do not
reach the plant surface until the plant is killed by
the disease.
The wilt-causing bacteria overwinter in plant
debris in the soil, in the seed, in vegetative propa-
gative material, and in some cases, in their insect
vector. They enter plants through wounds, and
they spread from plant to plant through the soil,
through tools and direct handling of plants, or
through insect vectors. The most important bacte-
rial wilts in which insects play a significant role in
the transmission of the bacteria from plant to
plant are described briefly below.
Bacterial Wilt of Cucurbits
Bacterial wilt of cucurbits has been reported
from most developed countries but it probably
occurs throughout the world. It affects many spe-
cies of cucurbits, including cucumber, muskmelon,
squash, and pumpkin. Watermelon is resistant or
immune to bacterial wilt. Diseased plants develop
a sudden wilting of their foliage and vines and
eventually die. Diseased squash fruit develops a
slimy rot in storage. Losses from bacterial wilt vary
from an occasional wilted plant to destruction of
75–95% of the crop (Fig. 93).

Transmission of Plant Diseases by Insects, Figure 93  Disease cycle of bacterial wilt of cucurbits caused
by Erwinia tracheiphila and transmitted by the striped cucumber beetle (Acalymma vittatum) (from
Agrios 1997).
Bacterial wilt of cucurbits is caused by the
bacterium Erwinia tracheiphila. The bacterium
survives in infected plant debris for a few weeks
but it survives over winter in the intestines of its
two insect vectors, the striped cucumber beetle
(Acalymma vittatum [Fabricius]) and the spotted
cucumber beetle (Diabrotica undecimpunctata
Mannerheim [Coleoptera: Chrysomelidae]). The
bacterium depends on these two vectors for its
transmission to and inoculation of new plants. In
the spring, striped cucumber beetles and, to a
lesser extent, spotted cucumber beetles, that carry
bacteria, feed and cause wounds on the leaves of
cucurbit plants. The insects deposit bacteria in the
wounds through their feces and the bacteria enter
the wounded xylem vessels in which they multi-
ply rapidly and through which they move to all
parts of the plant. In the xylem, the bacteria
Transmission of Plant Diseases by Insects
T 3859
excrete polysaccharides, secrete enzymes that
break down some of the cell wall substances, and
induce xylem parenchyma cells to produce tylo-
ses in the xylem. All of them together form gels or
gums that clog the vessels, especially at their end
walls, thereby reducing the upward flow of water
in the xylem by up to 80% and causing the leaves
and vines to wilt. Beetles feeding on infected
cucurbit plants pick up bacteria on their mouth-
parts and when they feed onto healthy plants they
deposit the bacteria in the new wounds they have
made. Thus, the bacteria start a new infection.
Each contaminated beetle can infect several
healthy plants after one feeding on an infected
plant. It appears that a relatively small percentage
of beetles become carriers of the bacteria through
the winter. Spotted cucumber beetles transmit
the wilt bacteria rather late in the season,
3860
T Transmission of Plant Diseases by Insects
therefore they are considered less important
vectors of this disease than the striped cucumber
beetles.
Bacterial Wilt of Corn
This disease is also known as Stewart’s wilt of corn.
It is caused by the bacterium Pantoea (formerly
Erwinia) stewartii. It occurs in North and Central
America and also in Europe and China. It is more
severe in the northern states. The bacterium invades
the vascular tissues but it also spreads into other tis-
sues. When sweet corn plants are affected at the
seedling stage they may wilt rapidly and may die, or
they develop pale green wavy streaks on the leaves,
become stunted, wilt, and may also die. If infected
plants survive, they often tassel prematurely, the tas-
sels become bleached and may die, and produce
deformed ears. Bacteria also enter the stalk pith,
which they macerate in places near the soil line and
form cavities. From there the bacteria invade all
vascular tissues and spread throughout the plant.
Field corn is more resistant to early infection but
becomes more severely infected later in the season.
Some hybrids are susceptible and their symptoms
parallel those of sweet corn. Later infections, after
tasseling, produce irregular streaks on the leaves
that originate at feeding points of the corn flea bee-
tle, Chaetocnema pulicaria Melsheimer. The corn
wilt bacteria are also transmitted by the toothed flea
beetle (Chaetocnema denticulata Illiger), the spot-
ted cucumber beetle (Diabrotica undecimpunctata
howardi Barber), and by the larvae of the seed corn
maggot (Delia platura Meigen), wheat wireworm
(Agriotes mancus Say), and the May beetle (Phyl­
lophaga sp.). It appears, however, that overwintering
and spread of the bacteria in the field is carried out
primarily by the corn flea beetle.
These beetles cause direct damage to corn
leaves and seedlings but their main damage comes
from harboring and transmitting the bacteria from
plant to plant. The beetles pick up the bacteria when
they feed on infected corn plants. The bacteria sur-
vive in the digestive tract of the insect as long as the
latter lives. The insects are also the main place where
the bacteria overwinter. The corn flea beetles over-
winter as adults in the upper 2–3 cm of soil in grass
sod. They are rather sensitive to low temperatures,
however. In mild winters, when the sums of mean
temperatures for December, January, and February
are above 3–4°C, large numbers of beetles survive.
When the soil warms up to about 17–20°C, they
begin to feed on corn seedlings, which they infect
with bacteria. Following mild winters, bacterial wilt
of corn is spread rapidly by corn flea beetles, and
corn losses can be quite severe. During cold winters
that average temperatures below 0°C, many of the
beetles do not survive and the incidence and spread
of bacterial wilt of corn the following spring and
summer are quite limited.
Southern Bacterial Wilt of Solanaceous
and Other Crops
This vascular wilt is caused by the bacterium Ralsto­
nia solanacearum. It occurs in the warmer regions
around the world and is particularly severe in the
tropics. It is known by different names in different
hosts, for example, southern wilt or brown rot in
potato and tomato, Granville wilt in tobacco, and
Moko disease in banana. Insects, primarily bees
(Trigona corvine Cockerell, Hymenoptera: Apidae),
wasps (Polybia spp., Hymenoptera: Vespidae), and
flies (Drosophila spp., Diptera: Drosophilidae) have
been implicated as vectors. Because these and other
insects visit infected stem wounds and natural
abscission sites oozing out bacteria, they are consid-
ered as playing a role in the transmission of the bac-
teria to natural infection courts and in providing
wounds for bacterial entry, but their importance as
vectors has not been documented.
Fire Blight of Pears, Apples and Other
Rosaceous Plants
The disease is caused by the bacterium Erwinia
amylovora. Fire blight occurs in North America,

Europe and countries surrounding the Mediterra-
nean Sea, and in New Zealand. It continues, how-
ever, to spread into new countries. Fire blight is the
most devastating diseases affecting rosaceous
plants. The symptoms consist of infected blossoms
and young shoots becoming discolored and water-
soaked, then being killed rapidly and appearing
brown to black as though scorched by fire. The dis-
ease spreads rapidly into larger twigs and branches,
which it also kills, and parts of or entire trees may
be killed. At the base of twig or branch infections,
cankers develop at the margins of which the bac-
teria overwinter. Fruit also become infected and
ooze droplets of bacteria. The bacteria kill and
macerate the contents of primarily parenchyma
cells on flowers and in the bark of young shoots
and twigs, but as they destroy these cells they move
on mass in the bark. The bacteria also enter the
phloem and xylem vessels through which they
may move over relatively short distances.
The fire blight bacteria overwinter at the mar-
gins of cankers of twigs and branches. In the spring,
the bacteria around cankers multiply and their
byproducts absorb water and build up internal
pressure. This results in droplets of liquid contain-
ing masses of fire blight bacteria oozing out of the
cankers. The bacteria in the ooze are disseminated
by splashing rain and also by flying and crawling
insects, several of which are attracted to the bacte-
rial ooze, and their legs, bodies, and mouthparts
become smeared with bacteria. More than 200 spe-
cies belonging to many insect groups, including
aphids, leafhoppers, psyllids, beetles, flies, and ants,
have been shown to visit oozing cankers and
healthy blossoms, although bees and wasps seem
not to visit oozing cankers routinely. Insects
smeared with bacteria oozing out at cankers carry
the bacteria to young shoots where they deposit
them in existing wounds or in fresh wounds they
make upon feeding, or in the nectar of the flowers.
Once the fire blight bacteria are transmitted to
blossoms by rain or insects, they enter the flower
tissues through nectarthodes or wounds, multiply
rapidly in them, and ooze out of them and com-
mingle with the nectar in the flower. The same
Transmission of Plant Diseases by Insects
T 3861
kinds of insects apparently can transmit fire blight
bacteria from infected to healthy flowers but flower
to flower transmission of fire blight bacteria is car-
ried out so much more efficiently by pollinating
insects, namely bees, that the contribution of other
insects to that type of transmission seems to be
relatively insignificant. As honeybees, wild bees,
bumblebees, wasps, and other insects visit pear,
apple, and other flowers infected with fire blight
bacteria, their mouthparts, legs, and other body
parts become smeared with the bacteria in the nec-
tar. The insects then carry the bacteria and deposit
them in the nectar of healthy flowers they visit and
there the bacteria start new infections. The bacte-
ria, however, do not survive on or in the insects
for more than a few days and do not appear to
overwinter in association with the insects.
Olive Knot
Olive knot is caused by the bacterium Pseudomo­
nas savastanoi. It occurs in the Mediterranean
region, in California, and probably the other parts
of the world where olive trees grow. The disease
occurs as rough galls of varying sizes developing
on leaves, branches, roots, on leaf and fruit peti-
oles, and on wounds in tree branches and trunks.
Sometimes the galls are so numerous on twigs that
the twigs decline and may die back. The galls are
the result of growth regulators being produced
by the bacteria, which grow and multiply in the
intercellular spaces of the outer cells of the galls. In
California, the bacteria are spread by running and
splashing rain water that carries the bacteria to
existing wounds, pruning wounds, and leaf scars.
In other parts of the world, however, such as the
Mediterranean region, the olive knot bacteria are
also spread by the olive fly or olive fruit fly, Bactro­
cera (formerly Dacus) oleae (Gmelin) (Diptera:
Tephritidae), which is the most destructive pest of
olive in its own right.
The bacterium and the olive fly have devel-
oped a close symbiotic relationship that contrib-
utes to the transmission of the olive knot bacteria
3862
T Transmission of Plant Diseases by Insects
from tree to tree. The bacteria are carried by all
stages (larvae, pupae, and adults) of the olive fly.
The adult olive flies, and related fly species, have
specialized structures along their digestive tract
that are filled with bacteria. There is even a con-
nection of the digestive tract with the oviduct
that insures contamination of the eggs before
oviposition. Transmission of the bacteria by the
insect takes place during feeding and oviposition
into olive tissues. The bacteria actually penetrate
the egg through the micropyle, thereby ensuring
that when the larvae hatch they are contaminated
with the bacteria. It appears that while the olive
fly plays a significant role in the transmission of
the olive knot bacteria, the bacteria contribute to
the insect by hydrolyzing proteins and making
available to the insect certain amino acids needed
by the insect for survival of the larvae and for
development of adults.
Insect Transmission of Xylem-
Inhabiting Bacteria
Quite a few important bacterial diseases of plants,
primarily trees, are caused by the fastidious bacte-
rium Xylella fastidiosa. These bacteria inhabit the
xylem of their host plants and are rather difficult
to isolate and to grow on the usual culture media.
The diseases they cause differ from the vascular
wilts caused by conventional bacteria in that
instead of wilt they cause infected plants to decline,
some of their twigs to die back, and in some cases
the whole plant to die. The xylem-inhabiting fas-
tidious bacteria are transmitted in nature only by
xylem-feeding insects, such as sharpshooter leaf-
hoppers (Cicadellidae: Cicadellinae) and spittle-
bugs (Cercopidae). Xylella bacteria seem to be
distributed in tropical and semitropical areas
worldwide. Among the most important diseases
caused by Xylella are Pierce’s disease of grape and
citrus variegated chlorosis. Other diseases caused
by xylem-inhabiting bacteria include phony peach,
plum leaf scald, almond leaf scorch, bacterial leaf
scorch of coffee, oak leaf scorch, and leaf scorch
diseases of oleander, pear, maple, mulberry, elm,
sycamore, and miscellaneous ornamentals, as well
as the alfalfa dwarf disease (Fig. 94).
Pierce’s Disease of Grape
Pierce’s disease is a devastating disease of European-
type grapevines (Vitis vinifera). It is caused by the
xylem-inhabiting bacterium Xylella fastidiosa. It
occurs in the Southern United States and in Cali-
fornia, in Central America, and parts of north-
western South America. The presence of Pierce’s
disease in an area precludes the production of
European-type grapes in that area but some mus-
cadine grapes and hybrids of European grapes
with American wild grapes are tolerant or resis-
tant to Pierce’s disease. The Pierce’s disease bacte-
rium moves and multiplies in the water-conducting
(xylem) vessels of shoots and leaves, some of which
become filled with bacteria and reduce the flow of
water through them. Leaves beyond such blocked
vessels become stressed from lack of sufficient
water and develop yellowing and then ­drying or
scorching along their ­margins. During the sum-
mer, the scorching ­continues to expand toward
the center of the leaf, while some or the entire
grape clusters begin to wilt and dry up. Scorched
leaves fall off leaving their ­petioles still attached to
the vine, while the vines mature unevenly and have
patches of brown (mature) and green bark. In the
following season(s), affected grapevines show
delayed growth and stunting. The leaves and vines
repeat the symptoms of the first year and both, the
top of the plant as well as the root system, decline
and die back.
The bacterium that causes Pierce’s disease of
grape is Xylella fastidiosa. The bacterium appar-
ently consists of various host specific strains. The
strain that causes Pierce’s disease of grape also
causes alfalfa dwarf disease and almond leaf
scorch. Apparently related but different strains
of the bacterium cause citrus variegation chloro-
sis, the other related leaf scorch diseases of fruit
and forest trees and of ornamental trees and
 Transmission of Plant Diseases by Insects
T 3863

Insect feeds on new

annual or perennial
plants, does not yet
transmit pathogen
(incubation period)
Pathogen is ingested into When pathogen is present in
gut lumen, later passes into salivary glands (sg) in large numbers
hemolymph, muscles, glands, etc, it is injected into new plants

Insect vector
feeds on vein of infected plant

Vector feeding on
leaf of healthy plant

Healthy insect vector feeds

on recently infected plant
and obtains pathogen

Pathogen spreads along

veins into new leaf
Vectors overwinter
Pathogen (e.g. mycoplasma) over winters os eggs or adults on Pathogen spreads
in trees, shrubs or perennial hosts or ground systemically through
herbaceous hosts. veins of plant

Transmission of Plant Diseases by Insects, Figure 94  Sequence of events in the overwintering,

acquisition, and transmission of plant viruses, mollicutes, and fastidious bacteria by leafhoppers (from
Agrios 1997).

shrubs. The identity and taxonomy, as well as the
host range and vector preference of the possible
strains of Xylella fastidiosa, are unknown. In all
cases, the bacterium is transmitted from plant to
plant through vegetative propagation, such as
cuttings, budding, and grafting, and by one or
more of several closely related insects. The
known vectors of Xylella fastidiosa are sharp-
shooter leafhoppers (family Cicadellidae, sub-
family Cicadellinae) or spittlebugs (family
Cercopidae). It is possible that other or all suck-
ing insects that feed on xylem sap, for example,
the cicadas (family Cicadidae), are also vectors
of Xylella fastidiosa. In California, there are at
least four important sharpshooter leafhopper
vectors of Xylella: The blue-green (Graphocephala
atropunctata), the green (Draeculacephala
­ inerva), the red-headed (Carneocephala fulg­
m
ida), and the glassy-winged (Homalodisca coag­
ulata) sharpshooters. The vectors may be
different in other parts of the world. All vector
insects acquire the bacteria when they feed on
infected plants. Ingested bacteria seem to adhere
to the walls of the foregut of the insect and when
the insect moves to and feeds on the next healthy
plant, the insect transmits the bacteria into the
xylem vessels of that plant where they multiply
and cause a new infection. Once a vector acquires
bacteria from a diseased plant, it remains infec-
tive indefinitely. When, however, infective insects
shed their external skeleton by molting, they
loose the bacteria and must feed on a diseased
plant again before they can transmit the bacteria
to healthy plants.
3864
T Transmission of Plant Diseases by Insects
Insect Transmission of Phloem-
Inhabiting Bacteria
At least four plant diseases are caused by bacteria
that inhabit only the phloem of their host plants.
These diseases include the destructive citrus green-
ing disease, the severe papaya bunchy top disease,
the cucurbit yellow vine disease, and the infrequent
clover club leaf disease. The bacteria causing these
diseases have not yet been grown on nutrient media
and so far many of their properties remain unknown.
All of them, however, are transmitted from plant to
plant only by specific insect vectors. The citrus
greening bacterium is transmitted by a psyllid,
while the papaya bunchy top disease bacterium and
the clover club leaf bacterium are transmitted by
leafhoppers, and the cucurbit yellow vine disease
bacterium is transmitted by the squash bug. In the
psyllid and leafhopper vectors, the bacterium also
multiplies in and is passed from the mother insect
to its offspring through the eggs (transovarial
transmission). It is not known what happens to the
bacteria transmitted by the squash bug.
Citrus Greening Disease
Citrus greening is a very destructive disease of all
types of citrus. It occurs in most citrus producing
areas of Asia, including the Arabian Peninsula, and
in Africa. The disease is caused by the bacterium
Liberobacter asiaticum in Asia, and L. africanum in
Africa. Both bacteria are limited to the phloem of
the host plants, and have yet to be cultured. The
disease first appears as a chlorosis and leaf mottling
on one shoot or branch, which it has given it the
name “huanglongbing,” or “yellow shoot,” in
­Chinese. Later on, entire trees become chlorotic as
though they are suffering from zinc deficiency,
their twigs die back, and the trees decline rapidly
and become non-productive. Fruit on diseased
trees is small, lopsided, and does not color uni-
formly as it ripens but large parts of it remain green
even when mature, thereby the “greening” name of
the disease. Diseased fruit is also quite bitter.
Citrus greening is spread by vegetative propa-
gation with buds and grafts, and by at least two
citrus psyllids: Diaphorina citri Kuwayama, which
is the principal vector of the more severe and more
destructive Asian form of the citrus greening
­bacterium that occurs at higher temperatures
(30–35°C), commonly found at lower elevations;
and Trioza erytreae Del Guercio, which is the prin-
cipal vector of the milder, less severe, lower tem-
perature (27°C) African form of the bacterium,
which is normally found at higher elevations. Both
vectors, however, can transmit both forms of the
bacterium. Asian psyllids acquire the bacterium
within 30  min of feeding while African psyllids
require 24 h. The bacterium apparently multiplies
in the vector and can be transmitted within
8–12 days from acquisition.
Infected plants and vectors have been intro-
duced into several citrus-producing countries but
in most cases it was eradicated before it could
become established. The vector of the greening
bacterium Diaphorina citri was introduced in
­Brazil in the early 1980s and in Florida in 1998
but, so far, the causal bacteria apparently have not
been introduced and no trees have been found in
either place to be infected with citrus greening.
Bunchy Top of Papaya Disease
Bunchy top is a devastating disease of papaya. It
occurs in most or all islands of the Caribbean
Basin and, probably, also in Central America and
in the northern part of South America. Young
leaves of infected plants show mottling, then
chlorosis and marginal necrosis, and become
rigid. Internodes become progressively shorter,
further apical growth stops, and the plant devel-
ops a “bunchy” top. Older leaves may fall off, any
fruits that are set are bitter, and the entire plant
may die.
Bunchy top of papaya is caused by a rickettsia-
like phloem-limited bacterium that moves and
multiplies in the phloem elements of the plant.
The bunchy top bacteria are transmitted from

diseased to healthy papaya plants by the leafhop-
pers Empoasca papayae Oman and E. stevensi
Young. Symptoms appear 30–45  days after
inoculation.
Cucurbit Yellow Vine Disease
Yellow vine disease affects watermelon, melon,
squash, and pumpkin. It was first reported in
the Texas–Oklahoma area and has since been
found in Massachusetts, New York, and Tennessee.
Affected plants show vines with yellow leaves, the
phloem of leaves and vines becomes discolored,
and the leaves and vines collapse and die. The dis-
ease has been severe in the Texas and Oklahoma
areas where it annually destroys thousands of acres
of cucurbits costing millions of dollars.
Cucurbit yellow vine disease is caused by a
phloem-limited bacterium that has been placed in
the species Serratia marcescens and its properties
are still being characterized. The bacterium is most
probably transmitted by insect vectors. The squash
bug, Anasa tristis, is considered to be a vector of
this bacterium, but its involvement in transmitting
this bacterium has been questioned.
Insect Transmission of Plant
Diseases Caused by Mollicutes
Mollicutes are prokaryotes (bacteria) that lack cell
walls. In nature, plant pathogenic mollicutes are
limited to the phloem of their host plants. Plant
pathogenic mollicutes are generally classified as
belonging to the genus Phytoplasma. Most phyto-
plasmas have an irregular spherical to elongated
shape and have been obtained and maintained on
complex nutrient media, although they do not
readily grow or multiply on them. A few plant
pathogenic mollicutes typically have spiral mor-
phology and belong to the genus Spiroplasma.
Spiroplasmas grow and multiply readily on spe-
cialized nutrient media. Plant diseases caused
by mollicutes appear as yellowing of leaves,
Transmission of Plant Diseases by Insects
T 3865
proliferation of shoots (witches’ brooms) and of
roots, stunting of shoots and whole plants, green-
ing of flowers, abortion of flowers and fruit, die-
back of twigs, and decline and death of trees.
Numerous important diseases of annual crops are
caused by mollicutes, mostly phytoplasmas, for
example, aster yellows of vegetables and orna­
mentals, tomato big bud (stolbur), corn stunt,
etc. ­Phytoplasmas cause even more, and more
severe, diseases on trees, including X-disease of
peach, peach yellows, apple proliferation, elm yel-
lows, pear decline, and lethal yellowing of coconut
palms. Spiroplasmas also cause severe diseases, for
example, corn stunt, and citrus stubborn disease.
All mollicutes, that is, phytoplasmas and
spiroplasmas, are spread from plant to plant
through vegetative propagation and, in nature,
these pathogens depend for their transmission on
phloem-feeding, sap-sucking insects, mainly leaf-
hoppers, planthoppers, and psyllids. These insects
can acquire the pathogen after feeding on appro-
priate infected plants for several hours or days, or
if they are artificially injected with extracts from
infected plants or insects. More insects become
vectors when they feed on young leaves and stems
of infected plants than on older ones. The insect
vector cannot transmit the pathogen immediately
after feeding on the infected plant but it begins to
transmit it after an incubation period of 10–45 days,
depending on the temperature. The quickest trans-
mission (10 days) occurs at about 30°C, while the
slowest (45 days) takes place at about 10°C.
The reason for the incubation period is that
the acquired phytoplasmas or spiroplasmas must
first multiply in the intestinal cells of the insect
vector and then move through the insect by pass-
ing into the hemolymph, then infect internal
organs and the brain, and finally reach and multi-
ply in the salivary glands. When the concentration
of the pathogen in the salivary glands reaches a
certain level, the insect begins to transmit the
pathogen to new plants and continues to transmit
it with more or less the same efficiency for the rest
of its life. Insect vectors are not generally affected
adversely by the phytoplasmas or spiroplasmas
3866
T Transmission of Plant Diseases by Insects
multiplying in their cells, but in some cases they
show severe pathological symptoms. Phytoplas-
mas and spiroplasmas can be acquired as readily
or better by nymphs than by adult leafhoppers,
etc., and they survive through subsequent molts of
the insect. The pathogens, however, are not passed
from the adults to the eggs and to the next genera-
tion. For this reason, young insects of any stage
must feed on infected plants in order to become
infective vectors.
Some of the most important plant diseases
caused by mollicutes and their insect vectors are
described briefly below.
Aster Yellows
Aster yellows is caused by phytoplasmas and
occurs worldwide. It affects numerous annual
crops, mostly vegetables and ornamentals, for
example, tomato, lettuce, carrot, onion, potato,
chrysanthemum, aster, and many others, on
which it causes severe symptoms and serious
losses, in some crops amounting to 10–25% of
the crop and occasionally up to 80–90% of the
crop. Plants infected with aster yellows develop
general chlorosis (yellowing) and dwarfing of the
whole plant, abnormal production of shoots and,
sometimes, roots, sterility of flowers, malforma-
tion of organs, and a general reduction in the
quantity and quality of yield. The aster yellows
phytoplasma is transmitted by several leafhop-
pers, one of which is the aster leafhopper Mac­
rosteles fascifrons. The various leafhopper vectors
have a wide host range, as does the aster yellows
phytoplasma. The phytoplasmas survive in peren-
nial ornamental, vegetable, and weed plants. The
vector leafhopper acquires the phytoplasmas
while feeding by inserting its stylet into the
phloem of infected plants and withdrawing the
phytoplasmas with the plant sap. After an incuba-
tion period, when the insect feeds on healthy
plants it injects the phytoplasmas through the
stylet into the phloem of the healthy plants where
they establish a new infection and multiply.
The phytoplasmas move out of the leaf and
spread throughout the plant causing the symp-
toms characteristic of the host plant.
Tomato Big Bud
The disease occurs in many parts of the world but
except for a few areas, it is of little economic
importance. It affects most Solanaceous vegetables
and lettuce. The symptoms include small, distorted,
yellowish green leaves and production of numer-
ous thickened, stiff, and erect apical stems that
have short internodes. The flower buds are exces-
sively big, green, and abnormal looking, and fail to
set fruit. Fruit present when infection takes place
becomes deformed.
Tomato big bud is caused by a phytoplasma
that is transmitted by several leafhoppers, the main
one of which is the common brown leafhopper
Orosius argentatus. The insect feeds and breeds on
infected weed hosts and when they become unde-
sirable the insects move into tomato or other crops
bringing with them the big bud phytoplasmas.
Apple Proliferation
It is the most important insect transmitted disease
of apple in most of Europe. It may also occur in
South Asia and South Africa. Depending on prev-
alence in an orchard, apple proliferation may cause
economic losses of 10–80% due to reduction in
fruit size, total yield, and vigor of trees. The most
conspicuous symptoms of apple proliferation are
the production of witches’ brooms or of leaf
rosettes, and of enlarged stipules at the base of
leaves. Affected trees leaf out earlier in the spring
but flowering is delayed. The leaves, fruit, and
entire trees are smaller, and fruit color and taste
are also poor. Proliferating shoots are often infected
with powdery mildew.
Apple proliferation is caused by a phyto-
plasma that also infects other wild and ornamental
apple species, and possibly pear and apricot.

The phytoplasma is spread in nature by several
leafhoppers, including Philaenus spumarius, Aph­
rophora alni, Lepyronia coleoptrata, Artianus inter­
stitialis, and Fieberiella florii. The leafhopper vectors
acquire the phytoplasmas when they feed on the
phloem elements of young leaves and shoots of
infected apple trees and, after an incubation period,
transmit the phytoplasmas into healthy apple trees.
The time between inoculation and appearance of
symptoms varies with the size of the inoculated
tree. Young nursery trees may develop symptoms
within a year while large established trees may do
so 2 or 3 years after inoculation.
Pear Decline
It is a serious disease of pear resulting in signifi-
cant crop losses and also in stunting and death of
affected pear trees grown on certain rootstocks.
The disease, which is caused by a phytoplasma,
occurs in North America and in Europe, and
probably in many other parts of the world where
pears are grown. The symptoms of pear decline
may develop as a quick decline, that is, sudden
wilt and death of a tree within a few days or weeks,
with or without first showing reddening of leaves,
or a slow decline. Quick decline usually develops
on trees propagated on certain hypersensitive
rootstocks in which a brown necrotic line devel-
ops at the graft union of the tree. Slow decline also
occurs on trees grafted on the same or other root-
stocks, and appears as a progressive weakening of
the tree of varying severity. Slow declining trees
have reduced or no terminal growth, have few,
small, leathery, light green leaves whose margins
are slightly rolled up and may be yellow or red in
the autumn. Such trees may or may not die a few
years after infection. Some infected pear trees,
however, show primarily a reddening of the leaves
in late summer or early autumn, and mild reduc-
tion in vigor.
The pear decline phytoplasma is transmitted
from tree to tree by grafting and by the pear psylla
(Psylla pyricola Forster) and in Europe, probably
Transmission of Plant Diseases by Insects
T 3867
by P. pyri and P. pyrisuga. Pear psylla acquires the
phytoplasma after feeding on infected trees for a
few hours and remains infective for several weeks.
Young trees inoculated with phytoplasma by the
insect show symptoms the same or the next year,
while older trees may take longer. The phyto-
plasma  is sensitive to low temperatures and dies
out in the above-ground parts of the tree but sur-
vives in the tree roots. In the spring, the phyto-
plasma recolonizes the stem, branches and shoots
and from the latter it can be acquired and trans-
mitted again by the insect vectors.
Lethal Yellowing of Coconut Palms
Lethal yellowing is a blight that kills coconut and
some other palm trees within 3–6  months from
the time the trees show the first symptoms. It
occurs in Florida, Texas, Mexico, most Caribbean
islands, in West Africa, and elsewhere. The disease
appeared for the first time in Florida in 1971 and
killed 15,000 coconut palm trees the first two
years, 40,000 by the third year, and by the fourth
year (1975), 75% of the coconut palms in the
Miami area were dead or dying from lethal yellow-
ing. The disease appears as a premature drop of
coconuts followed by blackening and death of the
male flowers. Subsequently, first the lower and
then the other leaves turn yellow and then brown
and die, as does the vegetative bud, and the entire
top of the tree falls off leaving the palm trunk
looking like a telephone pole.
Lethal yellowing is caused by a phytoplasma
that lives and multiplies in the phloem elements
of the plant. The main means of spread of lethal
yellowing from tree to tree is through the plan-
thopper Myndus crudus, although other vectors
are also possible. As with the other phytoplasma
diseases, the vector acquires the phytoplasma
while sucking juice off the phloem of palm leaf
veins, the phytoplasma multiplies in the vector
during an incubation period, and the insect then
transmits the phytoplasma when it visits and feeds
on leaf veins of healthy palm trees.
3868
T Transmission of Plant Diseases by Insects
Corn Stunt
Corn stunt causes severe losses where it occurs
although losses vary from year to year. It occurs in
the southern United States, Central America, and
northern South America. Symptoms consist of
yellow streaks in young leaves followed by yellow-
ing and reddening of leaves, shortening of inter-
nodes, stunting of the whole plant, and sterile
tassels and ears.
Corn stunt is caused by the spiroplasma Spiro­
plasma kunkelii. The spiroplasma invades phloem
cells from where it is acquired by its leafhopper vec-
tors Dalbulus maidis, Dalbulus eliminatus, and other
leafhoppers after feeding on infected plants for sev-
eral days. The vectors transmit the spiroplasma after
an incubation period of 2–3 weeks, during which
the spiroplasma moves and multiplies in the insect.
Citrus Stubborn Disease
It is present and severe in hot and dry areas such as
the Mediterranean countries, the southwestern
United States, Brazil, Australia, and elsewhere. It is
one of the most serious diseases of sweet orange
and grapefruit. It is hard to diagnose but reduces
yield, quality, and marketability of fruit dramati-
cally. Infected trees grow upright but are stunted.
There is less fruit and it is smaller, lopsided, green,
and sour, bitter, and unpleasant.
Citrus stubborn disease is caused by the spiro-
plasma Spiroplasma citri, which is found in the
phloem of affected orange trees. It is transmitted
by budding and grafting and, in nature, by several
leafhoppers such as Circulifer tenellus, Scaphyto­
pius nitrides, and Neoaliturus haemoceps. Role of
insects on fungal diseases of plants.
Insect Transmission of Fungi
As with bacteria, many insects are involved in the
transmission of numerous plant pathogenic fungi
from diseased to healthy plants. Insects are
also involved in plant diseases by breaking the
epidermis and other protective tissues of plants
with their mouthparts or with their ovipositor and
thereby allowing the fungus to enter. Most of the
insect transmissions of fungi are accidental, that is,
they occur because the insects happen to become
externally or internally contaminated with the
fungus or its spores when they visit infected plants
and then carry the spores with them to the plants
or plant parts they visit next. In some cases, insect
transmission of a fungus occurs as the insect visits
blossoms during pollination, in others it occurs
while wounding plants during oviposition, and in
other and most frequent cases, transmission occurs
while wounding the plant during feeding. In rela-
tively few cases, the insect and the fungus it trans-
mits develop a symbiotic relationship in which
each benefit from its association with the other.
Root-Infecting Fungi
It should be pointed out that there are innumerable
cases for which there is circumstantial evidence that
insects are apparently involved in the transmission
of many plant pathogenic fungi and in the develop-
ment of disease by them, but this has not been
proven experimentally. In this category belong, for
example, root infections by fungi such as Pythium,
Fusarium, and Sclerotium, being facilitated by bill-
bugs such as Calendra parvula and Anacentrus
deplanatus, by the Hessian fly Phytophaga destruc­
tor, and by the southern and northern corn root
worms Diabrotica undecimpunctata howardi and
Diabrotica longicornis, respectively. In the black
stain root disease of pines, hemlock, and Douglas fir
is caused by the fungus Leptographium wageneri,
the teliomorph of which is Ophiostoma wageneri,
and is transmitted by the root-feeding bark beetle
Hilastes nigrinus and two root and crown weevils,
Steremnius carinatus and Pissodes fasciatus.
Stalk or Stem-Infecting Fungi
Many fungi infecting stalks or stems, for example
Gibberella, Fusarium, and Diplodia in corn, are

apparently aided by various insects, for example,
the widespread European corn borer, Pyrausta
nubilalis.
Trunk and Branch Canker-Causing Fungi
Many fungi, such as species of Neofabrea, Nectria,
Leucostoma (Cytospora), Ceratocystis, and Lep­
tosphaeria, causing tree cankers, are apparently
also often associated with and assisted by insects
in the initiation and development of the cankers.
The insects involved vary with the particular host
and fungus. For example, the fungus Neofabrea
perennans (Gloeosporium perennans), the cause
of the perennial canker of apple, is transmitted
by  the wooly aphid Eriosoma lanigerum. The
woolly aphids feed on the bark at the base of the
trunk where they cause the formation of galls
within which they multiply. In early spring the
galls burst, the aphids come out and the fungus
attacks the injured tissue and from it advances into
healthy tissue and produces a canker. In the sum-
mer, the apple tree produces callus tissue and seals
off the fungus and the spread of the canker stops.
The aphids, however, grow into the callus tissue
and form a new gall, and the process is repeated.
The spittlebug Aphrophora saratogensis seems
to be involved in the Nectria canker of pines, the
nitidulid beetle Carpophilus freemani and the dros-
ophilid fly Chymomyza procnemoides in the Cera­
tocystis cankers of stone fruit trees, while the tree
cricket Oecanthus niveus and the raspberry midge
Thomasianna theobaldi are involved in the tree
cricket canker of apple and the midge canker of
raspberry, respectively. Many more such insect-
pathogen associations could be mentioned.
In the beech bark canker, caused by the fun-
gus Nectria coccinea var. faginata, the fungus is
transmitted to some extent by the scale insect
Cryptococcus fagi but the main effect of the insect
is in weakening the tree and reducing its defenses
to the fungus. Thus, after beech trees have been
heavily infested by scale insects for about 3–5 years,
the fungus invades and kills the bark and the tree
Transmission of Plant Diseases by Insects
T 3869
forms a canker that may girdle the tree partially or
completely and may kill it.
In the birch constriction disease, the lower
parts of shoots become constricted at the point
where the apical birch woodwasp (Pseudoxiphy­
dria betulae Ensl.) feeds on the shoots. The leaves
above the constriction wither and die but cling to
the twigs past the autumn. Almost all (92%) of the
constrictions are also infected with the anthra-
cnose fungus Melanconium bicolor.
A similar case in which twig canker initiation
and development are facilitated by insects is the
cacao dieback disease in which the fungi Calonec­
tria (Fusarium) rigidiuscula and/or Botryodiplodia
theobromae enter the twigs through wounds cre-
ated by the feeding of the capsid insects Sahlber­
gella singularis and Distantiella theobroma. In
isolated infections the tree defenses take over, iso-
late the fungus, and its further spread stops. In
trees massively infested with the insect, however,
the fungus develops unchecked in the insect-
infested tissues and causes a chronic dieback of
twigs. Control of the insects also halts the invasion
by the fungus and the tree recovers.
In mango malformation disease, presumably
caused by the fungus Fusarium moniliforme, the
fungus is transmitted by the eriophyid mite Aceria
mangifera, while other fungi seem to be carried in
the digestive tract of certain termites.
Sooty Molds
These are black-colored fungi that grow on the
surfaces of mostly leaves of plants, especially in
the tropics and subtropics. Sooty mold fungi do
not penetrate and infect plants but cause disease
by blocking the light from reaching the leaves.
Sooty mold fungi do not parasitize plants but feed
off the honeydew excreted by insects such as
whiteflies, scales, mealybugs, aphids, etc. The sooty
mold fungi are disseminated through their spores
being blown about by wind. However, they are also
spread by the honeydew-producing insects and,
also, by several other types of insects such as flies,
3870
T Transmission of Plant Diseases by Insects
wasps, bees, and ladybug beetles, all of which seek
honeydew as a source of food and in the process
become smeared with fungus spores which they
carry about.
Wood Rots
Rotting of wood is carried out primarily by wood-
rotting basidiomycete fungi. The shelf or conk-
shaped fruiting bodies of many of these fungi are
visited routinely by many types of insects and it is
believed that many of these insects act as vectors of
the wood-rotting fungi. Insects and mites have also
been implicated in the spread of some pine rust dis-
eases, while at least three common scolytid beetles
have been shown to be involved in the transmission
of the scleroderis canker of pine and spruce.
Wood-Stain Diseases
Wood stain or wood discoloration diseases occur
in conifer trees and felled timber. They are caused
by the so-called blue-stain fungi, of which the
most common are species of Ceratocystis and Oph­
iostoma. The blue-stain fungi are associated with
several species of bark beetles, such as Dendrocto­
nus ponderosae, Ips pini, etc., which serve as vec-
tors of the fungi and provide them with wounds
for penetration. On the other hand, the fungi
reduce the water content of the tree and otherwise
improve the microenvironment for the developing
brood of insects. Such a fungus-insect relationship
is described as true mutualistic symbiosis. In other
blue-stain diseases, like the ones caused by the
fungi Trachosporium tingens and T. t. var. mac­
rosporum, the fungi are constantly associated with
their bark-beetle vectors Myelophilus (Blastopha­
gus) minor and Ips acuminatus, respectively, and
are found regularly in the breeding places of the
insects in pine stems. Such fungal-insect associa-
tions are known as symbiotic ambrosia cultures.
In the Southern United States, attacks of
short-leaf pines by beetles like Dendroctonus
f­ rontalis are quickly followed by heavy fungus
infection soon after the beetles tunnel through the
bark and outer wood. Several fungi, including Cer­
atocystis pini, Saccharomyces pini, Dacryomyces sp.
and Monilia sp. can be isolated from the infected
wood and are carried by the same insects both
externally and internally. A similarly complex
association seems to occur in spruce attacked by
Dendroctonus engelmani, followed by the fungi
Leptographium sp., Endoconidiophora sp., or Oph­
iostoma sp. infecting the wood and causing a gray
stain in the sapwood of the infected trees.
Vascular Wilts
Several vascular wilts affect trees and some of them
cause extensive death of trees, because the fungus
responsible for the disease is transmitted from dis-
eased to healthy trees by specific insect vectors. The
spores produced by the causal fungi are sticky and
are produced primarily inside the tree, therefore,
they can be spread by no other means but only by
certain insects closely associated with the disease.
These vascular wilts include (i) persimmon wilt, a
devastating disease caused by the fungus Cepha­
losporium diospyri which enters through all kinds
of wounds but is also transmitted by the powder-
post beetle. Xylobiops basilaris and the twig girdler
beetle Oncider cingulatus, and (ii) mango wilts, one
caused by the fungus Diplodia recifensis and trans-
mitted by the beetle Xyleborus affinis, and another
caused by the fungus Ceratocystis fimbriata and
transmitted by the scolytid beetle Hypocryphalus
mangiferae. The other two vascular wilts are oak
wilt and the Dutch elm disease and will be dis-
cussed in some detail below.
Oak Wilt
It is caused by the fungus Ceratocystis fimbriata
and is one of the most important diseases of forest
trees. The fungus enters the xylem vessels of trees
through fresh wounds to which it is carried by air

or insects, and through natural root grafts. Tree
parts beyond the point of infection wilt, turn
brown and die while newly infected wood shows
dark streaks. The fungus is spread to healthy trees
by nitidulid beetles such as Carpophilus lugubris,
Colopterus niger, Cryptarcha ample, and several
species of Glischrochilus. These fungi breed in the
mycelial mats of the fungus between the bark and
wood and carry the fungus both externally on
their bodies and internally through their digestive
tract. In addition to the nitidulid beetles, several
scolytid beetles, such as Monarthrum fasciatum
and Pseudopityophthorus minutissimus, the bren-
tid beetle Arrhenodes minuta, the buprestid Agril­
lus bilineatus, the flat-headed borer Chrysobothrys
femorata, and others, have been shown to carry the
spores of the fungus, both externally and inter-
nally, when they emerge from the tunnels in dis-
eased trees in which they breed and overwinter
and to carry them to susceptible trees in the spring.
Transmission of the oak wilt fungus by insects not
only spreads the fungus and the disease to new
trees and into new areas, it also increases the abil-
ity of the fungus to produce new variants and new
races more virulent than the existing ones. This is
accomplished by the insects bringing together in
the same tree the compatible self-sterile mating
types which results in the production of perithecia
containing the sexual spores ascospores. The latter
express any new characteristics brought together
during the formation of the spores, some of the
characteristics possibly being increased virulence.
Dutch Elm Disease
It is caused by the fungus Ophiostoma ulmi and
the most recent variant Ophiostoma novo-ulmi,
which is replacing the earlier species. The disease
was first described in the Netherlands in 1921,
found in Ohio and New York in the 1930s, and has
since spread throughout the United States and
much of the rest of the world. It kills elm tree twigs,
branches and whole trees by clogging their xylem
vessels and blocking movement of water from the
Transmission of Plant Diseases by Insects
T 3871
roots to these parts. Dutch elm disease has been
particularly devastating in the United States where
the native elm tree Ulmus americana is extremely
susceptible to the pathogen. The disease has killed
almost all trees in its path, especially elm trees
planted along streets and parks. Elm trees in for-
ests have also been killed but many of them have
escaped infection so far (Fig. 95).
The fungus causing Dutch elm disease is
spread from diseased to healthy trees by the
­European elm bark beetle Scolytus multistriatus
and the native elm bark beetle Hylurgopinus
rufipes, and by natural root grafts. The fungus
overwinters in the bark of dying or dead elm trees
and logs as mycelium and spores. The elm bark
beetles lay their eggs in galleries they make in the
intersurface between bark and wood of weakened
or dead elm trees. If the tree is already infected
with the Dutch elm disease or if the insects carry
with them spores of the fungus, the fungus grows
and produces new spores in the tunnels. After the
eggs hatch, the larvae make tunnels perpendicular
to that made by the adult female and pupate. The
adults emerge, carrying thousands of fungal spores
on their body. The emerging adults prefer to feed
on young twigs of trees and the crotch of small
branches. As the beetles burrow into the bark and
wood for sap, the spores they carry on their body
are deposited in the wounded moist tissues of the
tree. There the spores germinate and grow into the
injured bark and wood and the fungus reaches
the xylem vessels of the tree in which it grows pro-
ducing mycelium and spores. The latter are carried
upward by the sap stream where they can start
new infections. Shoots beyond the infected areas
turn brown, wilt, and die, and as their number
increases the tree shows more browning and more
wilted branches. Eventually large parts of or entire
trees wilt and die, while the fungus continues to
grow and spread in the dead tree. Such trees are
then visited by adult female beetles that lay their
eggs in them and the cycle is repeated.
In Dutch elm disease there is a clear depen-
dency of each organism, the fungus and the insect,
on the other. Probably more than 99% of the elm
3872
T Transmission of Plant Diseases by Insects

Discolored ring of xylem

in infected stem

Emerging adult
beetle carrying
fungus spores Beetle carries
spores to
healthy elm
trees

Mycelium and Cephalosporium-type

spores in xylem vessels of elm
Graphium-type
conidia Beetle carrying Leaves above Mycelium
fungus spores infection and spores
Coremium point wilt in vessels

Ascospores Healthy
released from elm
perithecium Beetles breed
Ascospores in elm logs and
diseased trees
Young beetle
in tunnel
Disease
elm

Perithecium
Coremia Perfect stage seldom found
in nature

Natural root graft

Fungus grows in elm bark

and tunnels
Tunnels of female beetle and
larvae in elm bark Fungus spreads through natural root graft

Transmission of Plant Diseases by Insects, Figure 95  Disease cycle of Dutch elm disease caused by the
fungus Ophiostoma ulmi and transmitted by the European and the American elm bark beetles (from
Agrios 1997).

tree infections are caused by the fungus being car-
ried to the elm trees by the elm bark beetles. On the
other hand, the elm bark beetles depend on the fun-
gus for causing many elm trees to weaken and die,
thereby becoming available as breeding grounds for
the two species of elm bark beetles that transmit the
fungus. The interdependence of the two organisms
has provided the most effective means of managing
the Dutch elm disease by burning or debarking dead
elm trees and logs, thereby denying the insects the
breeding ground they need and, through the reduced
number of insects produced, reducing the number
of elm trees to which they spread the disease.
Foliar Diseases
Many foliar diseases are probably spread by vari-
ous insects visiting and moving about on leaf
­surfaces that are exhibiting infections by spore-
producing fungi. Spores or the spore containers of
many such fungi are sticky or have appendages
that cling to the legs or other body parts of such
insects and are carried by them to other plants or
plant parts they visit next. A few examples of foliar
diseases in which insect transmission of the fungal
pathogen has been shown to occur are described
briefly below.

Powdery Mildews
These are diseases that affect most annual and peren-
nial plants. They are characterized by white superfi-
cial mycelial growth and sporulation by a small
group of fungi that cause symptoms on leaves,
shoots, blossoms and fruit of their host plants. Pow-
dery mildews serve as food for many mycophagous
fungi and produce large numbers of loosely attached
spores. Such spores become attached to, and are dis-
seminated by, insects with which they come in con-
tact. Examples include the feeding of thrips on and
the transmission of spores of the fungi Sphaerotheca
panosa and Uncinula necator that cause powdery
mildew on rose and grape, respectively. Although
these fungi are disseminated readily by wind, it is
likely that transmission is aided by insects.
Rust Diseases
Most rust diseases produce several types of super-
ficial spores on their host plants that, like those of
the powdery mildews, are easily disseminated by
air currents but are also visited, eaten, and trans-
ported by a wide variety of insects. Furthermore,
many rust fungi produce spermatia and receptive
hyphae in the same spermagonium but they are
self-sterile. Many insects, when visiting such sper-
magonia become smeared with sticky spermatia.
When the insects visit successive spermagonia,
they transfer to the receptive hyphae spermatia
from the opposite, compatible type. These sperma-
tia can fertilize the receptive hypha which then
produces dikaryotic mycelium and spores that
contain two nuclei. These dikaryotic spores have
entirely different properties. For example, they can
infect an entirely different host plant from the
plant on which they were produced. The involve-
ment of insects in rust diseases is, therefore,
important in both the dissemination of the spores
to new hosts and, more importantly, in the fertil-
ization of the fungus and, thereby, in increasing
the potential of the fungus to produce more new
and possibly more virulent races.
Transmission of Plant Diseases by Insects
T 3873
Some other examples of foliar diseases in
which insects have been shown to play a role in
their transmission include: red pine needle blight
caused by the fungus Pullularia pullulans and
transmitted and aided in penetration of pine nee-
dles by a cecidomyiid midge; cucurbit anthracnose,
caused by the fungus Colletotrichum lagenarium
and transmitted and aided in penetration by the
spotted cucumber beetle Diabrotica undecimpunc­
tata; oil palm leaf spot, caused by the fungus Pesta­
lotiopsis palmarum and transmitted and aided in
penetration by the oviposition punctures of a
tinged of the genus Gargaphia.
Diseases of Buds and Blossoms
Insects often overwinter in buds of plants and
many also visit blossoms to feed on the nectar
they produce. Buds also often contain mycelium
and spores of plant pathogenic fungi, and blos-
soms are often the first plant organ such fungi
attack in the spring. Examples of bud infections
in which insects have been implicated to play a
role include: bud-blast disease of rhododendron,
caused by the fungus Pycnostyamus azalea and
aided by the leafhopper Graphocephala coccinea;
bud rot disease of carnations caused by the fungus
Fusarium poae and aided by the mite Siteroptes
graminum.
Several diseases of blossoms have been asso-
ciated with insect vectors. In most cases, transmis-
sion of the fungus by the insect is related to the
activities of the insect during pollination. Some of
the better-known examples include:
Anther Smut of Carnations
This is caused by the fungus Ustilago violacea. In
this disease, the pollen is replaced by the telio-
spores of the fungus but the petals remain unaf-
fected and continue to attract insects. The visiting
insects become smeared with the smut spores,
which they transfer to previously healthy flowers.
3874
T Transmission of Plant Diseases by Insects
Blossom Blight of Red Clover
This is caused by the fungus Botrytis anthophila
and is transmitted primarily by pollinating bees.
Ergot of Cereals and Grasses
This is caused by the fungus Claviceps purpurea,
which develops in the flowers and produces spores
that are contained in a sweet and sticky substance.
That substance is attractive to many insects, particu-
larly flies and beetles. The insects feed on the spores
and also become smeared with them externally and
carry them, externally and through their feces, to
healthy flowers. Although primary infections by the
ergot fungus are primarily from ascospores pro-
duced by sclerotia overwintering on the ground
and carried via air currents, insect transmission of
conidia is important for secondary transmission
of  the disease and for transmission over long dis-
tances. Some beetles, however, feed on ergot sclero-
tia on the ground and may carry mycelium and
ascospores on their bodies to healthy plants and
through them may cause primary infections.
Anthracnose Disease of Musa Balsamiana
This is caused by the fungus Gloeosporium
musarum and is transmitted by the hymenopter-
ans Polybia occidentalis, Synoeca surinama, and
Trigona sp. The fungus infects the floral parts of
the plant but these are dropped while still produc-
ing conidia and sweet exudate. The insects are
attracted to the exudate on the fallen flowers and
there they become smeared with conidia, which
they subsequently carry to healthy flowers, which
the spores infect.
Flower Spot of Azalea
This is caused by the fungus Ovulina azaleae and
is transmitted by several species of bees, thrips,
and ants. The insects carry spores on their bodies
and drop them off on healthy flowers they visit
which, in addition, may injure directly and facili-
tate penetration and infection by the fungus.
Diseases of Fruit and Seeds in
the Field
Fruits and seeds are the source of food and the
breeding grounds of many insects. Insects punc-
ture fruit and seeds to obtain food and to lay their
eggs in them. Although insects often cause direct
damage to fruits and seeds that make them unsal-
able, the damage increases manifold when the
insects also carry to the fruits and seeds fungi
that infect and cause these organs to rot or to
develop other symptoms. Numerous examples of
fruit-insect-pathogen interactions could be cited,
although in many cases no hard data of such inter-
actions exist. Some of the better-studied cases are
described briefly below.
Rots of Fleshy Fruits
Fig Rots
Several kinds of fungi attack figs and cause rotting
of fruits in the field. In most such cases, certain
types of insects play a more or less important role
in the transmission and introduction of the fun-
gus into the fig.
Endosepsis of Figs
This is caused by the fungus Fusarium monili­
forme, and results in the entire fruit content turn-
ing into a pulp. The fungus is transmitted from
fruit to fruit by the fig wasp Blastophaga psenes,
which also plays a crucial role in the pollination of
figs. Fig trees, being dioecious, have male trees that
produce staminate flowers around the opening
and gall flowers in the cavity, and female trees that
produce only pistilate flowers. The fig wasp lays its
eggs in the ovules of the gall flowers of male plants,
which are thereby stimulated to grow. The eggs

hatch and the larvae parasitize the galls until they
pupate. The adults emerge from the pupae and the
females are fertilized while still in the male fig.
When they come out of the fig, the females brush
against the staminate flowers that surround the
opening and become smeared with pollen. The
female wasps carry the pollen to male and female
flowers they subsequently visit for oviposition. In
female flowers, however, because of the length of
styles, oviposition fails but pollination is neverthe-
less successful and the fruit develop into edible
figs. If, however, as the female wasp visits some
infected figs it becomes smeared with spores of
the fungus, it transmits the spores to male and
female figs it visits, and the fungus then causes
endosepsis of the female figs.
Souring of Figs
This is caused by yeast fungi that cause fermenta-
tion, and appears as discoloration and wateriness
of the fig contents which then exude from the fig
opening. Such figs shrivel, dry, and cling to the
tree. The fermenting yeasts are transmitted to figs
externally and internally on the bodies of the two
most common visitors of figs still in the tree, the
sap beetle Carpophilus hemipterus and the fruit fly
Drosophila melanogaster.
Fig Smuts and Molds
These are caused by the black mycelium and spores
of Aspergillus niger and the variously colored
growths of other fungi. These fungi are carried
into green figs on the bodies of predatory mites
and, to a lesser extent, by thrips.
Brown Rot of Stone and Pome Fruits
This is caused by the three related fungi Monilinia
fructicola, M. fructigena, and M. laxa and affects all
the stone fruits and, to a lesser extent, the pome
fruits. The fungi are aided in their penetration of
the fruit by the feeding and oviposition wounds
made by the insects plum curculio (Conotrachelus
nenuphar) and the oriental fruit moth (Grapholitha
Transmission of Plant Diseases by Insects
T 3875
molesta), and the feeding wounds of the dried fruit
beetle (Carpophilus hemipterus) and two nitidulid
beetles (Carpophilus mutilatus and Haptonchus
luteolus). The insects also become smeared with
spores of the brown rot fungi which they carry on
their bodies and deposit at the wounds they make
on the fruits they visit. In pome fruits, the fungus is
facilitated in penetrating the fruit by the feeding
holes made by the earwig Forficula auricularia at
the beginning of ripening of the fruit, at which
time they are susceptible to brown rot.
Gray Mold of Grapes
This is caused by the fungus Botrytis cinerea. The
fungus spores are generally spread by air currents.
Penetration of the grapes and shoots, however,
seem to be increased by the wounds made on them
by the larvae of the lepidopterans Argyrotaenia
pulchellana and Lobesia botrana.
Black Pod of Cacao
This is caused by the fungus Phytophthora palm­
ivora and results in devastating losses of yield.
Insects of several different families play a role in
the transmission of this disease. At least 10 species
of ants, especially Crematogaster striatula and to
a lesser extent Camponotus acvapimensis and
Pheidole megacephala, appear to spread the fungus
vertically within the tree, especially during the
rainy season, when they carry spore-containing
soil particles up the cacao tree for nesting pur-
poses. Certain coleoptera, such as the nitidulid
beetle Brachypeplus pilosellus, and certain dipter-
ans, such as the fly Chaetonarius latifemur, colo-
nize black pods in the field and may carry the
fungus internally or externally on their bodies to
healthy pods. Because of their large numbers on
cocoa trees, their habit of visiting wounded pods,
and their proven efficiency to transmit the fungus,
these insects are considered the main vectors of
the fungus locally and over long distance.
3876
T Transmission of Plant Diseases by Insects
Boll Rots of Cotton
These are caused by several fungi including Fusarium
moniliforme, Alternaria tenuis, Aspergillus flavus, and
Rhizopus nigricans. Various insects are apparently
involved in the transmission of these fungi and they
seem to use different mechanisms of transmission.
Thus, in boll rot due to Fusarium and Alternaria, the
fungi penetrate cotton bolls through feeding and ovi-
position wounds made by the boll weevil (Anthono­
mus grandis), the cotton bollworm (Heliothis zeae),
and the tarnished plant bug, Lygus lineolaris, or they
are brought to and penetrate through the nectarines
by nectar feeding flies such as Drosophila and cab-
bage looper, Trichoplusia ni. In boll rots caused by
Aspergillus flavus and other aflatoxin-producing spe-
cies, the fungus is primarily wind disseminated but is
also carried internally and externally by insects, such
as the lygus bug Lygus hesperus and the stink bug
Chlorochroa sayi, that frequently visit cotton bolls.
The latter fungus, however, seems to depend for
entrance on the presence of large wounds like the
large exit holes made by the mature larvae of the pink
bollworm, Pectinophora gossypiella. On the other
hand, boll rots by Rhizopus stolonifer occur when
wounds made by the bollworm Earias insulana and
by the pink bollworm are available. In the lint rot of
cotton, caused by the fungus Nigrospora oryzae, the
fungus is transmitted very efficiently by the mite Sit­
eroptes reniformis. In Stigmatomycosis or internal
boll disease, caused by the fungus Nematospora gos­
sypol, the cotton fibers are stained in the absence of
external symptoms. This disease is associated with
the feeding of several species of plant bugs primarily
of the genus Dysdercus, often referred to as cotton
stainers. The insects carry the fungus spores exter-
nally on the mouthparts and internally in their deep
stylet pouches and introduce it via their proboscis
through the wall of young cotton bolls.
Coffee Bean Rot
This is caused by the related fungi Nematospora
corylii and N. gossypii, which cause berries to turn
black and subsequently to rot. The fungi are intro-
duced into the berries through the feeding wounds
made by the insects Antestia lineaticolis and A. fac­
eta. The insects feed on small and large berries and
if they carry the fungus the latter causes infection
of the bean. The number of infected berries is pro-
portional to the number of insects, approximately
300 insects per tree resulting in infection of all the
berries on the tree.
Molds and Decays of Grains and
Legumes
Numerous decays and molds affect the various
grains and legumes while still in the field and their
frequency and severity increase as the number of
insects infesting the crops, and feeding on the
seeds, increases. In corn, for example, seed rots can
be caused by species of the fungi Fusarium, Gib­
berella, Diplodia, Cephalosporium, Nigrospora,
Physalospora, Cladosporium, Penicillium, Aspergil­
lus, Rhizopus, Trichoderma, and others. The insects
most commonly involved in transmitting and
facilitating infection of corn kernels by these fungi
are the corn earworm, Heliothis zea, and the Euro-
pean corn borer, Pyrausta nubilalis, but other bor-
ers and other insects also play important roles as
vectors and, most importantly, as facilitators of
infection by these fungi by creating wounds that
allow the fungus to enter the seed. In seed infec-
tions by Aspergillus and by Fusarium there is the
added adverse effect of production of debilitating
mycotoxins. Similar, although less studied situa-
tions have been reported for rice infections by
fungi, e.g., Nematospora corylii, transmitted and
facilitated by wounds made by the rice stinkbug
Oebalus pugnax; wheat and corn infections by
Nigrospora sp. and Fusarium poae, transmitted by
large numbers of Peliculopsis mites feeding on and
transporting spores of the fungus in their abdomi-
nal sacs; and in various legume infections by the
fungi Nematospora, Cladosporium, Aureobasidium,
etc., transmitted and facilitated in their penetra-
tion and infection of the seeds by the stinkbugs

Acrosternum hilare and Thyanta custator, the
lygaeid Spilostethus pandurus, by thrips, aphids,
and other insects.
Molds and Decays of Harvested
Fruits and Seeds
Generally little is known definitively about the
roles of specific insects on the transmission and
facilitation of rots of specific fruits and vegetables,
and of molds and decays of seeds of specific grains,
legumes, or nuts by specific fungi. It is generally
accepted, however, that postharvest infections of
plant products are greatly increased in numbers
and in severity if insects are also present in the
same or adjacent containers. There is agreement
that insects moving about among stored fruits,
seeds, etc., transport externally and internally on
their bodies spores of fungi infecting such fruits
and seeds and deposit such spores on the next fruit
or seed they feed on. There is also agreement that
by creating feeding or oviposition wounds on har-
vested fruit and seeds, the insects create openings
through which the fungi can penetrate and release
sap and additional nutrients. The fungi then can
grow and build momentum to eventually infect
and rot the entire fruit or seed.
The fungi that cause most rots of fleshy fruits
and vegetable after harvest include Penicillium,
Fusarium, Botrytis, Rhizopus, Alternaria, Sclero­
tinia, Monilinia, and Colletotrichum, while the
molds and decays of grains and legumes involve
primarily Aspergillus, Fusarium, and Penicillium.
The insects involved in transmission and facilita-
tion of infection of fleshy organs after harvest
include larvae and adults of various Lepidoptera
such as the oriental fruit moth, Grapholitha
molesta, Diptera such as the apple maggot,
Rhagoletis pomonella, the Mediterranean fruit fly,
Ceratitis capitata, the house fly, and others. The
insects involved in the transmission and facilita-
tion of infection by fungi causing molds and
decays of grains and legumes are the larvae
and adults of various Coleoptera such as the rice
Transmission of Plant Diseases by Insects
T 3877
weevil Sitophilus oryzae, the granary weevil Sito­
philus granarius, and the confused grain beetle,
Tribolium confusum, and also Lepidoptera such as
the Angoumois grain moth, Sitotroga cerealella,
the European corn borer, Pyrausta nubilalis, the
ear cornworm, Heliothis zea, and other insects.
Insect Transmission of Plant
Pathogenic Nematodes
Two very serious plant diseases caused by nema-
todes of the genus Bursaphelenchus are transmit-
ted by insects. In both diseases there is a symbiotic
relationship between the fungal pathogen and the
insect vector.
Pine Wilt
This is a lethal disease of many species of pines
and other conifers. It is caused by the nematode
Bursaphelenchus xylophilus, known as the pin-
ewood nematode. The nematode is about 800 µm
long by 22  µm in diameter and it develops and
multiplies rapidly, each female laying about 80
eggs and completing a life cycle in as short as
4 days. The nematode produces the four juvenile
stages and the adults. The juvenile stages develop
in the resin canals of infected pine trees, feeding at
first on plant cells and later on fungi that invade
the dying or dead tree. Later, the nematode pro-
duces special fourth-stage dispersal juveniles that
are adapted to survive in the respiratory system of
the cerambycid beetles Monochamus carolinensis
and M. alternatus by which they are transmitted to
healthy pine trees.
The pinewood nematode overwinters in the
wood of infected dead trees, which also contain
larvae of the beetle vectors of the nematode. Early
in the spring, the larvae dig small cavities in the
wood in which they pupate. As the adult beetles
emerge from the pupae later in the spring, large
numbers of fourth-stage juvenile nematodes
enter the beetles and almost fill the tracheae of the
3878
T Transmission of Plant Diseases by Insects
respiratory system of each insect with about
15,000–20,000 juveniles. These nematode-carrying
adult beetles emerge and fly to young branch tips
of healthy pine trees where they feed for several
weeks. As the beetles strip the bark and reach the
cambium, the nematode juveniles emerge from
the insect and enter the pine tree through the
wound. The juveniles in the tree then undergo the
final molt and produce adult nematodes. The latter
migrate to the resin canals, feed on their cells and
cause their death, and then they move in the xylem
and in the cortex where thy reproduce quickly and
build enormous populations of nematodes and
kill twigs, branches and entire trees.
After the adult Monochamus beetles, the vec-
tor of the pine wilt nematode, have fed on young
twigs for about a month, they are ready to breed
and look for stressed and dead pine trees, includ-
ing trees showing symptoms or dying from infec-
tion by the pinewood nematode. The female beetles
deposit their eggs under the bark of such trees
where the first two instars develop and feed. The
third instar penetrates the wood where it under-
goes the next molt and produces the fourth instar,
which overwinters there. In early spring, the fourth
instar digs a cavity in the wood where it pupates
and to which numerous third-stage nematode
juveniles are attracted and congregate. The juve-
nile nematodes undergo the next molt and pro-
duce the fourth-stage dispersal juveniles, which by
the thousands infect the tracheae of the adult
insects as soon as they emerge from the pupae and
are carried by them to healthy pine trees, thus
completing the cycle.
Red Ring of Coconut Palms
This disease kills coconut palm trees from Mexico
to Brazil and in the Caribbean islands. It is caused
by the nematode Bursaphelenchus cocophilus,
which is transmitted from palm to palm by the
American palm weevil, Rhynchophorus palmarum,
the sugarcane weevil, Metamasius sp., and proba-
bly other weevils. The nematodes infect, ­discolor,
and kill the palm tissues in a ring 3–5  cm wide
about 5  cm inside the stem periphery over the
length of the stem.
The nematode pathogen lays its eggs and pro-
duces all its juvenile stages and the adults inside
infected palm trees, completing a life cycle in about
9–10 days. Female weevil vectors are attracted to
red ring-diseased trees but they also lay eggs on
healthy or wounded palm trees. If the female car-
ries red ring nematodes, it deposits them in its
feeding wounds at bases of leaves or at internodes.
The nematodes then enter the palm tissues and
undergo repeated life cycles and spread intercel-
lularly in the parenchyma cells of the petioles,
stem, and roots, where the cells break down and
form a flaky, orange to red discolored tissue with
cavities. Red ring nematodes do not invade xylem
and phloem tissues but cause tyloses to develop in
xylem vessels within the red ring that block the
upward movement of water and nutrients. In the
meantime, the weevil larvae of the insect vector
feed on the red ring tissue and swallow several
hundred thousand nematode third-stage juveniles.
Of these, however, only a few hundred of the nem-
atodes survive and pass through the molt, inter-
nally or externally, to the next stage weevil larvae
and to the adult weevil. As weevil females emerge
from rotted palms, a small percentage of them
carry with them third-stage juveniles of the nema-
todes. Nematode populations increase rapidly at
first but later they decline and about 3–5 months
after infection there are hardly any red ring nema-
todes or their eggs left in decomposed stem tissue
of infected, dead palm trees. The nematodes, how-
ever, survive in newly infected palm trees and,
briefly, in their insect vector.
Insect Transmission of Plant
Pathogenic Protozoa
Three plant diseases: phloem necrosis of coffee,
heartrot of coconut palms, and sudden wilt of oil
palms, are caused by flagellate protozoa of the
genus Phytomonas. In all three diseases, protozoa

invade the phloem elements of infected plants and
multiply in them, reaching populations of varying
densities. Some of the sieve tubes become plugged
by protozoa. Generally, the more severe the symp-
toms of infected plants, the higher the populations
of protozoa in their phloem. The pathogen is
transmitted from infected to healthy plants occa-
sionally through natural root grafts, and primarily
by stink bugs (Pentatomidae) such as the genera
Lincus and Oclenus, and possibly others.
Insect Transmission of Plant
Pathogenic Viruses
Plant viruses cause many and severe diseases of
plants, their number and importance being second
only to fungal diseases of plants. Most viruses infect
their host plants systemically, that is, the virus mul-
tiplies internally throughout the plant. Almost all
viruses enter and multiply in phloem and in paren-
chyma cells. Viruses do not produce spores, nor do
they come to the surface of the plant. All plant
viruses are transmitted to new plants that are prop-
agated from infected plants vegetatively (that is, by
grafting or budding, by cuttings, by bulbs, corms,
roots, tubers, etc.), and many can be transmitted
artificially by mechanical inoculation, that is, by
rubbing sap from infected plants onto leaves of
healthy plants. Some plant viruses can be transmit-
ted from diseased to healthy plants by pollen or
seed produced by infected plants, some by the par-
asitic higher plant dodder when it is infecting both
virus-infected and healthy plants, and some plant
viruses are transmitted from plant to plant by cer-
tain plant pathogenic fungi, nematodes, or certain
mites. More than half of the plant viruses, number-
ing more than 400, are transmitted from diseased
to healthy plants by insects.
The number of insect groups that are vectors
of plant viruses is relatively small. The most
­important vector groups, with the number of vec-
tor ­species and viruses transmitted, are listed
below. Hemiptera, which includes the aphids
(Aphididae, 192 species, 275 viruses), leafhoppers
Transmission of Plant Diseases by Insects
T 3879
(Cicadellidae, 49 species, 31 viruses), the planthop-
pers (Fulgoroidea, 28 species, 24 viruses), the
whiteflies (Aleurodidae, 3 species, 43 viruses), the
mealybugs (Pseudococcidae, 19 species, 10
viruses), and some treehoppers (Membracidae, 1
species, 1 virus), contain by far the largest number
and the most important insect vectors of plant
viruses, but the true bugs (Hemiptera, 4 species),
the thrips (Thysanoptera, 10 species, 11 viruses)
and the beetles (Coleoptera, 60 species, 42 viruses)
also are implicated. Grasshoppers (Orthoptera, 27
species) seem to occasionally carry and transmit a
few viruses. Unquestionably, the most important
virus vectors are the aphids, leafhoppers, white-
flies, and thrips. These and the other groups of
Hemiptera have piercing and sucking mouth-
parts, although several thrips have rasping, suck-
ing ones. Beetles and grasshoppers have chewing
mouthparts, but many beetles are quite effective
vectors of certain viruses. Generally, viruses
transmitted by one type of vector are not trans-
mitted by any other type of vector.
Aphids and Aphid-Transmitted
Viruses
Aphids have evolved as the most successful exploit-
ers of plants as a food source, particularly in the
temperate regions. Many species of aphids alter-
nate between a primary and a secondary host,
although there are many variations of aphid life
cycles depending on the aphid species and on cli-
mate. Some aphids overwinter as parthenogenetic
viviparous forms while others go through their life
cycle on one host species or on several related spe-
cies. On the other hand, there are several aphid
species, such as Myzus persicae, that have as many
as 50 primary and alternate species of host plants.
Aphids have mouthparts that consist of two
pairs of flexible stylets held within a groove of the
labium. During feeding, the stylets are extended
from the labium and, through a drop of gelling
saliva, the stylets rapidly penetrate the epidermis.
Penetration may stop at the epidermis or it may
3880
T Transmission of Plant Diseases by Insects
continue into the middle layers of leaf cells with a
sheath of saliva forming around the stylets. The
stylets move between the cells until they reach and
enter a phloem sieve tube from which the aphids
obtain their food. Individual aphids vary in their
ability to transmit the virus to individual plants.
Infection of a plant with a virus often makes the
plant more attractive for aphids to grow on and to
reproduce. Both acquisition and transmission of
virus by aphids are affected by temperature,
humidity and light.
Virus–Vector Relationships
Insect vectors that have sucking mouthparts carry
plant viruses on their stylets, and such viruses are
known as stylet-borne, externally borne, or non-
circulative, because they do not pass to the vector’s
interior. The remaining viruses are taken up inter-
nally within the vector and are called internally
borne persistent circulative or persistent propaga-
tive viruses.
Stylet-Borne Non-Persistent
Transmission
Most externally borne viruses can be transmitted
in the typical stylet-borne non-persistent manner.
In such a transmission the virus is assisted in its
transmission by a specific configuration of its coat
protein or by a non-structural virus-encoded pro-
tein. The insect acquires the virus from the plant
by feeding on it for only seconds or, at most, min-
utes. The insect can transmit the virus immediately
after the acquisition feeding, that is, without any
incubation period required for transmission. The
insect retains the virus and is usually able to trans-
mit it for only a few minutes after it acquired it.
Most of the nearly 300 known aphid-borne plant
viruses are stylet-borne non-persistent. Some of
the most important groups of plant viruses, such
as those in the genera Potyvirus, Cucumovirus,
Alfamovirus, and the Caulimovirus transmitted by
Myzus persicae are stylet-borne non-persistent
viruses. In the few seconds in which aphids acquire
the virus, the aphid stylet usually penetrates only
the epidermal cell. Actually, deeper penetration of
the stylet into leaf tissues reduces the ability of
aphids to transmit the virus. Aphids vary greatly in
their ability to transmit viruses, each particular
virus being transmitted by one or a few species of
aphids. Sometimes, certain virus strains are trans-
mitted by distinct aphid species. Also, even indi-
vidual aphids in a population vary in their ability
to transmit the same virus, some of them being
incapable of transmitting the virus.
All non-persistently transmitted viruses have
simple structures of elongated or isometric parti-
cles with the nucleic acid encapsidated by one or
more kinds of coat proteins. In some viruses, the
coat protein interacts directly with the binding site
of virus retention in the aphid. In other viruses,
the virus encodes a non-structural protein which
interacts with the aphid-virus retention binding
site and forms a bridge between the virus and
the aphid stylet. However viruses are bound to the
aphid stylet, there must also be a mechanism for
release of the virus when the aphid feeds on the
next plant. It appears that saliva alone may carry
out this function.
Semi-Persistent Viruses
Some externally borne non-persistent viruses are
known as semi-persistent because they reach but
do not seem to go past the foregut of the vector;
the vector must feed on an infected plant (acquisi-
tion period) for several minutes or hours before it
can transmit the virus; and the vector can then
retain (retention time) and transmit the virus to
healthy plants for several hours. Semi-persistent
viruses are also assisted in their transmission by a
transmission helper protein or coat protein con-
figuration. The best known semi-persistent viruses
are caulimoviruses, which occur in most cell types,
and the closteroviruses beet yellows virus and
curly top virus, which are found primarily in

phloem cells. In several of the semi-persistent
viruses, a helper component seems to be involved
in their transmission. In cauliflower mosaic virus,
the helper component consists of two non-capsid
proteins, one of which is associated with the virus
particles and the other has two binding domains
that interact strongly with microtubules. In some
cases, certain viruses can be transmitted only in
the presence of a second virus which acts as the
helper virus.
Persistent Viruses
Internally borne viruses are either persistent
circulative or persistent propagative. Persistent
circulative viruses are acquired from the plant
by the vector after an acquisition feeding period
of several hours to several days, and then they
are retained by the insect vector and can be
transmitted by it for several days or weeks. Per-
sistent circulative viruses require a latent period
of several hours to several days beyond the
acquisition time before they can be transmitted
by the insect vector, they reach the hemolymph
of the vector, and pass through the various
stages of the insect, but not through the ovaries
to the egg. Persistent propagative viruses are
acquired by the insect after a feeding period of
several hours to several days, are retained by the
vector for several weeks to several months, they
multiply in the vector, they have a latent period
of a few to several weeks, and can pass through
the various stages of the insect, including trans-
ovarial passage to the egg. Persistent viruses are
generally transmitted by one or a few species of
aphids and cause symptoms characterized by
leaf yellowing and leaf rolling.
Persistent Circulative Viruses
These include primarily the luteoviruses, such as
barley yellow dwarf virus, and the nanoviruses,
such as banana bunchy top virus. The luteoviruses
Transmission of Plant Diseases by Insects
T 3881
are acquired after a feeding period as short as
5 min but it usually takes 12 h. After an incubation
period of an additional 12 h, the vector can trans-
mit the virus within a 10–30 min inoculation feed-
ing and can continue transmitting it for several
days or a few weeks. In the vector, the virus parti-
cles seem to associate only with the hind gut of the
aphid, entering its cells by endocytosis into coated
pits and vesicles and accumulating in tubular ves-
icles and lysosomes. Virus particles are then
released into the hemolymph by fusion of the ves-
icles with the plasmodesmata and enter the sali-
vary glands of the aphid via invaginations with
two plasma membranes on the hemocoel side of
the salivary gland accessory cells. It appears that
persistent circulative viruses do not require a non-
capsid protein for helper component but they
require a protein produced via a read-through of
the coat protein stop code if they are to advance
beyond the hemocoel. Some persistent circulative
viruses also require a helper virus to be present for
them to be transmitted by their aphid vector.
Persistent Propagative Viruses
Propagative viruses are transmitted primarily by
leafhoppers and planthoppers but several mem-
bers of the Rhabdoviridae multiply in and are
transmitted by their aphid vector. These bacilli-
form viruses replicate in the nucleus and the cyto-
plasm of cells in the brain, salivary glands, ovaries,
and muscle of the insect vector. The virus goes
through the egg to about 1% of the nymphs. Infec-
tion of aphids with rhabdoviruses results in
increased mortality of the aphids.
Leafhoppers and Planthoppers,
and Transmission of Plant Viruses
Leafhoppers lay eggs that hatch to nymphs which
pass through several molts before becoming adults.
Some of them overwinter as eggs, some as adults,
and some as immature forms. They all feed by
3882
T Transmission of Plant Diseases by Insects
sucking sap from phloem elements of plants. Their
feeding behavior is similar to that of aphids in that
the mouthparts, surrounded by the salivary sheath,
penetrate the phloem of host plants.
Virus–Vector Relationships
All hopper-transmitted viruses are persistent
circulative or persistent propagative, and are
transmitted by only one or by a few closely
related species of the hopper vectors. Only two
of the 60 sub-families of leafhoppers (Cicadelli-
dae) contain species that are vectors of viruses:
the Agalliinae feed on herbaceous dicotyledon-
ous hosts and the Deltocephalinae that feed on
monocots. Of the 20 planthopper families (Ful-
goroidea), only one, the Delphacidae, have spe-
cies that are vectors of viruses all of which infect
monocotyledonous plants and many of them
cause severe diseases on cereal crops such as rice,
wheat, and corn.
Semi-Persistent Transmission
Two viruses, maize chlorotic dwarf virus (MCDV)
and rice tungro spherical virus (RTSV), are
acquired by their vectors (Graminella nigrifrons
and Nephotettix virescens, respectively) from their
hosts within about 15  min and are retained by
their vectors for one to a few days. MCDV parti-
cles have been seen in the foregut and a few other
tissues but not beyond. Hoppers egest material
from the foregut once in a while during feeding
and it is thought that transmission occurs during
this ingestion-egestion process.
Persistent Transmission
This involves the internal movement of the virus
obtained from the plant to the salivary glands of
the insect vector. Some of these viruses are circula-
tive while others are propagative.
Circulative Viruses
Only two genera of geminiviruses (Mastrevirus
and Curtovirus) are transmitted by leafhoppers in
the persistent circular manner. The viruses are
acquired by the vector after feeding for a few sec-
onds to an hour. There is a latent period of about a
day, presumably for the virus to reach the salivary
glands. The internal movement of these viruses
is determined by the viral coat protein and by
­receptor-mediated endocytosis.
Propagative Viruses
There are four families and genera of plant viruses
that replicate within the cells of their insect vec-
tors as well as the cells of their host plants. Two of
these families, Rhabdoviridae and Reoviridae,
contain viruses that infect animals, and their
virus members that infect plants have been con-
sidered as animal viruses that infect plants. The
propagative viruses have a latent period of about
2  weeks. During this period the virus replicates
and invades most tissues of the insect vector.
When the virus reaches the salivary glands of the
vector, the latter can transmit the virus to new
plants and can continue to transmit it for the rest
of their life. Only a small percentage of the hop-
pers feeding on infected plants become vectors
and of these only about 1% pass the virus through
their eggs to the next generation. Various capsid
proteins seem to be necessary for passage of
viruses through the organs of the vector and are
required for transmission.
The two genera that have propagative viruses
are Tenuivirus, members of which are transmitted
by delphacid planthoppers, and Marafivirus,
which is vectored by the leafhopper Dalbulus
maydis. These viruses have an acquisition feeding
period of 15  min to 4  h, a latent period of
4–31  days, inoculation periods as short as 30  s,
and can transmit the virus for as long as they live.
Almost all of these viruses are transmitted transo-
varially to the egg.

Whitefly Transmission of Plant
Viruses
Whiteflies transmit the viruses in the genus Bego­
movirus of the family Geminiviridae, and all the
viruses in the genus Crinivirus and some in the
genus Closterovirus of the family Closteroviridae.
Whitefly adults are winged but only the first instar
among the larvae is mobile. Whiteflies produce
many generations in a year and reach high popula-
tions. Only a few species of whiteflies transmit
viruses, mostly in the tropics and subtropics, but the
viruses they transmit cause very severe diseases.
Begomoviruses are transmitted by Bemisia tabaci
whiteflies, while the criniviruses and the whitefly-
transmitted closteroviruses are vectored by the
whiteflies Trialeuroides vaporariorum, T. abutilonea,
B. tabaci, and the type B of B. tabaci (also referred to
as B. argentifolii). Whitefly mouthparts and feeding
behavior resemble those of aphids.
Begomoviruses are bipartite geminiviruses
and are transmitted by whiteflies in the persistent
circulative manner. A helper factor coded by the
virus seems to be involved in the transmission. The
whitefly-transmitted monopartite closteroviruses
and the bipartite criniviruses reach only the foregut
of the vector and are transmitted in the semi-
persistent manner. These viruses are retained in
the vector for about 3–9 days. Two capsid proteins
help the virus in its transmission by the vector.
Thrips Transmission of Plant
Viruses
About 10 species of thrips of the family Thripidae
are the vectors of about a dozen viruses belonging
to four genera (Carmovirus, Ilarvirus, Sobemovirus,
and Tospovirus) of four families. Thrips are polypha-
gous insects that have many hosts. Some of the vec-
tor species reproduce mainly parthenogenetically.
The larvae are rather inactive but the adults have
wings and are very active. Thrips adults feed by
sucking the contents of subepidermal cells. Adults
live up to 3 weeks and there may be as many as 20
Transmission of Plant Diseases by Insects
T 3883
generations per year. The tospoviruses are transmit-
ted in the persistent propagative manner, while the
viruses of the other genera are transmitted in the
pollen carried by the thrips vectors and by mechan-
ical damage during feeding of the vector.
By far the most important thrips-transmitted
viruses are the tospoviruses, which include the
widespread and severe tomato spotted wilt virus
and the impatience necrotic spot virus. In tospo-
viruses, only the larvae but not the adults can
acquire the virus, and their ability to acquire it
decreases with age. Larvae sometimes acquire the
virus after feeding on a diseased plant for as little
as 5  min, but usually they must feed for more
than an hour both in acquiring and in inoculat-
ing the virus. There is a latent period of 3–4 days
before the larvae can transmit the virus. The virus
is passed from the larvae to the adults which can
transmit it, although erratically, for as long as
they live. These viruses appear to multiply in the
vector but are not passed through the egg. Sev-
eral structural proteins of the virus seam to be
associated with the acquisition, passage through,
and inoculation of the virus by its larval and
adult insect vector.
Mealybug and Other Bug
Transmission of Plant Viruses
Mealybugs are important as virus vectors primar-
ily on some perennial plants in the tropics and sub-
tropics. They move slowly on plants and therefore
are not as efficient virus vectors as those discussed
previously. They move from plant to plant, mostly
as crawling nymphs, through leaves of adjacent
plants being in contact with each other; by ants
tending the mealybugs and moving them from one
plant to the other; and occasionally by wind.
Mealybugs feed on the phloem and they are
vectors of the badnaviruses, such as the cacao
swollen shoot virus (CSSV), several closterovi-
ruses, such as grapevine leafroll associated viruses
and the pineapple mealybug wilt associated
virus, and the trichoviruses, such as grape viruses
3884
T Transmission of Plant Diseases by Insects
A and B. Mealybugs acquire the viruses after feed-
ing on diseased plants for only a few, about 20 min
and retain the virus for a few, up to 24  h, so the
transmission resembles the non-persistent or semi-
persistent mechanism of transmission by aphids.
Other bugs that transmit plant viruses include
the mirid bugs, which transmit some sobemo­
viruses in manners that have characteristics of
­non-persistent, semi-persistent, and beetle-like
transmission, and the piesmatid bugs, which
­transmit beet leaf curl virus in a persistent propa-
gative manner.
Virus Transmission by Insects That
Have Biting/Chewing Mouthparts
Although there are a few vectors in the orders
Orthoptera and Dermaptera, there are more than
60 vector species in the order Coleoptera (beetles),
30 of them in the family Chrysomelidae. Most bee-
tle vectors tend to eat plant cells between the leaf
veins and regurgitate during feeding, thereby bath-
ing their mouthparts with sap and virus. Virus
transmission by beetles, however, is specific between
each virus and its vector. Beetle-transmitted viruses
belong to the genera Tymovirus, Comovirus, Bro­
movirus, and Sobemovirus. Most of these viruses
are small (25–30  nm in diameter), stable, reach
high concentrations, and are easily transmitted by
sap. These viruses can also be translocated through
the xylem of the plant. Beetles can acquire and can
transmit the virus after feeding for a few seconds
and they can retain the virus from 1 to 10 days.
Virus Transmission by Mites
Several members of the mite family Eriophyidae
transmit viruses of the genus Rymovirus which
cause many serious diseases in grain crops. Two
mite species of the family Tetranychidae transmit
two plant viruses, one of them transmitting the
peach mosaic virus. All mites in these families feed
by piercing plant cells and sucking their contents.
Eriophyid mites are small (0.2  mm long),
move little by themselves and, instead, they are
spread by wind. They have two nymphal instars
followed by a resting pseudopupa. They complete
a life cycle within 2 weeks. Mites can acquire virus
from infected host plants within 15 min from the
start of feeding and can transmit it to healthy plant
within a similar duration. Mites acquire the virus
as nymphs but not as adults. They carry the virus
through molts and remain infective for 6–9 days.
Tetranychid mites are larger (0.8  mm long).
Pre-adult mites readily acquire the virus and they,
as well as the adults, transmit the virus efficiently.
Virus Transmission by Pollinating
Insects
Honey bees and other pollinating insects seem to
play a role in distributing virus-infected pollen from
infected plants to healthy ones. It appears, however,
that no special mechanisms or involvement of the
insect are present in such virus transmission.
Summary
Insects play various roles in the transmission of
plant pathogens, and in the initiation and develop-
ment of disease in plants. In some diseases, the
insects incidentally carry pathogens on their bod-
ies or in their feces and deposit them on healthy
plants where they cause disease, without develop-
ing any special relationships with the pathogens. In
several cases, the insects weaken the plants on
which they feed and make them much more sus-
ceptible to attack by pathogens. In other cases, the
pathogens depend on the insects to carry them to
healthy plants and to deposit them on fresh wounds
through which they penetrate and infect the plants.
While pathogens seem to be the beneficiaries of
these actions, insects also derive advantages by the
pathogen making the diseased plant more attrac-
tive to the insect for feeding or breeding purposes,
and in some cases, by the insect feeding on the
 Transmission of Xylella fastidiosa Bacteria by Xylem-Feeding Insects
pathogen growing in the cavities made by its insect
vector. Also, while in most cases the pathogen does
not affect its insect vector directly, there are several
plant viruses and mollicutes that multiply in the
insect vector as well as in their plant host, and such
vector insects often show histopathological symp-
toms, reduced reproduction, and shorter life span.
Most of the insect/pathogen associations are highly
specific and involve sophisticated molecular mech-
anisms that regulate the uptake, retention, and
transmission of the pathogen by its insect vector.
 Plant Viruses and Insects
 Management of Insect-Vectored Pathogens of
Plants
 Transmission of Xylella fastidiosa Bateria by
Xylem-Feeding Insects
 Vectors of Phytoplasmas  of grape, phony disease of peach, and citrus varie-
References
Agrios GN (1997) Plant pathology, 4th edn. Academic,
San Diego
Anonymous. Compendium of Diseases of…A series of books
on diseases of individual crops published periodically
by APS, St. Paul, MN
Capinera JL (2001) Handbook of vegetable pests. Academic,
San Diego
Hull R (2001) Matthews’ plant virology, 4th edn. Academic,
San Diego
Harris KF, Maramorosch K (1980) Vectors of plant pathogens.
Academic, San Diego
Hiruki C (ed) (1988) Tree mycoplasmas and mycoplasma dis-
eases. University of Alberta Press, Edmonton
Nault LR (1997) Arthropod transmission of plant viruses: a
new synthesis. Ann Entomol Soc Am 90:521–541
Schowalter TD, Filip GM (eds) (1993) Beetle-pathogen inter-
actions in conifer forests. Academic, San Diego
Transmission of Xylella fastidiosa
Bacteria by Xylem-Feeding
Insects
Alexander H. Purcell
University of California, Berkeley, CA, USA
Insects that feed predominantly on the sap of
plants’ water-conducting systems (xylem) can
T 3885
transmit bacteria that are specific parasites of the
plant xylem. Most xylem sap-feeders are spittle-
bugs (families Cercopidae and Machaerotidae) or
sharpshooters (subfamily Cicadellinae) belonging
to the leafhopper family (Cicadellidae) in the order
Hemiptera (Fig. 96). Xylem sap is extremely low in
nutrition, and xylem sap-feeders have the highest
feeding rates of any terrestrial animals, consuming
up to 1,000 times their body weight per day.
The best known xylem-limited bacterium that
causes plant diseases is Xylella fastidiosa. Various
strains of X. fastidiosa cause disease in grape, peach,
almond, orange, alfalfa, and numerous tree species
(Table 14). The bacteria and associated gums plug
the xylem system, leading to discoloration and kill-
ing or stunting of leaves and fruits. Pierce’s disease
gated chlorosis are among the best known and most
economically damaging of these diseases. For
example, Pierce’s disease is so severe and widespread
in the southeastern United States that it has pre-
vented commercial viticulture there using suscep-
tible European grapes. Less appreciated, but
economically and ecologically important, are the
numerous and more widespread leaf scorch dis-
eases caused by X. fastidiosa in numerous forest
trees such as oak, sycamore, maple, and elm. This
bacterial species has an enormously wide range of
plant species – about 75–90% of all plant species
tested – in which it can multiply, but it causes symp-
toms in relatively few. Except for a leaf scorch dis-
ease of pear in Taiwan, these diseases appear to be
limited to the Americas. However, in 1996, Pierce’s
disease was confirmed to occur in southeastern
Europe. Numerous other bacterial pathogens invade
the xylem system, but not exclusively. The wide-
spread Leifsonia (Clavibacter) xyli, a xylem-limited
bacterium that causes ratoon stunt disease of sugar
cane, is not transmitted by insects.
The great majority of insect species that are
xylem sap-feeding specialists that have been tested
as vectors (transmitters) of X. fastidiosa have
been shown to be able to transmit this bacterium to
plants. Only a small fraction of the species that are
xylem sap-feeding specialists have been tested as
3886
T Transmission of Xylella fastidiosa Bacteria by Xylem-Feeding Insects
Transmission of Xylella fastidiosa Bacteria by Xylem-Feeding Insects, Table 14  Examples of plant
diseases caused by strains of the bacterium Xylella fastidiosa
Crop Disease
Grape (Vitis vinifera and other Vitis Pierce’s disease
species)
Citrus Variegated chlorosis
Peach Phony disease (dwarfing)
Oak, sycamore, elm, others Leaf scorch diseases
Pear Leaf scorch
Alfalfa Dwarf
Coffee Leaf scorch
See Purcell (1997) for a more complete list
Transmission of Xylella fastidiosa Bacteria by
Xylem-Feeding Insects, Figure 96  The
glassy-winged sharpshooter (Homalodisca
coagulata) a vector of the xylem-limited bacterium
Xylella fastidiosa. Drawing by and with permission
of Rosser Garrison.
vectors, so several thousand species are probably
vectors of X. fastidiosa. This broad degree of vector
specificity, as well as other characteristics of vector
transmission point to the method by which insects
transmit the bacterium. There is no time delay
(latent period) between a vector’s acquiring the
bacterium by feeding on infected plants and its
introducing the bacterium to other plants. Once
infective, a vector can transmit for the rest of its
life, but immature vectors lose the ability to trans-
mit when they shed their skin. All of these charac-
teristics can be best explained if the bacteria
are transmitted from the foregut of the vector.
Where found
Southern North America, Central
America (northern South America?)
South America
Southeastern United States
Southeastern United States
Taiwan
California, probably other locations in
North and Central America
South America, possibly Central
America
The exact location in the foregut from which the
bacteria are transmitted is not yet known. The lack
of a latent period and the persistence of infectivity
in vectors makes control of diseases caused by
X. fastidiosa especially difficult. Because a few
infective insects can quickly transmit the
bacterium to susceptible plants, insecticides to kill
vectors within vineyards has not proven to be
effective.
References
Goodwin P, Purcell AH (1992) Pierce’s disease. In: Grape pest
management, 2nd edn. University of California, Divi-
sion of Agriculture and Natural Resources, Oakland, pp
76–84
Purcell AH (1989) Homopteran transmission of xylem-
inhabiting bacteria. In: Harris KF (ed) Advances in dis-
ease vector research, vol. 6. Springer, Berlin Heidelberg
New York, pp 243–266
Purcell AH (1997) Xylella fastidiosa, a regional problem or
global threat? J Plant Pathol 79:99–105
Purcell AH, Finlay AH, McClean DL (1979) Pierce’s disease
bacterium: mechanism of transmission by leafhopper
vectors. Science 206:839–841
Purcell AH, Hopkins DL (1996) Fastidious xylem-limited
bacterial plant pathogens. Annu Rev Phytopathol
34:131–151
Raven JA (1984) Phytophages of xylem and phloem: a com-
parison of animal and plant sap-feeders. Adv Ecol Res
13:135–234

Transmission Threshold
The level of abundance of a parasite, or the abun-
dance of its vector, that is necessary for disease to
spread.
Transovarial Transmission
Passage of a material through the ovariole and
within the egg.
Transovum Transmission
Passage of a material on the surface of the egg.
Transpiration
The evaporation of water from the surface of plant
foliage.
Transposable Element
An element that can move from one site to
another in the genome. Transposable elements
have been divided into two classes, those that
transpose with an RNA intermediate, and those
that transpose as DNA.
Transposon
A transposable element carrying several genes
including at least one coding for a transposase
enzyme. Many elements are flanked by inverted
repeats. Drosophila melanogaster contains multiple
copies of 50–100 different kinds of transposons.
Transstadial Transmission
The transmission of pathogens or parasites
through successive stages of the host’s life cycle, as
from the egg to the larva, pupa and adult.
Traps for Capturing Insects
T 3887
Trap Crop
A crop or portion of a crop that is intended to lure
insects away from the main crop.
 Cover, Border and Trap Crops for Insect and
Disease Management
Traps for Capturing Insects
Nancy D. Epsky1, Wendell L. Morrill2
Richard W. Mankin3
1
USDA/ARS, Subtropical Horticulture Research
Station , Miami, FL, USA
2
Montana State University, Bozeman, MT, USA
3
USDA/ARS Center for Medical, Agricultural, and
Veterinary Entomology, , Gainesville, FL, USA
Traps developed for capturing insects are as
­varied as the purpose for the trapping, the insects
targeted, and the habitats in which they are used.
Traps are used for general survey of insect diver-
sity, and these usually are simple interception
devices that capture insects moving through an
area. Traps also are used for detection of new
invasions of insect pests in time and/or space,
for delimitation of area of infestation, and for
monitoring population levels of established
pests. This information is used to make decisions
on the initiation of control measures or to mea-
sure effectiveness of a pest management pro-
gram. Traps may be used as direct control
measures, for example, by mass trapping (use of
a high density of traps throughout the infested
area) or by perimeter trapping (use of traps as a
barrier around a pest-free area to intercept
insects moving into the area) to remove a large
number of individuals, with the goal of prevent-
ing or suppressing population buildup. Traps can
be used as direct control measures if they are
highly effective, if they capture a high percentage
of females (especially if they capture them
before they have a chance to lay eggs), and if
they are integrated with other pest management
approaches. Factors such as cost per trap, the
3888
T Traps for Capturing Insects
need to service the traps frequently and the high
reproductive rate of individuals that escape
­capture, however, prevent widespread use of
traps as a stand-alone pest control measure
(Figs. 97 and 98).
Traps for specific insect species or pest groups
may use combinations of cues to lure the target
insect and exploit aspects of the insect’s behavior
to facilitate movement of insects into the trap.
Several factors influence the effectiveness of a
specific trap. The ability of the trap to mimic and
present those cues to the insect, the strength of
those cues in influencing the insect’s behavior,
and the proper placement of the trap in the habi-
tat are important.
Following is an overview of the basic trap
types, and variations of those basic trap types for
specific uses. Traps may be used with or without
attractant cues, and may use a combination of
cues, including visual (color, light, shape), chem-
ical (food/host, pheromone, parapheromone,
oviposition) and acoustic stimuli to make them
more specific and/or more effective. Automated
monitoring systems exist that will transmit
information on trap capture to an offsite station.
Insect traps are an important part of insect pest
management programs. Although a number of
trapping systems are discussed, the intent is to
provide a general framework of types of traps
that are used with some representative examples.
It is not intended to be a complete listing of all
traps that have been developed or are in use.
Representative literature is presented at the end
of the section that will provide additional infor-
mation on insect traps and specific uses.
Trap Types
There are a few basic designs that describe
almost all insect traps. They may be a surface
that is presented flat or is formed into baffles or
cylinders; containers with holes on the sides,
top or bottom; and funnels leading up or placed
over the container to hold captured insects.
However, different types of traps are used for
insects moving through air (that is, flying or
wind-borne insects), ground-dwelling or walk-
ing insects, subterranean insects, or aquatic
insects. A number of these are described
below.
Traps for Flying Insects and
Wind-Blown Insects
Interception Traps
Interception traps are commonly used for fau-
nal surveys in ecological studies, although they
can also have pest management applications.
In its simplest form, it is a suspended net with
an  invagination along the top that leads to a
collecting tube. The Malaise trap is an example
of an interception trap. Fixed interception traps
have been used to study insect migration, with
separate collecting tubes for north-bound
­versus south-bound insects. Or, the trap may
be  used with a wind vane attachment so that
the flat surface of the net swivels to face into
the wind. Large, funnel-shaped nets have been
mounted on moving trucks for sampling flying
insects such as biting midges (Ceratopo­
gonidae) or attached to a suction device to
sample Russian wheat aphids, Diuraphis noxia
(Mordvilko).
Sticky Traps
Panels, cylinders or spheres covered with sticky
material are probably the most commonly used
traps for faunal surveys in agricultural studies. In the
simplest form, they may be clear panels that are
coated with a material that will retain insects that
are blown onto the panel or fly into it. Panels may
also be used with a color and/or a shape and a chem-
ical attractant. Very small insects will be retained by
a thin coating of motor oil, but larger insects may
escape this substance. To capture both small and
 Traps for Capturing Insects
T 3889

Traps for Capturing Insects, Figure 97  Some insect traps: top left, Malaise trap, an interception trap for
capture of flying insects; top right, Steiner trap, a lure-based trap used for capturing fruit flies; second row
left, PC floor trap, a lure-based trap for stored product insects; second row right, pitfall trap for capture of
insects walking on the soil surface; third row left, solar bait station for early detection of wireworms; third
row right, suspended black ball coated with adhesive for capture of tabanid flies; bottom left, red sphere
on yellow panel coated with adhesive for detection of apple maggot flies; bottom right, boll weevil trap.
3890
T Traps for Capturing Insects

Traps for Capturing Insects, Figure 98  Additional insect traps: top left, grain probe traps for detection
of stored grain insects; top right, blacklight trap for detection of nocturnal flying insects; second row
left, wing trap, a lure-based trap with a sticky interior for sampling flying insects; second row right, wasp
trap, a food lure-based trap; third row left, unitrap, a popular pheromone-based trap for capture of
moths; third row right, a bucket trap baited with pineapple and pheromone for capture of palm-infesting
­weevils; bottom left, a cylindrical yellow panel coated with adhesive for detection of flying insects;
­bottom second from left, New Jersey light trap for capturing mosquitoes; bottom third from left, mosquito
emergence trap; bottom right, McPhail trap, a food lure-based trap for capture of fruit flies.

large insects, sticky material such as Tangle-trap is
applied to the surface. The traps can be serviced by
using a small tool to scoop insects of interest off the
trap and onto a card, or the entire trap can be
replaced. For transport, the panel with sticky mate-
rial can be covered with clear plastic wrap or the
panel can be placed in a box with spacers to keep
panels from touching other surfaces. To reuse the
trap, a paint scraper or thinner can be used to remove
sticky material from the surface so that new material
can be applied. The advantage of this trap is that it is
inexpensive and will capture a variety of insects that
are moving through the area. The surface area and
trap orientation can be increased by using two pan-
els that are crossed into baffles. The primary disad-
vantage is the trap can be very messy, can become
coated with dirt or debris and will no longer capture
insects, and the sticky material is difficult to remove
from the captured insects. These traps, as well as
other traps for flying insects described below, are
usually placed above the ground at the height of the
vegetative growth. When used in row crops, the traps
usually are attached to a wooden or metal stake, and
the traps are moved higher as the plants grow over
the season. When used in trees, traps are normally
hung within the canopy. Trap placement and orien-
tation within the canopy, as well as amount of vege-
tation near the trap, will vary among the trap types
and target species.
Three-Dimensional Triangular Traps,
Diamond Traps and Wing Traps
This group is another set of fairly inexpensive traps
that are used with an attractant. These are basically
sticky traps with the sticky surface protected on
the interior of the trap and are either disposable or
used with a sticky component that is replaced at
servicing. Delta traps are small and light-weight
triangular (tent-shaped) traps that are easy to hang
in trees and to transport. The Jackson trap is a
delta trap used for a number of tropical tephritid
fruit flies. It has a removable base coated with
sticky material that can be replaced at time of
Traps for Capturing Insects
T 3891
s­ ampling. Diamond-shaped (in profile) traps are
used to monitor indoor pests in public areas, such
as stores and supermarkets. Wing traps composed
of a roof and a floor are used for pest Lepidoptera.
These are larger and more cumbersome than delta
traps, but the larger surface is more suitable for
larger pest moths. Because the sticky surface is
enclosed, these traps are less susceptible to dirt
and dust and capture fewer non-target insects than
sticky traps, but the surface still may be coated
with dust or debris that gets blown into the trap.
Water Pan Traps
A simple collection method for aphids and other
small flying insects is a water pan trap. Insects flying
over the trap are attracted to the reflective surface of
the water and are captured. The traps are made from
rectangular baking pans, storage containers, or
dish-washing pans partially filled with aqueous
solutions of soap or car antifreeze. Care should be
used in selecting soap to be used so that it does not
contain odors that may be repellent to target insects
or that the antifreeze is environmentally safe. (Most
antifreeze solutions are poisonous, and traps con-
taining antifreeze should be placed so that animals
are unable to gain access to them.) These traps are
open containers, so there may be problems with
movement in wind, evaporation during dry periods
or overflowing during periods of heavy rain.
Bucket Traps
Another simple and inexpensive trap is a bucket
trap. The bucket trap may be used without a lid, or
as a closed container with holes on either the top or
sides for insects to enter. Small drainage holes may
be placed near the bottom of the trap to allow
trapped water to drain out. The Nadel trap and
Mission trap are examples of bucket traps that are
translucent closed containers with entrance holes
around the periphery. The corn rootworm trap has
a large dome-shaped top and a gap between the top
3892
T Traps for Capturing Insects
and the container. Size of the container and place-
ment, diameter and number of entry holes is dic-
tated by the targeted insect. These usually are used
with a chemical lure of some type. These may be
used without a killing agent so that live insects can
be recovered, however captured insects may escape
through the entrance openings. A variety of reten-
tion devices can be used with bucket-type traps. A
pesticide such as dimethyl 2,2-dichlorovinyl phos-
phate (DDVP, mothballs) can be used inside, but if
the concentration is too high it may prevent insects
from entering. Aqueous solutions of soap or car
antifreeze or surfactants such as triton may also be
used. Again, care should be used in selecting soap
that does not contain odors that may repel target
insects and/or environmentally safe antifreeze
should be used. Sticky material may also be used
on either the interior or exterior surface. When
used on the exterior, this may increase effectiveness
of lure-baited traps because usually only a propor-
tion of the insects attracted to the trap will proceed
to enter the trap. However, the same problems out-
lined above for sticky panels will apply to sticky-
coated bucket traps. Open-bottom cylindrical traps
are essentially bucket traps used upside down. The
Phase 4 trap is a green cylinder that uses a yellow
panel as a sticky insert to retain captured insects.
Clear versions of the trap have also been used. In
addition to the opening on the bottom of the trap,
entrance openings also are located around the
periphery of the cylinder.
Bucket Traps with Funnels
Probably the most common traps for agricultural
use are combinations of bucket traps with funnels.
They are more costly than simple bucket traps and
they are often used with some type of odor attrac-
tant. The funnel essentially provides an enlarged
hole that directs movement of the attracted insect
into the bucket. There are differences among this
group of traps in orientation of the funnel and size
of the funnel in relation to size of the bucket. The
Steiner trap is a clear plastic horizontally oriented
cylinder with small funnels centered on the flat
sides of the cylinder. For insects that approach
from the underside of the trap and move upward,
the funnel is used with the large opening facing
downward and the small opening leading up into
a bucket or other container. Because it is difficult
for the insect to find the top of the funnel for exit-
ing, and these insects tend to move upward, they
can be used with or without a pesticide or liquid to
retain the insects. A well-known example of the
downward facing trap is the McPhail trap, which is
a bell-shaped invaginated trap that is used for
tephritid and drosophilid fruit flies. The original
trap was made from glass and there are several
plastic versions of McPhail-type traps available
including dome fruit fly traps, International Pher-
omones McPhail traps and Multilure traps avail-
able that typically have a clear top and a yellow
base. Another example is a wasp trap, such as the
Victor yellowjacket trap. This trap has holes around
the sides of the base for wasps to enter, and then a
funnel that leads to a separate upper container that
retains the wasps.
Other insects approach from the top and
either move or fall downward. For these insects,
bucket traps with funnels that have the large open-
ing facing upward and the small opening leading
down into the bucket are appropriate. The univer-
sal moth trap (unitrap) and Multipher trap are
examples of this trap and they commonly are used
for Lepidoptera adults. These traps have lids held
above the funnel opening to shelter the contents
from rain and are available in a variety of colors. A
trap developed for the Japanese beetle, Popillia
japonica Newman, uses a funnel with the large
opening facing upward and the small opening
over a container, but the funnel is topped by two
panels crossed to form a baffle. Insects are inter-
cepted by the baffles, fall into the funnel and are
captured in the container. The boll weevil trap is a
version of a bucket trap that contains a funnel
mounted on a cylinder. Insects land on the cylin-
der and move up the sides of the trap, enter the
funnel and move into the small collection bucket
above the small funnel top. The Lindgren funnel

trap consists of 4, 8 or 12 plastic funnels stacked
vertically over the container. It is used for ambro-
sia beetles and bark beetles. Fast-flying beetles hit
a funnel and are deflected down into the collec-
tion container.
Cone Traps
Cone traps are essentially bucket traps with funnels,
but the funnel is very large in relation to the size of
the bucket or collecting tube. These are used with
the large opening of the funnel oriented toward the
ground and the top of the funnel leading up to a
container. Examples of these traps include Heliothis
traps and butterfly bait traps. These traps are made
from a light cloth or mesh material and the design
takes advantage of the moth or butterfly’s tendency
to move upward. The butterfly bait traps have a large
container for the butterfly to move into so that the
insect is undamaged.
Traps for Walking Arthropods and
Soil-Dwelling Insects
Pitfall Traps
Pitfall traps are useful for collecting insects
and other arthropods that are walking across
a  surface. This surface is usually a soil surface,
for capturing beetles, spiders and other ground-
dwelling organisms, although they also may
catch flying insects that are walking across
the soil surface. Pitfall traps placed into the top
of stored grain also have been used to sample
stored product insects. Pitfall traps consist of a
container that is buried in the substrate, and into
which insects and arthropods fall and are cap-
tured. The traps used in soil consist of an upper
funnel, a collecting container, and perhaps a
liner that makes servicing easier. Upper funnels
can be made from disposable plastic funnels
with the bottoms removed to enlarge the hole.
Collecting containers can be made from plastic
Traps for Capturing Insects
T 3893
cups, and can be designed for dry catches with
screens in the bottom to permit rain water to
flow through, or can be made to hold a glycol
(antifreeze)/water/detergent solution. Dry con-
tainers need to be serviced several times a week
to minimize destruction of the sampled insects
from other insects entering the trap. They have
the advantage of providing live specimens for
further studies. Wet containers can be serviced
at longer intervals, but have the disadvantage of
filling with rain water. Traps should be designed
to produce minimal impact on the nearby soil,
because insects may be repelled or attracted to
the disturbance. To do this, holes can initially
be  cut with golf-hole cutters and lined with
4”diameter polyvinylchloride (PVC) pipe. The
top of the pipe should be carefully leveled with
the soil, and the traps serviced without disturb-
ing the soil. Covers can be installed over the top
to prevent rainfall from entering. Enhancement-
fences or guides can be installed to guide insects
to the trap. A cone with a gradual slope and
smooth edge is necessary because insects may
back away from the void of a direct hole. Cap-
tured insects should be removed at least weekly
(wet) or twice weekly (dry).
Grain Probe Traps
Grain probe traps are a special modification of a
pitfall trap for use in stored grain. Grain probe
traps consist of an elongated cylinder with holes
drilled into the sides that are above a funnel and
insect receptacle. An early version of the trap
was machined from solid brass and included a
­hollow cylinder made from 14 gauge brass sheet.
Subsequently, probe traps have been made from
clear polycarbonate (Lexan) plastic and from a
perforated section of tubular polyethylene. The
receptacle is coated with liquid Teflon (polytetra-
fluoroethylene) to prevent captured insects from
escaping, however, insects remain alive for a while
and may damage previously captured insects.
These traps may be used at any depth within the
3894
T Traps for Capturing Insects
grain mass, with long rods used to push the traps
into place. A rope connected to the trap is affixed
to the roof of the grain bin to allow removal of the
grain probe trap and to prevent loss of the trap
during grain bin filling and emptying operations.
Traps should be inspected at 1–2 week intervals
to remove the trapped insects. The PC trap is a
cone-shaped trap that usually is used on grain
mass surface, although it too can be pushed into
the grain mass as long as it remains in an upright
position. The top is covered by a convex lid that is
covered with concentric circles of small holes to
allow insects to enter the trap. When used at the
grain surface, the traps are easy to remove for ser-
vicing, but webbing produced by larvae of lepi-
dopteran grain pests, such as the Indianmeal
moth, may block the openings into the trap and
render them ineffective.
Shelter Traps
Shelter traps are used for insects that prefer a dark
harborage and are useful in areas where it is pre-
ferred that the trap be inconspicuous. These are
usually used to intercept insects as they walk over
a surface and have small openings that encourage
insects to enter the trap. Roach motels are the most
well-known examples of such traps. They usually
have a sticky material inside to trap insects that
have entered or contain an oil or other substance
to retain attracted insects. Shelter traps are used
for stored product insects, and designs include
dome traps, stealth traps and corner traps. The PC
floor trap has been modified from the PC trap for
use as a shelter trap by replacing the cone-shaped
bottom with a flat container, which allows the trap
to be placed on the ground or hung on a wall.
Swarm traps are shelter traps that are used to cap-
ture unwanted swarms of domestic honey bees
and to detect invading swarms of Africanized
honey bees. These traps are fairly large bucket-
shaped traps made of molded fiber material, have
a single entrance hole, and are hung at least one
meter above the ground. They provide a nesting
site for bees, and the captured bees can be kept
alive and moved to standard bee hives for honey
production or pest bees can be identified and
destroyed.
Emergence Traps
Emergence traps are a type of cone trap used for
capturing adults that have subterranean larval
and/or pupal stages. These traps are made from
aluminum screening shaped into a funnel, with
the top opening leading to a collecting tube or
vial. The trap is placed flush with the ground and
soil is pushed up around the edges to seal the trap
to the ground. Adults emerging from below-
ground stages move up into the trap and are cap-
tured in the collecting tube. The number of insects
per unit area can be determined and the source of
infestations can be identified. However, these
traps may interfere with ground maintenance
activities that prevent use in certain situations.
Circle traps are another type of emergence trap.
They are wire cone traps that are attached to the
trunk or branch of a tree. Insects moving up a tree
are captured, and because the traps are off of the
ground, they do not interfere with ground main-
tenance activities.
Solar Bait Stations
The above traps can be used to capture the above-
ground stages of subterranean insects, however
the below-ground stages of wireworms (Elateri-
dae), and false wireworms (Tenebrionidae) can
be captured with solar bait stations. These are
used to estimate wireworm populations and
to  make decisions on seed treatment/non-­
treatment. Larvae of these insect groups can be
concentrated by creating microenvironments
that have favorable moisture, temperatures, and
food. A handful of grain (wheat, etc.) is buried a
few inches below the surface of the soil. The bait
is covered with a mound of soil, about 18” high,

and is covered with clear plastic. Edges of the
plastic should be covered with soil to prevent
them from blowing away. Stations should be con-
structed in the fall before soil freezes, and they
can be examined in the spring before planting
time. Surveyors’ flags can be used to mark sites
for easy location.
Traps for Aquatic Insects
Interception Traps
Interception traps capture aquatic insects moving
through the water and are generally similar to
interception traps used for wind-borne insects.
Often, these traps are tapered nets with either
round or rectangular openings which can be fixed
in place to sample insects in moving water or
pulled through the water manually. The size of the
mesh governs the size of insects retained, but use
of too fine a mesh may impede movement of water
through the trap and retain too much debris.
Emergence Traps
Floating emergence traps are used to capture
insects with aquatic larval stages when they emerge
as adults. Construction and use is similar to that
for emergence traps used for soil-dwelling insects.
Attractant Cues
Attractant cues are signals that are used by insects
to locate resources for feeding, members of the
opposite sex for mating, and oviposition sites for
egg laying. Cues are added to traps to increase
insect specificity and effectiveness of the traps.
Attractive cues from natural substrates may be
perceived by one or several of the senses includ-
ing sight, sound, and smell. Semiochemicals are
naturally occurring, message-bearing chemicals
that are used by insects (and other organisms) for
Traps for Capturing Insects
T 3895
communication and for perception of their envi-
ronment. Semiochemicals that have a behavioral
effect on insect orientation, that is, chemicals that
cause an insect to move toward the source, are
used in insect traps. Of specific interest are kai-
romones, which are signals emitted and received
by members of different species (interspecific)
that give an advantage to the receiving species,
and pheromones, which are signals emitted and
received by members of the same species
(intraspecific). Traps may use single cues to lure
insects, but often a combination of cues is used to
improve insect capture. For each cue and each
insect species being targeted, there is usually an
optimal range of stimulus intensity, below which
attraction is minimal and above which attraction
is reduced. Control of the stimulus level is par-
ticularly important for semiochemical cues, and
considerable research has been conducted to opti-
mize emission rates and ratios of semiochemical
blends. This effect seems less important for acous-
tic cues, where it has usually been determined
that the greatest capture rates are found for traps
with the highest sound levels.
Visual Cues
Color
Color can serve as a strong attractant for use in a
trap. Insects may use a specific color to locate host
fruit or plant material, with both hue and intensity
affecting insect response. Contrasts between light
and dark can also play a role, with either the trap
in contrast with the background color or through
the use of lines with insects orienting to an edge
between a light and dark area on a trap. Most sticky
traps use a color to target certain insects. Yellow is
the most commonly used attractant color, and is
used to capture hemipterans such as whiteflies and
aphids, but is also used for almost every order of
flying insects. The Rebell trap is constructed from
two yellow panels as baffles, and is used for walnut
husk flies, Rhagoletis completa Cresson, and cherry
3896
T Traps for Capturing Insects
fruit flies, Rhagoletis cingulata (Loew). A disad-
vantage of using yellow for sticky traps is that it
also attracts beneficial insects such as hymenopteran
parasitoids, and the traps may fill up with these
and other non-target insects. Yellow-colored pan
traps are used to capture Hymenoptera, especially
the parasitoid species. Orange sticky traps are used
for carrot rust fly, Psila rosae (Fabricius), and blue
sticky traps for western flower thrips, Frankliniella
occidentalis (Pergande). Blue is also highly attrac-
tive to tsetse flies (Glossinidae). White sticky traps
are used as panels and as trunk wraps for capture
of tarnished plant bug, Lygus lineolaris (Palisot de
Beauvois), and eastern apple sawfly, Hoplocampa
testudinea (Klug), and red trunk wraps for apple
blotch leafminer, Phyllonorcycter crataegella
­(Clemens). Use of contrasts may increase insect
capture, such as the use of insect silhouettes added
to the surface of white sticky panels to increase
capture of house flies, Musca domestica L.
Shape
Shape can be used as an attractant, although it is
combined with appropriate color for the target
insect. Spheres commonly are used as traps for
tephritid fruit flies. Red spheres are used for apple
maggot flies, Rhagoletis pomonella (Walsh), small
green spheres for blueberry maggot flies, Rhagole­
tis mendax Curran, and large green spheres for
papaya fruit flies, Toxotrypana curvicauda Gers-
taecker. A Ladd trap is a red sphere that is mounted
on a yellow panel and is used for apple maggot
flies and cherry fruit flies, Rhagoletis cingulata
(Loew). Black spheres have been used to capture
biting flies in the family Tabanidae, which are
attracted to the movement of the black ball hang-
ing in a tree. A tree silhouette is mimicked by a
Tedders trap, which is a baffle constructed from
two dark isosceles triangles, with the unequal side
forming the base. The size of the Tedders trap can
be adjusted to optimize capture of tree-dwelling
beetles. Root-infesting weevils, such as pecan wee-
vils, Curculio caryae (Horn) and several citrus root
weevils, as well as wood-boring beetles, may be
captured by these traps. Beetles emerging from
soil or moving along the soil surface respond to
the trap as if it were the trunk of a tree. The insect
moves up the baffles and is captured in a small col-
lection container at the top of the trap.
Light
Attraction of insects to light is easily observed by
standing next to a porch light or street light dur-
ing the night. A commonly accepted explanation
of this phenomenon is that insects have evolved
mechanisms to travel straight paths at night by
orienting at a constant angle to the light of the
moon. Artificial light produced by man-made
devices interferes with this response. Moving at a
constant angle to a light source always directs the
insect toward the source of the light, once it comes
within a few meters. Lights that include ultravio-
let (UV) frequencies may also be attractive
because insects in a confined area can use UV
light as a cue to the direction of an opening into a
clear area. A variety of insect traps have been
developed and used that are based on a light as
the attractant. Lights used include mercury lamps
and black lights (UV) for moths, incandescent
lights for flies and mosquitoes, green lights for
stored product insects and cyalume lightsticks for
aquatic light traps. Light traps, also called electric
traps, are typically bucket traps with funnels.
When used with fluorescent bulbs, the traps have
baffles alongside the bulb that knock insects
attracted to the light down into the trap. The
Pennsylvanian light trap is an example of this
design. Rothamsted and Robinson-type traps use
incandescent bulbs with a reverse funnel over the
light bulb. The New Jersey trap and the CDC trap
are light traps developed for mosquito surveil-
lance. They use incandescent bulbs, a fan that cre-
ates a suction to draws attracted mosquitoes down
into the bucket and a filter to prevent larger insects
from entering the trap. Lights may also be used
with sticky traps to retain attracted insects. These

more commonly are used for control of indoor
pests such as house flies, stored product insects
and fleas. A LED-CC trap for whiteflies uses a
green light-emitting diode (LED) to attract insects
into an open-bottom clear cylindrical trap with a
yellow ring on the bottom.
Chemical Cues
Food/Host Lures
Volatile chemicals emitted from host plants, ani-
mals and other materials are used by insects to
locate food sources. These chemicals are referred
to as kairomones, that is, chemicals produced by a
plant or animal that are advantageous to the
receiving individual of a different species. Host
material can be used to bait traps for insect cap-
ture, and the spectrum of use of food-based baits
for insect control and pest management are cov-
ered in separate chapters. Examples of use of host
material in a trap include use of carrion in pitfall
traps or fruit in butterfly bait traps as survey tools,
or fruit and meat in traps for yellowjackets
(Hymenoptera). Grain or grain products (e.g.,
wheat germ, wheat germ oil, corn oil, etc.) are used
for stored product insect pests, and grain oils used
in shelter traps provide both an attractant and a
method to kill attracted insects. However, host
material may rapidly decay or may release attrac-
tive chemicals for only a short time period after
initial placement. The insect may be using only a
few of the sometimes numerous volatile chemicals
emitted by a host and traps baited with synthetic
chemical versions of the host can be used to lure
an insect into a trap. The quality and quantity of
the chemical can be controlled by the method of
formulation, providing a standard release rate for
a known time period, which improves trap perfor-
mance. Carbon dioxide is used by mosquitoes to
locate vertebrate hosts, and addition of dry ice to a
trap can be used to survey blood-feeding mosqui-
toes. Octenol (1-octen-3-ol) is a naturally occur-
ring chemical emitted by oxen and cows because
Traps for Capturing Insects
T 3897
they ingest large amounts of ­vegetable matter,
and combinations of octenol and carbon dioxide
are used to bait traps for mosquitoes, biting
midges and no-see-ums (Ceratopogonidae). To
make these chemicals more attractive, they can be
combined with heat and moisture in a trap such as
the Mosquito Magnet. Host kairomones are used
with blue sticky traps to capture tsetse flies and in
rootworm traps for corn rootworm adults. Floral
cues are used in traps for Japanese beetles, and for
­nectar-feeding female moths (Lepidoptera). These
are used in bucket traps with funnels. Fruit lures
that provide volatile chemicals emitted from apples
and plums are used in traps for apple ­maggot flies
and for plum curculio, Conotrachelus ­nenuphar
(Herbst). Fruit lures for apple maggot flies are
hung near red sphere traps; fruit lures for plum
curculio are used in a variety of traps, including
Tedders, circle and boll weevil traps. McPhail-type
traps can be used with a variety of liquid baits.
They have been used with fermenting sugar solu-
tions to ­capture small fruit flies (Drosophilidae)
and moths (Lepidoptera), and with aqueous pro-
tein solutions for fruit-infesting fruit flies (Tephrit-
idae). Ammonia has been found to be the primary
chemical responsible for attraction of tephritid
fruit flies to protein solutions, and ammonia
alone or in combination with other synthetic vol-
atile chemicals emitted from protein baits are
used in sticky panels, sticky spheres or McPhail
traps to catch these fruit flies.
Pheromone Lures
There are two main types of pheromones that are
used with insect traps. Sex pheromones are
­produced by one sex to attract the opposite sex.
The sex pheromones most commonly used in
traps are ones that are produced by females. These
are used in either wing traps or bucket with fun-
nel traps, and there are lures available for numer-
ous species of pest Lepidoptera and for sweetpotato
weevils, Cylas formicarius elegantulus (Summers).
The moths tend to be active at night, so visual cue
3898
T Traps for Capturing Insects
is less important, however, the contrast of a white
or light colored trap versus the dark background
often increases capture. The advantage of traps
baited with these sex pheromones is that they are
highly specific and very effective, however, they
capture only males and so no information on or
samples of females are obtained. Some male
tephritid fruit flies produce a sex pheromone that
is attractive to female flies, and the papaya fruit fly
pheromone increases capture of both male and
female flies on green sticky sphere traps.
Aggregation pheromones are used with insect
traps also. These are attractive to both sexes and
are used to bring both sexes to a common loca-
tion for both feeding and mating. Although both
males and females can be captured in traps baited
with aggregation pheromones, they tend to be less
effective lures than sex pheromones or they need
to be presented with other cues. Exceptions are
the pheromone produced by boll weevils (Grand-
lure), Anthonomus grandis grandis Boheman, and
the lesser and larger grain borers, Rhyzopertha
dominica (Fabricius) and Prostephanus truncatus
(Horn). Sticky, shelter and wing traps baited with
these pheromone lures capture both sexes of these
borers. Aggregation pheromones are often pro-
duced by males in conjunction with feeding, thus
since both insect pheromone and host kairomones
are emitted as signals, both are needed to elicit
attraction. Combinations of synthetic aggregation
pheromone and host material as source of kai-
romones are used in shelter traps for stored prod-
uct beetles and cockroaches, in Lindgren or panel
traps for bark beetles, and in bucket traps for palm
weevils. A combination of honey bee pheromones
is used in swarm traps to increase bee capture.
This includes honey bee queen mandibular
­pheromone (BeeBoost) and an orientation phero-
mone produced by worker bees (Nasonov).
Parapheromone Lures
Parapheromones are a special group of lures that
are used to trap some species of tephritid fruit
flies. They act as sex pheromones because they
are highly attractive to male fruit flies, similar to
female-produced sex pheromones. However,
these are not insect-produced compounds and
do not appear to play a dominant role in the biol-
ogy of the responding species. They may be syn-
thetic kairomones, as they are similar in structure
to some plant compounds, and access to the syn-
thetic or natural versions of these compounds
have been shown to increase sexual competitive-
ness of males. These compounds include trimed-
lure for Mediterranean fruit flies, Ceratitis
capitata (Wiedemann), cuelure for melon flies,
Bactrocera cucurbitae (Coquillett), and methyl
eugenol for oriental fruit flies, Bactrocera dorsalis
(Hendel). These lures are most commonly
deployed in white Jackson traps (triangle traps)
or on yellow sticky panels.
Oviposition Lures
Oviposition lures are chemicals that attract egg-
laying (gravid) females. A gravid mosquito trap
uses a baited water solution to attract and capture
the adult females. A trap and bait also has been
developed for navel orangeworms, Amelyois tran­
sitella (Walker), on which the female moth lays
eggs.
Acoustic Cues
Just as many insect species produce volatile chemi-
cals to attract members of the opposite sex, some
species use sound alone or in combination with
chemicals for this purpose. Such cues have been
incorporated successfully into panel or bucket traps
of several different shapes. The different sounds
broadcast as attraction cues have included songs
recorded from conspecifics of the targeted insect
and synthetic mimics of the songs. A variety of dif-
ferent speaker systems have been used, including
standard loudspeakers, piezoelectric boards with
extensive surface areas, and piezoelectric cylinders.

The most successful use of acoustic traps has
been for mole cricket (Gryllotalpidae). Sound
traps have been developed that produce highly
amplified synthetic or recorded calls of male
mole crickets. A bucket or bucket with funnel
trap is placed under the sound emitter to capture
responding crickets. These traps also capture
tachinid flies that parasitize adult crickets and
that locate them by responding to the call. Sticky
traps broadcasting the recorded male lesser wax
moth, Achroia grisella (Fabricius), calling song
have been used to attract virgin females. Many
tephritid fruit flies perform wing-vibration
behaviors during courtship, and there have been
a few attempts to attract female fruit flies by
broadcasting songs recorded from courting
males. Such songs have been demonstrated to be
attractive to Mediterranean fruit flies over dis-
tances of 50  cm or less, but the traps are noisy
and require electric power. Jackson traps broad-
casting the recorded male Caribbean fruit fly,
Anastrepha suspensa (Loew), calling song have
been demonstrated to attract virgin females.
Another use of acoustic cues is as an attrac-
tant for males of some midge and mosquito spe-
cies that form swarms to attract females. When
females fly into a swarm, the males are attracted
by their wingbeats, which are of distinctly lower
frequencies than those of the males in the
swarm. Consequently, males can be attracted in
great numbers by placing a black cloth or other
swarm marker on the ground and broadcasting
recorded or synthetically generated female
wingbeats from a speaker inside or at the edge
of a sticky panel, cylinder, or cup hung about
1 m above the swarm marker. Acoustic traps can
greatly reduce male populations of sedentary
mosquito species, and also have been used to
chemosterilize and ­re-release males rather than
killing them. However, they are not yet in com-
mon use in isolated field environments because
they require electricity and some technical skill
to operate, and the sound that must be broad-
cast at high amplification for optimal trap catch
can be a nuisance.
Traps for Capturing Insects
T 3899
Automated Monitoring Systems
Advances in information technology, computer
technology, and remote sensing are adding to the
field of precision agriculture; that is, use of comput-
ers to aid in management decisions. The ability to
rapidly move data from traps into computer data-
bases or spreadsheets is an integral component of
precision agriculture, and will facilitate making pest
management decisions in a timely manner. Bar
codes can be added to traps and a bar code scanner
can be taken to the field to expedite data entry on
trap type, trap location, etc., so that only insect
counts need to be entered manually. In addition,
data can now be transmitted by cable or wireless
devices directly to a local computer for later down-
loading, or data can be transmitted to an off-site
computer. Ideally, the tasks of species identification
and counting would be automated to eliminate
expensive, time consuming labor. This ideal has not
yet been realized to any practical extent, although it
is a goal of considerable interest to agricultural engi-
neers and entrepreneurs.
A potential method for automating the insect
identification process is to analyze the wingbeats of
insects coming into a trap or flying overhead. Fou-
rier transforms, nearest neighbor classification, and
artificial neural network classification schemes
have been tested in feasibility studies with aphids
and mosquitoes, and species classification accura-
cies of up to 70–90% have been reported. If the
costs of hardware needed to detect and transmit
wingbeat sounds continue to decrease, automated
identification will soon emerge from the labora-
tory as a practical option in environments where
traps are difficult to service or labor costs are pro-
hibitive. An example of counting insects where
traps might be difficult or dangerous to service is a
device to evaluate the intensity of honey bee defen-
sive attacks near a hive. The device includes a
microphone set inside a plastic target, connected to
a datalogger with an amplifier, tone decoder, and a
microcontroller that times and stores information
from the decoder continuously, and later transfers
data to a personal computer. For operation, the
3900
T Traps for Capturing Insects
target is moved next to the hive and the hive is dis-
turbed. The bees attack the target with sharp blows
that are counted and saved for downloading after
the attack is over.
Another already existing approach to auto-
mated off-site monitoring is the use of gravimet-
ric analysis of flight trap captures of red flour
beetles, Tribolium castaneum (Herbst). Beetles
responding to cone-shaped flight traps fall into a
small container coated with liquid Teflon which
rests on the weighing pan of a digital pan balance.
Signals from the balance are sent over a cable to a
personal computer, and the weight, which is
recorded at sequential intervals, is used to esti-
mate the numbers of insects captured over time.
Insect movements that interrupt an infrared light
beam can be counted by a computer that moni-
tors fluctuations in the beam intensity. Infrared
beams can be used in actigraphs to monitor insect
movement in activity chambers. Infrared beams
also are used in a recently developed electronic
grain probe insect counter system. The beams are
located below the bottom of the funnel in a cylin-
drical grain probe trap. Insects falling through the
funnel are counted electronically and time-
stamped data is transmitted to off-site computers.
Counts from electronic traps along with informa-
tion from automated temperature and relative
humidity probes can be collected together and
used for management decisions.
Trap Uses in Integrated Pest
Management (IPM)
The goals of trapping are highly variable. Traps
may be used for general survey of biota, for detect-
ing the start of population increase in infested
areas, for identifying the source of stored product
pest infestation in a store or warehouse, or for
detecting invasion by exotic invasive insect pests
in previously uninfested areas. Trapping systems
for insects are important components in integrated
pest management programs. Trapping data can
be used to make decisions on the initiation or
termination of control measures, as well as to
assess efficacy of control approaches that have
been implemented. Detection trapping is used to
alert personnel to the presence of a new insect
pest in a previously pest-free area so that control
measures can be implemented in a timely man-
ner. Early detection and targeting the locations of
small infestations will facilitate pest management
strategies such as biological control or sterile
insect technique that are most effective when pest
populations are low. With the availability of suffi-
ciently effective traps that capture both female
and male pest insects, trapping systems may be
used as control measures, and thus could be added
to the growing list of biologically based technolo-
gies for insect control. Traps can be used as toxi-
cant delivery systems, with insects that visit the
trap taking a slow-acting poison back to the rest
of the population. This approach is used with
social or gregarious insects such as termites, ants
and cockroaches. Mass-trapping is the use of large
numbers of traps in an effort to suppress the pop-
ulation. Sticky traps are usually used in this
approach as a high percentage of responding
insects are captured. This approach has been used
to suppress populations of a pest such as apple
maggot flies and papaya fruit flies, which spend
part of their life cycle away from the host and can
be intercepted by traps placed around the periph-
ery of the orchard. However, these traps require
frequent servicing to maintain activity. An alter-
nate approach is the development of attract-and-
kill systems, sometimes called attracticides. In
this approach, insects responding to traps con-
sume or contact a toxicant, but then exit the trap
and die away from the trap. Examples include
addition of insecticide to artificial cows for con-
trol of tsetse flies, methyl eugenol mixed with
insecticide for control of oriental fruit flies, addi-
tion of insecticide to pheromone to control cod-
ling moth in apples, and addition of insecticide to
feeding stimulant in corn rootworm traps. All of
these control approaches should be combined
with other pest management strategies to be fully
successful.

References
Hienton TE (1974) Summary of investigations of electric
insect traps. Technical Bulletin 1498. Agricultural
Research Service, USDA, 136 pp
Mayer MS, McLaughlin JR (1991) Handbook of insect phero-
mones and sex attractants. CRC, Boca Raton, 1083 pp
Muirhead-Thomson RC (1991) Trap responses of flying
insects. Academic, San Diego, 287 pp
Pedigo LP, Buntin GD (1993) Handbook of sampling methods
for arthropods in agriculture. CRC, Boca Raton, 714 pp
Southwood TRE (1966) Ecological methods. Chapman and
Hall, New York, 524 pp
Traumatic Insemination
A form of insemination practiced by bed bugs
(Hemiptera: Cimicidae) and some other bugs
wherein the male punctures the female’s abdo-
men with his needle-like penis and deposits
sperm within her hemolymph; they then migrate
to her ovary to fertilize the eggs. This is also
called “hemocoelic insemination.”
 Bed Bugs 
Tree Crickets
A subfamily of crickets (Oecanthinae) in the order
Orthoptera: Gryllidae.
 Grasshoppers, Katydids and Crickets
Trehalose
A polysaccharide found in insects that is one of the
two most common carbohydrate stored reserves
(the other is glycogen) for insect flight. It occurs
principally in the hemolymph, fat body, and gut tis-
sues. Trehalose is usually the first metabolite used
when energy is needed. Each molecule of trehalose
is hydrolyzed into two molecules of glucose. Treha-
lose also is rapidly synthesized from glucose as it is
absorbed in the midgut. Glucose is not usually pres-
ent in high concentrations in the hemolymph
because of this synthesis, so glucose absorption is
easily accomplished.
Treehoppers (Hemiptera: Membracidae)
T 3901
Treherne, John E
John Treherne was born on May 15, 1929, near
Swindon, England. He was educated at Bristol
University. After military service he was invited by
Vincent Wigglesworth the join the Unit of Insect
Physiology at Cambridge. Treherne did so, and
also served as lecturer and reader at the University.
Upon Wiggleworth’s retirement, Treherne headed
up a new Unit of Invertebrate Chemistry and
Physiology at Cambridge. Treherne’s reputation
was based on research of insect neurobiology, the
blood-brain barrier of insects, gut physiology, cir-
cadian rhythms, hormones, cuticle permeability,
osmoregulation, and other physiological subjects.
His subjects were not just insects, as he worked on
molluscs and annelids. Indeed, he was a physiolo-
gist first and foremost, and never pretended to be
an entomologist in the classic sense. Nevertheless,
he enjoyed field entomology, especially marine
and salt marsh insects, and made insightful behav-
ioral and evolutionary contributions in this area.
Treherne served as editor of “The Journal of
Experimental Biology,” and edited “University
Reviews of Biology,” “Advances in Insect Physiol-
ogy,” and others. He served as president of Down-
ing College from 1985 to 1988. Treherne also wrote
popular novels, some of which included entomo-
logical elements. He died on September 23, 1989.
Reference
Foster W (1990) John E Treherne (1929–1989). Antenna
14:6–9
Treehoppers (Hemiptera:
Membracidae)
Chris H. Dietrich
Illinois Natural History Survey, Champaign, IL,
USA
Most treehoppers are readily distinguished from
their close relatives, the leafhoppers, by their
3902
T Treehoppers (Hemiptera: Membracidae)
enlarged pronotum, which extends posteriorly
over the remaining thoracic segments and often
bears horns, spines, bulbs, or other projections. A
few treehoppers have a pronotum that is more
modest in size; these differ from leafhoppers in
that the scutellum is enlarged with either a median
longitudinal keel, or a distinct median longitudi-
nal groove or notch (Fig. 99).
    Order: Hemiptera
     Infraorder: Cicadomorpha
      Superfamily: Membracoidea
       Family: Membracidae
Membracidae, a large and diverse family of
plant-feeding insects, comprises approximately
3,100 described species in 400 genera. Their clos-
est living relatives are Melizoderidae (a small
group of treehopper-like insects endemic to Chile)
and Aetalionidae (a small, mostly neotropical
­family with one endemic southeast Asian genus).
­Aetalionidae, Melizoderidae and Membraci-
dae  together constitute a specialized lineage
­apparently derived from leafhoppers (Cicadelli-
dae). Treehoppers are mainly a tropical group, but
a sizeable fauna of mostly oak-feeding species
occurs in temperate North America. Most of the
subfamilies of Membracidae are endemic to the
new world. Centrotinae, the only treehopper sub-
family that occurs worldwide, is well represented
in tropical and subtropical regions of Africa, Asia
and Australia, but the palearctic fauna is extremely
depauperate. The oldest fossil treehoppers are
known from Tertiary-age Dominican and Mexi-
can amber.
External Morphology
Adult treehoppers range from 3 to 30  mm in
length. In addition to differences in coloration and
the shape of the pronotum, genera and species of
treehoppers differ in the shape and proportions of
the head, the wing venation, the arrangement of
setae on the legs (particularly the hind tibia), the
shape of the female ovipositor and the male geni-
talia. Sexual and seasonal dimorphism in pronotal
shape and color is common in many species. Tree-
hopper nymphs are often even more bizarre than
the adults. some species have large spines on the
head, thorax and abdomen; others are well adapted
for crypsis, being strongly depressed with the flat-
tened tibiae fitting like puzzle pieces into notches
in the sides of the thorax.
Life History and Habits
Details of the life cycle vary from species to spe-
cies. The female deposits several eggs on the bark
or into the living tissue of a woody host plant and
may cover the eggs with a frothy substance that
hardens when dry. The eggs either remain dor-
mant for a period ranging from a month to over a
year, or they develop and hatch within a few weeks.
The young, known as nymphs, feed on plant sap by
inserting their mouthparts into the phloem vessels
of the host plant and go through a series of five
molts reaching the adult stage after a period of
several weeks. The adult males and females seek
each other out for mating, locating each other
through vibrational signals made by sound pro-
ducing organs at the base of the abdomen called
tymbals. These signals are transmitted through the
substrate and are usually too faint to be heard by
human ears. Some treehoppers exhibit anointing
behavior similar to that of their relatives, the leaf-
hoppers, but, unlike leafhoppers, treehoppers do
not produce brochosomes (a hydrophobic, granu-
lated coating).
As implied by their name, most treehoppers
are strong jumpers as adults. However, treehopper
nymphs cannot jump and avoid predation through
crypsis, ant-mutualism, or parental care. Although
many species are solitary as nymphs and adults,
numerous treehopper species are gregarious and
exhibit various degrees of parental care (or preso-
cial) behavior. In the most advanced form of
parental care, females guard their eggs and remain
with the nymphs throughout their development,
repelling invertebrate predators by kicking with
the legs or buzzing the wings.
 Treehoppers (Hemiptera: Membracidae)
T 3903

Treehoppers (Hemiptera: Membracidae), F ­ igure 99 ­Treehoppers (Membracidae). (a) Heteronotus sp.

adult; (b) Smilia fasciata Amyot & Serville adult; (c) Enchenopa binotata (Say) adult; (d) Microcentrus
caryae (Fitch) adult; (e) Microcentrus caryae nymph; (f) Stictocephala taurina (Fitch) nymph. (Photos by C.
H. Dietrich.)

Predators and Parasites invertebrate predators such as spiders, assassin

bugs, wasps and robber flies. Treehoppers also
Treehoppers are a food source for vertebrate are attacked by various parasitoids such as
predators such as birds and lizards, as well as dryinid and mymarid wasps, epipyropid moths,
3904
T Trench Fever
pipunculid flies and strepsipterans. They also
are attacked frequently by entomopathogenic
fungi.
Economic Importance
Several treehopper species are minor pests, par-
ticularly of tropical fruit trees such as papaya,
cacao and palm. A few species are known to
transmit plant pathogens. The buffalo treehopper
(Stictocephala bisonia Kopp & Yonke), a North
American species that injures apple and related
fruit trees, was introduced accidentally into
Europe and now is well established in the tem-
perate zone of the palearctic region as far east as
central Asia.
Control
Treehoppers rarely inflict economic damage on
crops, but when they do, control usually involves
the use of conventional contact insecticides.
 Bugs
References
Deitz LL (1975) Classification of the higher categories of the
New World treehoppers (Homoptera: Membracidae).
North Carolina Agricultural Experiment Station Tech-
nical Bulletin 225:1–177
Deitz LL, Dietrich CH (1993) Superfamily Membracoidea
(Homoptera: Auchenorrhyncha). I. Introduction and
revised classification with new family-group taxa. Syst
Entomol 18:287–296
Dietrich CH, Deitz LL (1993) Superfamily Membracoidea
(Homoptera: Auchenorrhyncha). II. Cladistic analysis
and conclusions. Syst Entomol 18:297–312
Dietrich CH, Mckamey SH, Deitz LL (2001) Morphology-
based phylogeny of the treehopper family Membracidae
(Hemiptera: Cicadomorpha: Membracoidea). Syst Ento-
mol 26:213–239
Mckamey SH (1998) Taxonomic catalogue of the Membra-
coidea (exclusive of leafhoppers). Second supplement to
fascicle I – Membracidae of the general catalogue of the
Hemiptera. Mem Am Entomol Inst 60:1–37
Trench Fever
A bacterial disease of humans transmitted by the
body louse, Pediculus humanus. The disease
agent is Bartonella (Rochalimaea) quintana. The
organism does not affect lice, and is defecated
after a few days within the louse. Humans con-
tract the disease primarily by scratching and
rubbing the organism into wounds (bites,
scratches) but possibly also through inhalation.
Formerly known mostly as a war-related illness,
particularly among soldiers lacking in sanita-
tion, it has also appeared in modern times within
urban settings among the homeless, drug abus-
ers, political refugees, and others lacking ade-
quate access to shelter and sanitation. Recovery
may require a few days to over a month. It is
treated with antibiotics. Symptoms include rash,
malaise, headache and bone pain; mortality is
not attributed to trench fever. Only humans are
known to host this malady.
 Chewing and Sucking Lice
Triassic Period
A geological period at the beginning of the Meso-
zoic era, extending from about 250 to 213 million
years ago.
 Geological Time
Trichobothrium (pl.,
Trichobothria)
Small spots or depressions on the cuticle that bear
setae or bristles. The number and location is often
used for identification of immature insects.
Trichoceridae
A family of flies (order Diptera). They commonly
are known as winter crane flies.
 Flies

Trichodectidae
A family of chewing lice (order Phthiraptera).
They sometimes are called mammal chewing lice.
 Chewing and Sucking Lice
Trichogrammatidae
A family of wasps (order Hymenoptera).
 Wasps, Ants, Bees, and Sawflies
Trichomes
Hairs or small spines on the surface of a plant, and
an important morphological defense against attack
by insects.
 Trichomes and Insects
Trichomes and Insects
Thomas G. Shanower
USDA-Agricultural Research Service, Sidney,
MT, USA
Trichomes, also called plant hairs, are found on
vegetative and reproductive structures in all
higher plant families. They have evolved indepen-
dently in a number of plant families. In general,
monocotyledons are less pubescent (hairy) than
dicotyledons, but trichome production can be
induced in many glabrous (hairless or smooth)
plant species. Several factors, including various
light and temperature regimes, moisture avail-
ability and soil conditions affect the development
and expression of trichomes. Trichomes are the
first structure an insect encounters when landing
on a plant, and provide the initial arena for com-
plex and varied plant-insect interactions.
Types and Functions of Trichomes
The structure and function of trichomes are
highly variably within and among plant species.
Trichomes and Insects
T 3905
There are two general types of trichomes: glan-
dular, which produce, secrete or contain chemi-
cals, and non-glandular, which are simple hairs
and do not produce or contain chemicals.
Trichomes have also been classified morphologi-
cally. Various morpho-types have been observed
including: simple unicellular, multicellular uni-
seriate, multicellular multiseriate, two to five
branched, stellate, dendritic or arboriform, and
peltate. Several different classifications have been
proposed and there is much variation and over-
lap in the description of trichome types. Devel-
oping a generalized classification system based
on trichome morphology has not been possible
because of their highly polymorphic nature
(Fig. 100).
Trichomes may have either or both physio-
logical and defensive functions for the plant,
though may be utilized for a different purpose by
an insect. For example, a dense covering of hairs
on a leaf may have a physiological role for the
plant but may provide a preferred ovipositional
surface for an insect. The following physiological
functions have been identified for trichomes:
altering optical properties of the leaf surface,
deflecting solar radiation and thus reducing leaf
Trichomes and I­ nsects, F
­ igure 100  Trichomes
on the surface of a p ­ igeonpea (Cajanus cajan)
pod. Three types of trichomes are visible: short
and long n ­ on-­glandular (simple hairs), and a
multicellular glandular trichome with a bulb-like
base. Photo credit: International Crops Research
­Institute for the Semi-Arid Tropics, Patancheru,
A.P., India.
3906
T Trichomes and Insects
temperature, maintaining water balance, acquir-
ing ­nutrients and water from the atmosphere, and
excreting excess salts. The focus of this discussion
is insect/trichome interactions; therefore, the
physiological functions of trichomes will not be
considered further. Trichomes can affect both pri-
mary (herbivores) and secondary (predators and
parasitoids) consumers.
The impact of trichome density, length, and
orientation on insect behavior and performance
has been well documented. Trichome density is
perhaps more important than length or orienta-
tion but all three characteristics have been shown
to impact insect behavior and/or performance.
Wild relatives are often good sources of pubes-
cence and have been utilized to develop insect
resistant crop cultivars.
Trichomes as an Ovipositional
Substrate
Oviposition has been positively correlated with
increasing trichome density in many herbivorous
species. For example, more eggs have been
observed on trichome-dense cotton cultivars
compared to smooth cotton cultivars for several
insects including Lygus hesperus, Helicoverpa
spp., Earias fabia and E. vitella. A similar situa-
tion has been noted for Laspeyresia glycinivorella
and Ophiomyia phaseoli on soybean pods and
leaves, respectively. Hairy surfaces can also posi-
tively alter egg and larval development and sur-
vival by ameliorating environmental factors such
as increasing humidity levels. Conversely,
trichomes inhibit oviposition in some insect spe-
cies. At least one species of bruchid, Callosobru­
chus chinensis, prefers smooth as opposed to
hairy pigeonpea (a tropical legume) pods for lay-
ing eggs. The cereal leaf beetle, Oulema melano­
pus, lays fewer eggs on wheat genotypes with
highly pubescent leaves compared to genotypes
with glabrous leaves. Both egg laying and larval
survival are lower on cultivars with relatively
longer and/or denser trichomes.
Impact of Trichomes on Herbivores
Trichomes interact with insect herbivores in many
ways. The role of trichomes in providing defense
against insect herbivores has been well docu-
mented and has been the topic of considerable
investigation. Trichomes provide protection to the
plant by acting as a physical barrier limiting an
insect herbivore’s contact with the plant, or as a
chemical barrier by producing toxic compounds
that poison the insect or by producing gummy,
sticky or polymerizing chemical exudates which
impede the insect. The effectiveness of the first
mechanism, as a simple physical barrier to reach-
ing the plant surface, is dependant on the length,
density, and orientation of the trichomes, and on
the insect’s size, mode of locomotion, and type of
mouthparts. In general, longer, denser and/or
more erect hairs provide a better barrier to insect
herbivores than shorter, sparser or recumbent
hairs. As a purely physical phenomena, trichomes
may also interfere with the insect digestion.
Wild relatives of cultivated plant species often
have higher densities of trichomes than the culti-
vated relatives. A wild relative of pigeonpea pos-
sesses twice the density of small, non-glandular
trichomes on pods as cultivated pigeonpea pods.
When newly emerged pod borer (Helicoverpa
armigera) larvae are placed on pods of both spe-
cies, mortality is increased by 85% relative to the
cultivated pigeonpea. The high density of non-
glandular trichomes prevent the larvae from
reaching the pod surface and they starve or desic-
cate before feeding.
Trichomes have been used to develop soybean
cultivars with resistance to several insect pests.
Soybean leaves possess simple non-glandular
trichomes and cultivars vary in their degree of
pubescence. Feeding and survival of at least four
different caterpillars and two species of beetles
were lower on pubescent leaves than on smooth
leaves. Trichome length and shape are also impor-
tant, especially for small-bodied insects such as
the potato leafhopper. Potato leafhopper popula-
tions decreased with increasing trichome length,

regardless of trichome density. The irregular shape
produced by the highly pubescent accessions pre-
vents potato leafhopper from attaching normally
for feeding and oviposition.
Reduced movement of first instar larvae of
pink bollworm on cotton has been observed on
highly pubescent versus glabrous leaves. Larvae
pause regularly to swing their heads and sample
the substrate while moving. This resulted in higher
larval mortality due to starvation or desiccation.
The larvae of Heliothis virescens are also more
likely to die from biotic (predators and parasites)
and abiotic (high temperature and insecticides)
factors because of slower movement on pubescent
genotypes.
In contrast to non-glandular trichomes, glan-
dular trichomes can act as both physical and
chemical barriers to insect herbivores. The fluidity
and volume of the exudates, whether toxic or
sticky, may vary with weather, time of day and age
of the plant. There is also tremendous diversity in
the structure of glandular trichomes and the com-
position of glandular exudates.
Glandular trichomes confer resistance to sev-
eral phytophagous insects and, because of the toxic
and deterrent properties of their exudates, are
often more effective than non-glandular trichomes
in providing resistance to insect pests. Glandular
trichomes secrete and/or accumulate a variety of
compounds that generally act either as insect
repellents or immobilize insects by entrapment. In
addition to protecting plants by deterring herbi-
vores, glandular trichomes may also attract polli-
nators; these structures contribute to the flavor
and aroma of many plants.
The commercial potato, Solanum tuberosum,
and its wild relatives, Solanum spp., possess two
types of glandular trichomes. Type A is short,
globular, and releases exudates after rupturing;
Type B is longer, more hair-like, and continu-
ously exudes a viscous fluid. After landing, an
insect first encounters Type B exudates. In strug-
gling to escape from the sticky coating, the insect
disturbs and ruptures Type A trichomes. The
exudates in Type A trichomes combine with the
Trichomes and Insects
T 3907
Type B exudates to harden the sticky exudate.
Thus, small bodied insects such as aphids and
leafhoppers are trapped and starve to death. The
Type B exudates also increase the mortality rate
and inhibit settling and probing behavior of
some aphids. These trichomes provide greater
resistance to wild Solanum spp. than in the culti-
vated S. tuberosum. In general, wild species are
more pubescent and have more glandular
trichomes, and are hence more resistant to insect
pests than the cultivated relatives.
Another type of glandular trichome are those
found on chickpea. They secrete highly acidic
(pH = 1) exudates, containing primarily malic and
oxalic acids. The quantity of malic acid in the exu-
date reportedly confers resistance to the leafminer,
Liriomyza cicerina, and the pod borer, H. armig­
era, though others have reported an antibiotic
effect of oxalic acid, but not malic acid.
Impact of Trichomes on Parasitoids
and Predators
Trichomes can have a direct negative impact on
the predators and parasitoids that attack insect
herbivores. The efficacy of these natural enemies
can be impaired by (i) increasing search time, (ii)
decreasing residence time in the host/prey habitat,
(iii) chemical and/or physical entrapment, and (iv)
chemical repellents. As with herbivores, small
bodied natural enemies are generally more affected
by trichomes than larger ones.
The time parasitoids and predators spend
searching for hosts/prey is directly related to their
walking speed; more hosts/prey are encountered
when parasitoids and predators walk faster.
Trichomes, even simple non-glandular hairs, inter-
fere with movement and reduce walking speed.
Faster walking speeds of several egg parasitoids
(Trichogramma spp.) have been measured on
smooth versus hairy cotton leaves and pigeonpea
pods. In addition, parasitoids which walk on the
plant surface can be slowed by exudates secreted
by glandular trichomes. Predators are similarly
3908
T Trichomycetes
hindered by glandular and non-glandular
trichomes. The walking speed of coccinellid larvae
are inversely related to the density of trichomes on
potato and tomato.
On pigeonpea, eggs of an important pest
(Helicoverpa armigera) are readily parasitized
(>55%) by an egg parasitoid (Trichogramma chilo­
nis) when placed on leaves but are rarely attacked
(<1%) when placed on pigeonpea pods. Parasitoids
walked significantly faster on leaves than on pods,
where their movement was inhibited by long
trichomes. The higher density of glandular trich­
omes on pods compared to leaves resulted in the
parasitoids being trapped by glandular exudates.
The same pest (H. armigera) feeds on chickpea, but
is never attacked by the egg parasitoid, T. chilonis.
The highly acidic trichome exudates secreted by
vegetative and reproductive parts of chickpea deter,
and may entrap, the egg parasitoid. Other examples
of Trichogramma spp. being trapped by sticky
trichome exudates have been reported from tomato
and potato.
The negative effects of glandular trichomes
on natural enemies may not be as strong under
field conditions as often observed in greenhouse
or laboratory experiments. Glandular trichome
exudates may be dried by the sun or wind, washed
off by rain, or even be rendered ineffective by dust
under field conditions.
Conclusions
Trichomes are found on vegetative and reproductive
structures in many plant species. There are two types,
non-glandular and glandular; both are found in a
variety of shapes and forms. Trichomes and insects
interact in numerous ways. Trichomes on a number
of plants have evolved a defensive function and may
protect plants from insect herbivores. Plants are pro-
tected from insect feeding when trichomes form a
chemical or physical barrier, preventing herbivores
from reaching the surface. Trichomes may also pro-
vide a preferred oviposition site and/or may inter-
fere with an insect’s movement on the plant surface.
Both positive and negative interactions, from the
insect’s point of view, have been documented. Gen-
eralizing about the role and function of trichomes
and how these structures interact with insects is dif-
ficult because trichomes vary greatly across plant
species and because the interactions may be specific
or unique to the plant-insect association.
 Plant Resistance to Insects
References
Gutschick VP (1999) Biotic and abiotic consequences of dif-
ferences in leaf structure. New Phytol 143:3–18
Juniper BE, Southwood R (eds) (1986) Insects and the plant
surface. Edward Arnold, London, 360 pp
Levin DA (1973) The role of trichomes in plant defense.
Q Rev Biol 48:3–15
Peter AJ, Shanower TG (2001) Role of plant surface in resis-
tance to insect herbivores. In: Ananthakrishnan TN (ed)
Insects and plant defense dynamics. Science, Enfield,
NH, pp 107–132
Romeis J, Shanower TG, Peter AJ (1999) Trichomes on
pigeonpea (Cajanus cajan) and two wild Cajanus spp.
Crop Sci 39:564–569
Trichomycetes
charles e. beard
Clemson University, Clemson, SC, USA
Trichomycetes are obligate symbiotic organisms
that typically live in the guts of arthropods. They
are generally viewed as commensals, having little
effect on the host, but in stressful environments
they might confer an advantage to colonized hosts;
in some cases they act as pathogens. In the broad
sense, trichomycetes (designated by a lower case t)
includes the fungal class Trichomycetes (desig-
nated by an upper case T) and some historically
similar protists that were earlier considered fungi.
Most trichomycetes colonize freshwater and
marine arthropods, but some colonize terrestrial
arthropods. Hosts are filter feeders, detritus feed-
ers, or aquatic grazers, but not predators or fluid
feeders (e.g., Brachycera) (Fig. 101).
 Trichomycetes
T 3909

Trichomycetes, Figure 101  Trichomycetes: (a) Fresh dissection of Harpella melusinae from Simulium

innoxium. Asexual spores and conjugating thalli are shown. cj = conjugating thalli, hf = holdfast,
sp = asexual spore, th = vegetative thallus. Scale bar is 30 μm. Phase contrast. (b) Preserved Smittium
sp. from Blepharicera similans. Scale bar = 20 μm. (c) Asexual spore showing collar. cl = ­collar. Scale bar
is 10 μm. (d) Zygospore of Trichozygospora chironomidarum showing thickened end walls, collar, and
multiple ­appendages. ap = appendages, cl = collar. Scale bar is 20 μm. Photo courtesy of R. W. Lichtwardt.
(e) Asellaria ligiae with asexual spores produced inside thallus (endogenous). sp = spore, th = vegetative
thallus. Scale bar is 20 μm. Photo courtesy of R. W. Lichtwardt.

Non-Fungal Trichomycetes Because of similar lifestyles, all trichomycetes were

The first trichomycetes were described by Joseph
Leidy in 1849 from millipedes. Initially, Leidy
thought trichomycetes were colorless algae. Later,
trichomycetes were placed in various fungal groups.
placed in the fungal class Trichomycetes until the
1990s. The non-fungal trichomycetes constitute
the orders Amoebidiales and Eccrinales. Recent
molecular analysis has shown that these trichomy-
cetes are protists in the Mesomycetozoa group.
3910
T Trichomycetes
Order Amoebidiales
The thalli of these trichomycetes are coenocytic
(one large multinucleate cell not divided into cells
by septae or cross walls) and unbranched. They are
usually associated with freshwater larval Diptera
or Crustacea. They are most common with filter
feeders and grazers, but might occur externally on
predatory insects. A secreted holdfast is usually
evident. Many workers had suspected that
organisms in the order Amoebidiales were not
fungi, because they produce amoeboid dispersal
cells and lack chitin (or have very little). This
order  includes two genera: Amoebidium and
Paramoebidium.
Amoebidium parasiticum attaches to the
external cuticle of freshwater arthropods (e.g.,
Diptera, Ephemeroptera, and Crustacea). Amoe­
bidium spp. are usually restricted to still-water
(lentic) environments. Although not pathogenic,
this fungus has a life cycle that is closely coordi-
nated with that of the host. During the intermolt
period of the host, the thallus produces asexual
spores that can attach to other areas of the cuticle.
Prior to molting or at host death, production of
amoeboid cells rather than spores begins. The
amoebae swarm from the thallus, encyst, and pro-
duce spores. These then form new thalli upon
external contact with hosts. Sexual reproduction
has not been verified.
Paramoebidium species live in the hindgut of
aquatic insect larvae, usually hosts from the orders
Diptera, Ephemeroptera, and Plecoptera. They do
not produce spores directly, as do Amoebidium
spp., but produce amoebae upon molting or death
of the host. The amoebae swarm and then produce
cysts that produce spores. Spores in this genus are
presumed to germinate in the gut after ingestion.
Sexual reproduction is unknown.
Order Eccrinales
The thalli are coenocytic and unbranched; how-
ever, in some species (e.g., Leidyomyces attenuatus
in passalid beetles), multiple thalli share a com-
mon attachment point and appear branched at the
base. The holdfast is a secreted material and can be
large. These trichomycetes are found in the foregut
or hindgut of Crustacea, Diplopoda, Insecta and
Isopods. Eccrinales is the only trichomycete group
in terrestrial insects (Passalidae and Scarabaei-
dae), other than Orchesellaria (see Asellariales
below) in Collembola. Various asexual spore types
are formed depending on taxon. The spores are
usually formed by division within the tips of veg-
etative thalli. Fusion of adjacent cells has been
reported, but confirmation of subsequent sexual
spores is lacking.
Fungal Trichomycetes (Class
Trichomycetes)
Trichomycetes are a class in the fungal division
Zygomycota and include the trichomycetes most
encountered in insects. Sexual zygospores are pro-
duced in many of the taxa.
Order Asellariales
Thalli of these fungi are branched and septate. The
septation produces endogenous (inside the thal-
lus) spores. The holdfast area (basal cell) often
appears bulbous or branched (digitate). The order
consists of two genera. The genus Asellaria inhab-
its isopods (Crustacea) and the genus Orchesell­
aria inhabits springtails (Collembola). Zygospore
production following conjugation of thalli has
been reported in this order.
Order Harpellales
The thalli produce large cells with septa. The spores
are produced exogenously. Many spores have non-
motile appendages that are usually longer than the
spore proper. The length and number of append-
ages have taxonomic value. Harpellales in the

midgut are unbranched (Harpellaceae), whereas
the species in the hindgut (Legeriomycetaceae)
have a branched growth pattern. These Trichomy-
cetes are common in aquatic insect larvae, espe-
cially Diptera. No Trichomycetes have been found
in predatory insects, and most occur in filter-­
feeding or grazing insects.
Harpellales exhibit three reproduction types
in their life cycle. The most common type is the
production of asexual spores that are shed in the
feces and ingested by hosts. When in the proper
gut environment, asexual spores quickly germi-
nate. Germination is a complex process involving
extrusion of the spore protoplast from the spore
wall and attachment to the host gut. The second
type of spore is the sexual zygospore, which is pro-
duced by fusion of nuclei from adjacent cells of
the same thallus or of neighboring thalli. Conjuga-
tion tubes between thalli are sometimes detected
in the latter, whereas the sexual apparatus might
not be evident in the former. The zygospores are
usually characterized by a thickened end wall on
one or both poles of the spore. The role of the
zygospore in the natural history has not been
determined, but because of the biomass invest-
ment, it presumably plays an important survival
role. A third type of spore is the pathogenic spore,
often referred to as a cyst (not to be confused with
the cysts of Amoebidiales). These spores prolifer-
ate in the ovaries of adult females and are depos-
ited as if they were eggs. The cysts produce spores
(smaller than other asexual spores) that presum-
ably colonize new larvae from adjacent eggs as the
clutch hatches. This cycle helps explain how tricho-
mycetes can colonize upstream hosts as the spores
in feces are washed downstream, because infected
females can carry the cysts upstream. The cyst
stage is documented in a few locations (due to
insufficient geographic sampling) (e.g., eastern
Canada), but is expected to be common at a site on
a temporal basis.
Harpellales are the Trichomycetes most likely
to be encountered by entomologists; therefore, a
few specific examples are presented. Harpella
­melusinae is common in larval black flies (Diptera:
Trichomycetes
T 3911
Simuliidae) on all continents except South Amer-
ica and Antarctica. Different species of Harpella are
found in South America and black flies are not
known from Antarctica. Harpella melusinae inhab-
its the midgut of the larva, where the pH is very
high (up to pH 11.3) in Diptera. The fungal thalli
attach to the peritrophic matrix and grow in this
seemingly hostile environment. Asexual spores
form on the unbranched thalli, usually absorbing
the protoplast from the vegetative thallus and leav-
ing empty cell walls. These spores continue through
the hindgut unaltered and exit with the wastes.
Sexual conjugations between adjacent vegetative
thalli occur in some populations. When conjuga-
tions are occurring, large numbers of thalli in a
locality might be sexual. Zygospores are seldom
seen in fresh dissections, but in nature zygospores
likely are produced by these conjugations. Other
larval Diptera have Trichomycetes in the midgut.
Species of Stachylina are common in chironomids
and occasionally in Blephariceridae. No Trichomy-
cetes have been reported from mosquito midguts.
Smittium species are the most commonly cul-
tured Trichomycetes. These branched hindgut-
dwelling species are known from larval Diptera
such as Chironomidae, Culicidae, Simuliidae, and
Tipulidae. Often, a species can inhabit larvae of
different host families, a degree of host plasticity
not seen in most Harpellales. Asexual spores are
produced on branched thalli and have one hair-
like appendage. When ingested, the spores react to
gut pH changes and potassium levels to avoid ger-
minating in the midgut (high pH) where they do
not grow, but delay germination until until they
pass to the hindgut with its lower pH. Zygospores
are formed after conjugation of thalli and can be
quite large. Zygospores of Smittium megazygospo­
rum can be up to 150 μm long. Pathogenesis has
been reported in the species Smittium morbosum.
This species appears to mechanically interfere with
molting of the hindgut lining and thus leads to
mortality.
Stoneflies are hosts of several genera, includ-
ing Capniomyces, Ejectosporus, Genistelloides,
Orphella, and Paramoebidium. The stonefly genus
3912
T Trichopsocidae
Allocapnia has been of particular interest because
of its hypothesized biogeography and use in dat-
ing symbiotic associations. Two of the species of
Trichomycetes (Genistelloides hibernus and Ejec­
tosporus spica) that colonize Allocapnia have a
wide distribution. Based on hypothesized host ori-
gins, the association is dated from the Pleistocene,
and must have been in the host from this time
(early in its evolution) and before dispersal. One
trichomycete species (Capniomyces stellatus) had
restricted distribution and was hypothesized to
have evolved after Allocapnia dispersal.
Organisms that Might Resemble
Trichomycetes
Insects host a variety of organisms that can be
confused with trichomycetes. Among the non-
fungal forms is a bacterium called Arthromitus.
This bacterium forms chains of cells attached at a
common point, so they appear as tufts or clusters.
Molecular evidence has shown that many of these
are an alternate growth form of the soil bacterium
Bacillus cereus.
External fungi that resemble Amoebidiales
include chytrid fungi and Laboulbeniales. The chy-
trid fungi resemble Amoebidium, but they produce
flagellated zoospores for reproduction. The names
Harpochytrium and Oedogoniomyces have been
associated with these fungi. These fungi are proba-
bly incidentals, and are usually expected on other
substrates. The Laboulbeniales can be distinguished
by thick cell walls and septate thalli that are often
branched. Also, Laboulbeniales are usually
restricted to terrestrial insects and often have a tan
color. Trichomycetes are usually colorless or white.
Passalid beetles host an ascomycete fungus
that grows in a trichomycete-like form in the gut.
The septate filaments form tufts on the hindgut
lining. These fungi have a yeast-growth form in
culture. They belong to the genus Pichia or Entero­
ramus (synonym). They have the ability to digest
xylose, which can be beneficial to wood-feeding
organisms.
References
Leidy J (1849) Enterobrus, a new genus of Confervaceae. Proc
Acad Nat Sci Philadelphia 4:225–233
Lichtwardt RW (1986) The Trichomycetes: fungal associates
of arthropods. Springer, Berlin Heidelberg New York,
343 pp
Lichtwardt RW (1996) Trichomycetes and the arthropod gut.
In: Howard D, Miller D (eds) The Mycota, animal and
human relations. Springer, Berlin Heidelberg New York,
pp 315–330
Lichtwardt RW, White MM, Cafaro MJ (2003) Freshwater
trichomycetes and their arthropod hosts. In: Tsui CKM,
Hyde KD (eds) Freshwater mycology. Fungal Diversity
Research Series 10. Fungal Diversity, Hong Kong, pp
81–100
Misra JK (1998) Trichomycetes-fungi associated with arthro-
pods. Symbiosis 24:179–220
Nelder MP, Beard CE, Adler PH, Kim S-K, McCreadie JW
(2006) Harpellales (Zygomycota: Trichomycetes) asso-
ciated with black flies (Diptera: Simuliidae): world
review and synthesis of their ecology and taxonomy.
Fungal Diversity 22:121–169
Trichopsocidae
A family of psocids (order Psocoptera).
 Bark-Lice, Book-Lice, or Psocids
Trichoptera
An order of insects. They commonly are known as
caddisflies.
 Caddisflies
Tricorythidae
A family of mayflies (order Ephemeroptera).
 Mayflies
Tridactylidae
A family of grasshoppers (order Orthoptera). They
commonly are known as pygmy mole crickets.
 Grasshoppers, Katydids and Crickets
 Tritrophic Interactions
T 3913

Trigonalyidae Tritocerebrum

A family of wasps (order Hymenoptera).
 Wasps, Ants, Bees, and Sawflies
Trimenoponidae
The portion of the brain that innervates the labrum
and stomatogastric nervous system, and the most
posterior portion of the brain (Fig. 102).
 Nervous System

A family of chewing lice (order Phthiraptera). Tritrophic Interactions

They sometimes are called marsupial lice.
 Chewing and Sucking Lice Marcel Dicke
Wageningen University, Wageningen, The Nether-
lands
Trinotonidae
Two central issues in ecology are (i) how do
A family of chewing lice (order Phthiraptera). organisms interact with their environment, and
 Chewing and Sucking Lice (ii) what interactions determine the composi-
tion and dynamics of communities. Ecologists
have long debated the relative importance of
Triozidae bottom-up and top-down effects on communi-
ties. An example of a bottom-up effect is that
A family of bugs (order Hemiptera, superfamily nutrient availability to plants can affect the com-
Psylloidea). position of insect communities and this can sub-
 Bugs sequently influence ­top-down forces. Top-down

Ocellar nerve Aorta

Optic lobe Crop
Antennal nerve Hypocerebral ganglion
protocerebrum
Recurrent nerve
Medial ocellus
Deutocerebrum

Tritocerebrum Ventricular nerve

Frontal ganglion Corpus allatum

Labral nerve
Subesophageal
Pharynx ganglion
Circumesophageal
connective

Tritocerebrum, Figure 102  Diagram of the insect brain, lateral view (adapted from Snodgrass, Insect
morphology).
3914
T Tritrophic Interactions
effects comprise, for instance, the effects of car-
nivores on herbivore populations with conse-
quences for plant population biology. However,
it is becoming more and more clear that this is
not an either/or issue, but rather one of the
degree to which bottom-up and top-down forces
are integrated. Bottom-up forces, such as nutri-
ent availability to plants, can affect the composi-
tion of animal communities and this can
subsequently influence top-down forces. Fur-
thermore, plants have many characteristics that
influence the effectiveness of carnivores in
reducing herbivore numbers, i.e., bottom-up and
top-down forces can be linked.
Although it is long-known that food webs
are composed of more than two trophic levels, it
was Price and coworkers who, in 1980, pointed
to the important effects of plants on interactions
between herbivores and carnivores, and of carni-
vores on herbivore-plant interactions. They
introduced the term “three-trophic level interac-
tions” or “tritrophic interactions.” With this term,
they indicated that apart from food web consid-
erations where one trophic level feeds on another
(lower) level, there are interactions between
alternate trophic levels that can be of decisive
importance to the outcome of interactions
between two subsequent trophic levels. Thus,
within a tritrophic context, indirect interactions
in a community are considered in addition to
direct interactions.
Direct versus indirect defense of plants
Indirect defense
Providing shelter,
alternative food or
improving
foraging
effectiveness
Tritrophic Interactions, Figure 103  Direct and indirect defenses of plants in a tritrophic context.
To obtain a sound ecological understanding
of each bitrophic interaction (one between plants
and herbivores and the other between herbivores
and carnivores), it is essential to consider at least
three trophic levels and all their interrelation-
ships. For instance, plant defense may be aimed
directly against herbivores, but, in addition, carni-
vores may be a component of the plant’s battery of
defense. Thus, there are two distinct kinds of plant
defense (i) direct defense where plant characteris-
tics have a negative effect on herbivores, and (ii)
indirect defense that affects herbivores by pro-
moting the effectiveness of their carnivorous ene-
mies. Direct defense may consist of such elements
as repellents, toxins or digestibility reducers, while
indirect defense may consist of the provision of
shelter, alternative food, or chemical information
that promotes the abundance and/or activity of
carnivores (Fig. 103).
The majority of research has been done on
plants and arthropods and, therefore, this discus-
sion concentrates on these organisms. The arthro-
pods involved are herbivorous arthropods and
carnivorous arthropods, i.e., predators and parasi-
toids (parasitic wasps). Tritrophic interactions
between plants, herbivores and carnivores will be
addressed. However, tritrophic interactions are
not restricted to these three trophic levels; they
may also encompass interactions between, for
example, herbivores, first order carnivores and
second order carnivores.
Carnivore
Herbivore
Direct defense
Toxins, digestibility
reducers, repellents,
thorns, spines
Plant

Plant Characteristics that Affect
Herbivores and Indirectly Affect
Natural Enemies of the Herbivores
Any plant condition that reduces the growth rate
of an herbivore makes the herbivore available to
natural enemies for a longer period of time and,
thus, raises the probability of mortality. This is
especially true for mortality from parasitoid attack,
because parasitoids are usually stage-specific and,
thus, prolongation of the vulnerable growth stage
may be essential for the parasitoid to find that
stage. For instance, digestibility reducers have
growth-retarding effects. This theory was tested
using several soybean varieties, the Mexican bean
beetle (Epilachna varivestis Mulsant) as the herbi-
vore and some predatory pentatomid bugs. It was
found that the herbivores that grew more slowly
were more effectively regulated by the predator
than those on the soybean variety that was more
favorable for herbivore growth. In addition, it was
found that the reduced growth rate of the herbi-
vore also affects the functional response of the
predator (the relationship between predation rate
and prey density) because more small prey are
needed for satiation than large prey, and small
prey are usually easier to handle by the predator.
Digestibility reducers produced by plants may
affect herbivore-natural enemy interactions in
several ways:
1.  Prolonged developmental time of herbivores and,
thus, prolonged risks of attack by carnivores.
2.  Reduced resistance of herbivores to pathogens and
natural enemies.
3.  Reduced herbivore body size and, thus, fecundity,
resulting in a lower rate of population increase.
This may determine the ability of natural enemies
to exterminate the herbivore population.
The influence on enemy effectiveness through
a direct influence on herbivores is not limited to
digestibility reducers. Any plant characteristic that
can affect growth, resistance to disease, or fecundity
can have an influence. Variation in plant nutrient
Tritrophic Interactions
T 3915
composition is probably important in this regard.
While such variation probably seldom involves
complete presence or absence of essential nutri-
ents, changes in their proportions appear to be
commonplace. Effects that are sublethal should,
therefore, also be commonplace. Negative effects
of imbalanced diets on insect survivorship, growth,
and development, not surprisingly, have been
demonstrated in controlled artificial diets for a
number of insects and nutrients.
On the other hand, retardation of herbivore
growth may hamper some predators or parasi-
toids. For instance, some predators do not take
small prey because of a low energetic (nutritional)
reward in combination with high capture costs.
For example, an insectivorous bird, the European
Great Tit, rejects small insect prey when large prey
are available.
Another effect of growth rate and size results
from the minimum size of an herbivore that is
acceptable to its natural enemies; however, this
critical size is different for different natural enemy
species. Luck and colleagues at the University of
California showed that host size is a very impor-
tant factor in the coexistence of Aphytis parasitoid
species attacking Californian red scale, Aonidiella
aurantii (Maskell). Aphytis lignanensis needs larger
hosts for female progeny than Aphytis melinus
DeBach. Thus, A. melinus can attack hosts before
they become available to Aphytis lignanensis Com-
pere. In addition, host size depends on plant part.
Host size is smallest on wood, largest on fruits and
intermediate on leaves. Thus, many more scales
are available to A. melinus than to A. lignanensis,
and the degree of this difference is dependent on
the location in the tree. As a consequence, A. meli­
nus can effectively replace A. lignanensis in many
citrus areas where red scale is a problem. It is sim-
ple to imagine that the three plant parts (wood,
leaves and fruits), actually represent different “cul-
tivars” of a species with different levels of defense,
and their different impacts on host-parasitoid
interactions.
Retardation of growth can also result from
induced resistance in plants. In many cases, plant
3916
T Tritrophic Interactions
defense is not active prior to herbivore infestation.
The damage inflicted by herbivores may induce
the defensive actions of plants. Thus, the produc-
tion of phytoalexins in response to infestation by
pathogens is well known. Such induced responses
also may occur after an herbivore attack. For
instance, tomato plants that are damaged, either by
herbivores or by mechanical means, produce pro-
teinase inhibitors that reduce the digestibility of
the plant material. These proteinase inhibitors are
produced systemically throughout the damaged
plant. Induced resistance (or induced direct
defense) appears to be rather nonspecific. Infesta-
tion with one species of herbivore often affects the
performance of other herbivore species as well.
Induced resistance lasts for some time after the
herbivores are gone. It may last for hours or days,
but in some cases (e.g., for perennial plants such as
trees), induced resistance has been reported to last
for one to several years. Thus, previous and cur-
rent herbivory may affect the growth rate of other
herbivores and, thus, their vulnerability to parasi-
toids and predators. In addition, mechanical char-
acteristics of plants can be subject to induction
also (e.g., trichomes of nettles).
Plant Characteristics that Directly
Affect the Effectiveness of Natural
Enemies of Herbivores
Mutualisms between plants and animals have been
known for a long time but, until the 1980s, the
focus had been almost exclusively on mutualisms
between plants and herbivores, e.g., involving pol-
lination or seed dispersal. The best and longest
(more than 100 years) known mutualism between
plants and members of the third trophic level is
that between Acacia plants and protective ants.
The Acacia plant provides sugar-containing secre-
tions from extrafloral nectaries and other macro-
nutrients from food bodies on their stems, leaves,
or buds. Some Acacia species even provide hollow
stems, thorns, or bulbs that the ants penetrate to
use as shelter for their colonies. The ants guard the
source of nutrients and simultaneously defend the
plant against herbivorous insects or even encroach-
ing vegetation. Recently, it was shown that ants
may even reduce the feeding by large herbi-
vores  such as giraffes. Also, less conspicuous
­structures, such as pits and pouches at vein cross-
sections, can function as shelter for carnivorous
enemies of herbivores. Such structures are called
“domatia” (Greek for “little rooms”) and are usu-
ally inhabited by predatory or fungivorous mites,
whose activities can be important in reducing the
abundance of plant attackers.
The protection of plants by ants is far more
general than the well-known example of Acacia
suggests. Many plant species have well-developed
nectaries on stems, stipules, or leaves, or they
secrete sugar-rich liquid from unopened flower or
leaf buds. Such nectaries attract virtually any
sugar-loving ants, most of which also eat insects.
In temperate climates, seedlings and developing
buds often secrete nectar, and are defended by
ants. For example, seedlings of cherry trees (Pru­
nus sp.) secrete nectar that encourages their
defense by a variety of opportunistic ants.
Ants are generalist protectors that can defend a
plant against a wide variety of herbivores. However,
recent evidence shows that mutualisms between
plants and members of the third trophic level also
involve much more specialized predators and para-
sitoids. When a plant is attacked by an herbivore,
the plant starts to produce and emit volatiles that
attract natural enemies of the herbivore. This
appears to be a common phenomenon among
plants and many different herbivore species have
been shown to induce carnivore attractants in plants
(Fig. 104). Herbivory is not always necessary. Hilker
and colleagues of the Free University of Berlin
showed that even the deposition of herbivore eggs
can induce a plant to emit induced volatiles that
attract egg parasitoids. It has been shown for several
tritrophic systems that the natural enemy discrimi-
nates between different plant species infested by the
same herbivore species and between different her-
bivore species on individuals of one plant species.
Chemical analyses have shown this specificity on

Herbivore-induced carnivore attractants:
a common phenomenon
Plants Herbivores Carnivores
• 8 families • 13 families • 8 families
• 23 species • 27 species • 28 species
Monocots e.g. mites, e.g. parasitic
and dicots thrips, aphids, wasps and
mostly agricultural butterflies predatory mites
plants and months and bugs
Tritrophic Interactions, Figure 104  The
­induction of carnivore attractants by herbivory
has been reported for a wide variety of tritrophic
systems.
the molecular level. The composition of the blend is
determined to the greatest extent by the plant spe-
cies/cultivar. Not only natural enemies of the herbi-
vore seem to use the herbivore-induced synomone,
herbivores may respond also; spider mites avoid
locations with high concentrations of induced plant
volatiles that are related to conspecific damage. In
addition, for a tritrophic system consisting of lima
bean or cotton plants, spider mites and predatory
mites, it was recorded that downwind, uninfested
neighbors of infested plants are more attractive to
predatory mites than upwind neighbors or other
control plants.
Apart from mutualistic interactions, plants
also may hamper the performance of natural ene-
mies. For instance, a thick bark hinders parasitoids
that attack herbivores that forage under the bark.
The same holds true for the effect of gall thickness
on parasitoids of gall-forming herbivores. Hairs
on stems and leaves may affect the locomotion and
the survival of natural enemies of herbivores (in
addition to adverse effects on herbivore perfor-
mance). For instance, cucumber leaves have many
long, non-flexible hairs that interfere with parasi-
toid movement. In addition, herbivore products,
such as honeydew, may adhere to these hairs,
which enhances the adverse effects on parasitoid
performance. The capability of the parasitoid
Encarsia formosa Gahan to reduce populations of
the greenhouse whitefly (Trialeurodes vaporario­
rum) on cucumbers depends on the density of
Tritrophic Interactions
T 3917
these hairs. Also, trichomes that hamper herbivore
survival may have strong adverse effects on the
survival of natural enemies. Hairs, usually seen as
a component of direct defense against herbivores
thus may be incompatible with natural enemies
that are a component of indirect defense.
Effect of Dietary Specialization
An animal’s degree of dietary specialization is an
important characteristic frequently used in com-
parative ecological and evolutionary studies. This
concept also has been applied to herbivores and
their natural enemies, although knowledge on
herbivore range used by natural enemies is gener-
ally sparse. Dietary specialization of herbivores is
assigned to the plant level, while dietary special-
ization of natural enemies can be assigned to both
the herbivore and the plant level.
Specialist herbivores are usually better
adapted to plant defenses, such as toxins, than are
generalized herbivores. Specialist herbivores can
usually tolerate higher levels of toxins and can
sequester the defensive plant chemicals. As a result,
they usually are much better protected against
their natural enemies such as pathogens, predators
and parasitoids. For example, consider the interac-
tions between the nicotine in tobacco, the ­specialist
herbivore Manduca sexta L. (tobacco hornworm),
the generalist herbivore Trichoplusia ni (Hübner)
(cabbage looper), and a pathogenic bacterium,
Bacillus thuringiensis. The generalist herbivore is
adversely affected by the nicotine in the plant,
while the nicotine has only minor effects on the
fitness components of the specialist herbivore.
Higher nicotine concentrations in the plant are
actually beneficial to the specialist herbivore
because infection by the pathogen B. thuringiensis
is reduced. Among predators and parasitoids, the
specialists also are better adapted to the defenses
of their prey/host. Thus, specialist herbivores are
better protected against generalist natural enemies
than against specialist natural enemies. This exam-
ple shows that tritrophic interactions also may
3918
T Tritrophic Interactions
extend to pathogens of herbivores. The following
example relates to the dietary specialization of
parasitoids. Nicotine may be sequestered by
Spodoptera frugiperda (J. E. Smith) (the fall army-
worm), and adversely affects the development and
survival of the polyphagous wasp parasitoid,
Hyposoter annulipes (Cresson). In contrast, the
specialist wasp parasitoid, Cotesia congregata (Say),
is much less affected by the sequestered nicotine.
The first step in the chain of events leading to
interactions between an herbivore and its preda-
tors or parasitoids is the location of an herbivore-
containing habitat from a distance by its natural
enemies. Predators and parasitoids are faced with
a great variety of stimuli they may use to locate
their victim, even when considering only one sen-
sory modality, i.e., chemoreception. Both plants
and herbivores produce odors and, thus, potential
information. The appropriateness and usability of
information ultimately depends on two factors (i)
its reliability in indicating herbivore presence,
accessibility and suitability, and (ii) the degree to
which stimuli can be detected. It is assumed that
the use of information that is both reliable and
easy-to-detect enhances searching efficiency and
consequently, Darwinian fitness.
Stimuli derived from the herbivore itself are
generally the most reliable source of information.
Ideally, the infochemicals should reliably tell nat-
ural enemies whether a herbivore is present, to
which species it belongs, whether there is more
than one individual and, if so, how many, whether
it is suitable to be parasitized or eaten, and
whether it is readily accessible or hidden. For
parasitoids, whose host continues to develop, and
for predators that search for an oviposition site,
there is the additional need to know whether the
food plant is suitable for the development of their
offspring. In fact, the more intimate the herbi-
vore-carnivore interaction, the more specific the
information that the carnivore needs.
However, the use of herbivore-derived stimuli
often is limited by low detectability, especially at
longer distances. Stimuli from plants, on the other
hand, are usually more readily available because of
the plants’ relatively larger biomass, but are less
reliable predictors of herbivore presence. Reliabil-
ity of plant cues depends on the predictability of
plant infestation over space and time. So, natural
enemies are challenged to combine the advanta-
geous characteristics of information from both
trophic levels. It has been hypothesized that detect-
ability of stimuli from the second trophic level
puts a major constraint on the evolution of herbi-
vore location by their natural enemies. Natural
enemies may approach the reliability-detectability
problem in three ways (i) by resorting to the use of
infochemicals from herbivore stages different
from the one under attack, that are more conspic-
uous in their infochemical release (infochemical
detour), (ii) by focusing their responses to
­herbivore-induced plant volatiles (HIPV) that
originate from specific interactions of the herbi-
vore and its food, and (iii) by learning to link easy-
to-detect stimuli (plant cues) to reliable but
hard-to-detect stimuli (herbivore cues). Which of
these options is/are employed is dependent on the
ecological context in which the parasitoid has
evolved, and the degree of dietary specialization is
an essential aspect of this.
By using the comparative approach, one can
speculate whether and, if so, how the natural
enemy species’ use of herbivore-induced syn-
omones correlates with their dietary specializa-
tion. The more natural enemies are specialized at
a certain trophic level, the more they innately use
infochemicals from that trophic level. In contrast,
polyphagy at a trophic level is expected to result
in more plastic responses to infochemicals from
that trophic level. Thus, it is hypothesized that (i)
natural enemies that are specialists on specialist
herbivores have strong fixed responses to kai-
romones from their victims, to uninduced plant
volatiles and to HIPV, (ii) natural enemies that
attack several herbivore species on one host plant
species have fixed responses to general kairomone
components shared by the different herbivores
and strong fixed responses to uninduced plant
volatiles and HIPV, (iii) natural enemies that are
specialists on a polyphagous herbivore have

strong fixed responses to kairomones and have to
learn to respond to plant volatiles and HIPV, and
(iv) natural enemies that are extremely polypha-
gous on polyphagous herbivores are not expected
to use infochemicals in finding their prey or hosts.
These four categories are extremes in a contin-
uum. The ecological settings of many natural ene-
mies are intermediates along the continuum. The
way these species use infochemicals will depend
on the relative importance of the diet breadth at
each trophic level.
Relative Importance of Plant and
Natural Enemies to Herbivore
Fitness
Herbivorous arthropods are affected by both their
food plants and by predators and parasitoids. They
have to deal with plant defenses such as toxins and
digestibility reducers, but also with predator
attacks. In general, it seems that there is a wide
variation in effects of plants and natural enemies
on the fitness of herbivores. This has led to specu-
lation on which effects are the most important:
“top-down effects” (effects of natural enemies) or
“bottom-up effects” (effects of plants). The answer
to this question is not likely to receive a general
answer. It seems that the relative importance of the
two effects is dependent on system-specific char-
acteristics and the two effects are integrated, rather
than alternatives.
The discussion about top-down and bottom-
up effects is remarkable with respect to herbivore
specialization. Two main selective forces have
been mentioned: plant secondary chemicals have
long been assumed to be the selective force deter-
mining the high degree of specialization among
herbivores. More recently, natural enemies of her-
bivores have been mentioned as another impor-
tant selective.
The role of toxic plant secondary chemicals
has centered on the so-called “arms race” of plants
and herbivores. Less than 10% of all herbivorous
insects are polyphagous species that feed on plants
Tritrophic Interactions
T 3919
in more than three different plant families. The
high degree of specialization of insect herbivores
usually is explained by the existence of secondary
plant chemicals. However, this has received criti-
cism by L. Bernays and colleagues at the Univer-
sity of Arizona who argue that generalist natural
enemies, especially predators of the herbivores,
may be an important factor in the evolution of
narrow host range. Bernays and colleagues argue
that oviposition choice and/or host utilization
ability can be significantly altered within only
10–16 generations, which implies that current pat-
terns of host use should probably be seen as eco-
logically dyn­amic, and not as an end result of
co-evolutionary processes over millennia. More-
over, host shifts by insects with a restricted host
range often are to unrelated plant species, suggest-
ing that behavioral barriers do not simply reflect a
need to avoid toxins. Plant secondary chemicals
tend to provide the proximate, mechanistic bases
for narrow host range, but do not necessarily pro-
vide the ultimate, functional basis for the patterns
presently seen. An important aspect in their argu-
ments is the concept of “enemy-free space,” which
indicates that, on some plants, an herbivore is not,
or is less, affected by natural enemies compared to
other plant species. Within a given place and time,
preference for a plant less likely to be visited by
natural enemies could evolve rapidly. Specializa-
tions for continued avoidance of predators also
may then be rapidly selected and established. For
example, it is self-evident that the most effective
insect crypsis is developed on specific substrates,
and the most celebrated instances of sequestration
of compounds toxic to vertebrates from plants are
reported for insects with specialized feeding hab-
its. Both of these specializations are predator
related. Because many parasitoids are relatively
restricted in host range, or restricted in the ranges
of plants searched, they might be more important
in causing host switches or broadening herbivore
host range. This could leave the predator element
as the most important factor in pushing insect
herbivores toward narrow host range and the spe-
cializations that can then follow.
3920
T Tritrophic Interactions
The Plant’s Perspective: A Paradox
in Its Defense Against Herbivores
and the Answer in a Tritrophic
Context
The previous section considered the herbivore’s
viewpoint of being in between plant defense and
natural enemy attack. When taking the plant’s
perspective of defense against herbivores, a
bitrophic view may yield a paradox. If plants affect
herbivore fitness by reducing the food quality
through digestibility reducers or nutrient compo-
sition (e.g., low nitrogen content), the herbivores
will respond by inflicting more damage to com-
pensate (e.g., by prolonged feeding, or more
intense feeding). Natural enemy attack may be the
essential factor needed to turn digestibility reduc-
ers into a positive trait. Digestibility reducers
result in longer duration of herbivore stages. This
may affect attacks by parasitoids that are usually
rather restrictive as to the herbivore instar they
attack, or attacks by (insect) predators that con-
sume more small prey than large prey. However,
experimental evidence for this often-mentioned
scenario is still limited.
Plants also may face another dilemma. If the
secondary chemicals the plants produce are
sequestered by specialist herbivores, that means
the herbivores exploit the plant’s defense for their
own protection against carnivores, and the plant
faces a net ecological cost. Many plants only start
the (increased) production of these secondary
metabolites in response to herbivory. A recent
example shows that the induction can be depen-
dent on the herbivore that feeds on the plant. Wild
tobacco plants initiate nicotine production in
response to wounding by such factors as rabbit
feeding or mechanical wounding. However, Kahl
and colleagues at the Max Planck Institute for
Chemical Ecology showed that when caterpillars
of a specialist herbivore, i.e., tobacco hornworm
(M. sexta), feed on the plant, the plant does not
initiate a high nicotine biosynthesis, but rather,
initiates the production of volatiles that attract
carnivorous enemies of the specialist herbivore.
Hidden Players
Currently, tritrophic interactions are mostly con-
sidered for above-ground interactions of plants,
and herbivorous and carnivorous arthropods.
However, it is increasingly apparent that microor-
ganisms play an important role in communities in
general, and in plant-insect communities in par-
ticular. Microorganisms may compete with insects
for food, and microorganisms may be symbionts or
pathogens of insects. Therefore, all interactions in
tritrophic systems can be affected by microorgan-
isms. Research in this area is rapidly increasing.
Moreover, most knowledge on tritrophic inter-
actions relates to above-ground systems, especially
because they are more easily investigated than
below-ground interactions. However, above-
ground and below-ground interactions cannot be
considered individually because they are intimately
linked. Intensified research on below-ground inter-
actions, as well as their link to above-ground
­interactions, is foreseen for the near future.
Theories on Plant Defense
Classical plant defense theory describes the evolu-
tion of secondary plant substances in direct
defense against herbivores as the result of an arms
race between plants and herbivores: plants evolve
secondary metabolites in response to attacks by
insects, while insects meet the challenge by evolv-
ing new detoxification systems. In the 1970s,
P. Feeny of Cornell University, and D. Rhoades and
R. Cates at the University of Washington, devel-
oped a theory that centers on plant “apparency,”
which emphasizes the herbivore’s perspective. A
third plant defense theory is the “resource avail-
ability theory,” developed by P. Coley and col-
leagues at the University of Utah. This theory
emphasizes the plant’s perspective and centers
around the possibilities of defense as affected by
the availability of nutrients and energy.
The relatively young field of three-trophic-
level interactions has not been the subject of many

theoretical considerations. Yet, Price at Northern
Arizona University has integrated the plant appar-
ency theory with the actions of natural enemies
(indirect defense). He argues that many of the
broad patterns relating to natural enemies discov-
ered to date relate to gradients from herbs to
shrubs to trees, from unstable to stable environ-
ments, and from herbivores with external to con-
cealed feeding habits. When using plant succession
as a starting point, and concentrating on parasi-
toids as natural enemies, Price notes five patterns:
1.  With plant succession, the number of parasitoid
species per host species increases.
2.  With plant succession, the prevalent parasitoid spe-
cies becomes more generalistic.
3.  With an increase in the number of parasitoid spe-
cies per host species, host mortality increases; this
has not been well-studied.
4.  With an increase of the number of parasitoid spe-
cies per host species, the probability increases that
herbivore populations are regulated.
5.  Host-specific parasitoids (that are more often pres-
ent in early succession stages) have innate and
strong responses to kairomones and plant vola-
tiles, whereas generalistic species (more frequently
present in later successional stages) have more
plastic responses that are subject to learning.
Price then theorizes on the differences in
plant defenses in early and late succession. In
early succession, plants are unapparent to herbi-
vores and defend themselves through specific tox-
ins. Thus, host location by parasitoids is constrained
and the parasitoids need specialized enzymes to
cope with the sequestered toxins in the herbivores.
Thus, selection will favor specificity of the parasi-
toids. It is exactly host-specific parasitoids that are
predicted to use specific synomones and kai-
romones in host location in a genetically fixed pat-
tern. In late succession, plants are apparent and
defend themselves in similar ways (convergence)
through digestibility reducers. This increases the
chance that an herbivore will include a new plant
species in its diet; herbivores are less plant-specific.
Tritrophic Interactions
T 3921
Parasitoid species may be more generalistic than
in early successional stages. For these parasitoids,
the recognition of, and innate response to, a large
number of specific synomones and kairomones is
less likely (physiological constraint) and, thus,
learning will be more important.
Applied Aspects
The importance of considering interactions between
insects and their food and enemies in a multitrop-
hic context has been realized since the beginning of
the 1980s. Thus, the field of tritrophic interactions is
a relatively young one. However, developments in
this field are quick and the knowledge gained is not
only important from a scientific point of view, but
also from an applied point of view. For instance, in
environmentally benign pest control, herbivores
can be controlled through plant breeding for resis-
tance and through biological control (Fig. 105). The
combination of these two methods may be explic-
itly exploited, or may occur without special inter-
vention, because naturally occurring, carnivorous
arthropods often play an important, but unnoticed,
role in the reduction of pest populations. Therefore,
it is important that these two methods are synergis-
tic rather than antagonistic. However, synergistic
interaction between host plant resistance and bio-
logical control is by no means self-evident. If cer-
tain plant characteristics are selected because they
have a negative influence on herbivores in the
absence of biological control agents, this does not
automatically mean that the plant contributes to
pest control in the presence of biological control
agents. A remarkable example was recorded for
cabbage plants. Two cabbage varieties differed in
resistance against the cabbage aphid, Brevicoryne
brassicae (L.), which resulted in reduced aphid pop-
ulations when parasitoids had been excluded. How-
ever, the susceptible cultivar emitted larger quantities
of a parasitoid-attracting volatile and, therefore,
under conditions where biological control was
applied, aphid densities were lower on the suscep-
tible variety than on the resistant variety.
3922
T Tritrophic Interactions
Natural enemy of herbivore
Biological control
Herbivore +,−,or 0
Host plant resistance
Plant
Tritrophic Interactions, Figure 105  Durable and
environmentally benign pest management can
incorporate host plant resistance and ­biological
control. Host plant ­characteristics may affect
biological control positively, negatively, or not
at all. Which of these interactions between host
plant resistance and biological control occurs can
be ­important for the success of environmentally
benign pest control.
Along similar lines, current developments
should be considered in the field of transgenic
insect-resistant plants. So far, the main emphasis
is on the effects of the transgenic plants on pest
insects, without much emphasis on tritrophic
effects. However, an important question is: Do
plants that have been engineered to express cer-
tain toxins affect non-target organisms, includ-
ing non-target herbivores and carnivorous
arthropods that attack target and/or non-target
herbivores?
Agricultural plants have to produce under
conditions where they are members of a com-
munity. Agroecosystems harbor a diverse
­community – even when they are usually less
diverse than the community in a natural ecosys-
tem – and if important carnivores are eliminated
or hampered by introducing crop plants that
have different characteristics, the result may be
that pest control is hampered rather than
improved. This is a lesson that is older than the
research on tritrophic interactions. The dusting
of crop plants with broad-spectrum pesticides in
the 1960s and 1970s can be seen as an artificial
alteration of plant characteristics that had severe
impacts on pest control, where even novel pests
were induced as a result of the elimination of
carnivorous arthropods.
Conclusion
Interactions in communities comprise direct and
indirect interactions. Characteristics of commu-
nity members can have effects on interactions
with their direct enemies or resources, but also
on non-producer/consumer interactions. Indi-
rect interactions are by no means less important
than direct interactions between producers and
consumers. Indirect interactions can decisively
influence producer-consumer interactions. Tri-
trophic interactions show that the debate on the
role of bottom-up versus top-down forces in
shaping communities is not an either/or debate,
but rather one of the degree of integration of the
two forces. Considering tritrophic interactions is
not only interesting from a basic point of view, it
is also important from an applied point of view
(for example, in developing novel methods of
environmentally benign pest control). Finally,
the study of tritrophic interactions is not an end-
point but only a beginning. After initiating stud-
ies on interactions among plants, herbivores and
carnivores (not exclusively insects), it is now clear
that microorganisms can play important roles in
these interactions. Moreover, second-order car-
nivores and interactions with organisms that
cannot be exclusively linked to a single trophic
level, such as omnivores, should be included as
well. Therefore, the study of tritrophic interac-
tions is evolving into the research area of multi-
trophic interactions.
References
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aspects of insect–plant interactions. Wiley, New York,
pp 201–229
 Trogidae
T 3923

Bernays E, Graham M (1988) On the evolution of host Triunguloid Larva

specificity in phytophagous arthropods. Ecology
69:888–892
Chadwick DJ, Goode JA (eds) (1999) Insect–plant interac- A larval body form with minute, active, spiny
tions and induced plant defense. Novartis Found Symp first instars, and found in certain predaceous
223. Wiley, Chichester beetles and stylopids.
Dicke M (1999) Direct and indirect effects of plants on
­performance of beneficial organisms. In: Ruberson JR  Triungulin
(ed) Handbook of pest management. Marcel Dekker,
New York, pp 105–153
Dicke M (1999) Evolution of induced indirect defense of
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evolution of inducible defenses. Princeton University
Trochanter
Press, Princeton, NJ, pp 62–88
Groot AT, Dicke M (2002) Insect-resistant transgenic plants A small leg segment found between the coxa
in a multitrophic context. Plant J 31:387–406 and femur. The second segment of the leg
Hilker M, Meiners T (2002) Induction of plant responses
towards oviposition and feeding of herbivorous arthro-
(Fig. 106).
pods: a comparison. Entomol Exp Appl 104:181–192  Legs of Hexapods
Karban R, Baldwin IT (1997) Induced responses to herbivory.
Chicago University Press, Chicago
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN,
Weis AE (1980) Interactions among three trophic levels:
influence of plant on interactions between insect herbi- Trochantin
vores and natural enemies. Annu Rev Ecol Syst
11:41–65 The basal part of the trochanter when it is sub-
Price PW (1991) Evolutionary theory of host and parasitoid
divided. In Coleoptera and some other groups,
interactions. Biol Control 1:83–93
Turlings TCJ, Loughrin JH, McCall PJ, Rose USR, Lewis WJ, it refers to a structure present on the outer side
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protect themselves by attracting parasitic wasps. Proc
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van Emden HF (1986) The interaction of plant resistance A family of chewing lice (order Phthiraptera).
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 Chewing and Sucking Lice
Interactions of plant resistance and parasitoids and
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Troctopsocidae
mol 37:141–172
A family of psocids (order Psocoptera).
 Bark-Lice, Book-Lice and Psocids

Triungulin
The active first instar of stylopids (Strepsiptera) Trogidae
and certain beetles (Coleoptera) that undergo
hypermetamorphosis, becoming less active after A family of beetles (order Coleoptera). They com-
they find a host and commence feeding (contrast monly are known as skin beetles.
with planidium).  Beetles
3924
T Trogiidae

2
Hidden true
3
segment
4

Coxa 5
Trochanter
Femur
Tibia

4 5
1 2 3
Pretarsus
Tarsus

Trochanter, Figure 106  Leg of a beetle (Coleoptera: Scarabaeidae) leg showing its c­ omponent parts, and
a close-up of one type of beetle tarsus (foot).

Trogiidae principal component. However, insects also are

carnivores, parasites, and detritivores, so they
A family of psocids (order Psocoptera). appear in various tropic levels (Table 15).
 Bark-Lice, Book-Lice and Psocids

Trophallaxis Trophic Structure

A behavior found in social insects involving the
exchange of food between members of the col-
ony, or among colony members and guests. The
food may originate from the mouth (stomodeal
trophallaxis) or from the anus (proctodeal
trophallaxis).
Trophic Egg
A degenerate egg that is inviable, and used to feed
other members of the colony.
Organization of a community in terms of energy
flow through the constituent trophic levels.
Trophobiosis
The indirect stimulation of reproduction through
plant conditioning following the host plant’s expo-
sure to insecticides. Normally the insecticide
affects the nutrient condition in a favorable man-
ner. This phenomenon is best documented in
aphids.

Trophic Level
The classification of organisms in a community
according to their feeding relationships. The first
trophic level usually is green plants. The second
tropic level includes herbivores, and insects are a
Trophogenic Polymorphism
Polymorphism in social insects due to differential
feeding of the larvae, or different sized eggs.
 Tropical Carpenterworm Moths (Lepidoptera: Metarbelidae)
T 3925

Trophic Level, Table 15  Trophic relationships of some insect orders

Primary consumers Secondary consumers (insectivores and Decomposers
(herbivores) carnivores)
Coleoptera (some) Coleoptera (some) Coleoptera (some)
Diptera (some) Diptera (some) Diptera (some)
Embiidina Ephemeroptera (some) Ephemeroptera (some)
Grylloblattodea Hemiptera (some) Isoptera
Hemiptera (some) Hymenoptera (SimpleParasitic and Plecoptera (some)
provisioning wasps)
Hymenoptera (sawflies, horn- Mallophaga  
tails, some bees)
Mecoptera Mantodea  
Lepidoptera Megaloptera  
Orthoptera Neuroptera  
Phasmatodea Odonata  
Thysanoptera (most) Plecoptera (some)  
  Raphidioptera  
  Siphunculata  
  Thysanoptera (some)  
  Trichoptera  

Tropical Burnet Moths with concealed head. Host plants include families
(Lepidoptera: Lacturidae) ­Celastraceae, Moraceae, and Sapotaceae.

John B. Heppner References

Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tropical burnet moths, family Lacturidae, total 138
species, mostly Indo-Australian but with a few in the
southern United States; actual world fauna probably
exceeds 250 species. The family is in the superfamily
Sesioidea in the section Tineina, subsection Sesiina,
of the division Ditrysia. Adults small to medium size
(11–65  mm wingspan), with head scaling average;
haustellum naked; labial palpi upcurved; maxillary
palpi small, 1- to 2-segmented; antennae filiform.
Wings elongated. Maculation usually colorful, espe-
cially with orange, red and yellow colors, and with
various bands or spots, and with darker hindwings.
Adults nocturnal but some may be crepuscular.
­Larvae are leaf skeletonizers and are colorful, but
most are not known biologically; somewhat ­slug-like,
Busck A (1913) Notes on the genus Mieza Walker, with
descriptions of three new species from Costa Rica.
Insecutor Inscitiae Menstruus 1:70–73
Common IFB (1990) Family Zygaenidae (burnets, foresters)
[part]. In: Common IFB, Moths of Australia. Melbourne
University Press, Carlton, pp 294–299
Heppner JB (1995) Lacturidae, new family (Lepidoptera:
Zygaenoidea). Trop Lepidoptera 6:146–148
Tropical Carpenterworm Moths
(Lepidoptera: Metarbelidae)
John B. Heppner
Florida State Collection of Arthropods,
Gainesville, FL, USA
Tropical carpenterworm moths, family Metarbeli-
dae, include 103 species, mainly Afrotropical and
3926
T Tropical Ermine Moths (Lepidoptera: Attevidae)
Oriental, with one species in the Palearctic region;
actual world fauna likely exceeds 150 species. The
family is in the superfamily Cossoidea (series Cos-
siformes) in the section Cossina, subsection
Cossina, of the division Ditrysia. Some recent views
place the group as a subfamily of Cossidae. Adults
small to medium size (21–48 mm), with head small
and rough scaled; labial palpi upcurved; maxillary
palpi minute; antennae short and bipectinate; legs
short. Body robust. Wings elongated and rounded
(frenulum-retinaculum usually absent). Macula-
tion mostly shades of brown and gray, even nearly
white background, with dark spotting (often also
with a preapical darker forewing discal spot); hind-
wings darker. Adults may be crepuscular. Larvae
nocturnal borers on tree bark or in tree trunks, but
most species remain unknown biologically. Host
plants include various trees in Anacardiaceae, Gut-
tiferae, Lauraceae, Leguminosae, Myrtaceae, Rham-
naceae, Rutaceae, Sapindaceae, and Sterculiaceae.
A few have minor economic status.
References
Dalla Torre KW, von Strand E (1923) Lepidarbelidae. Lepi-
dopterorum Catalogus, 28:1–14 [part]. W. Junk, Berlin
Holloway JD (1986) Family Metarbelidae. In: Moths of Bor-
neo, 1:42–46, pl. 4. Malayan Nature Society, Kuala Lum-
pur (Malayan Nat J 40:42–46, pl. 4)
Janse AJT (1925) A revision of the South African Metarbeli-
dae. S Afr J Nat Hist 5:61–100, pl. 4–8
Seitz A (1929) Familie: Indarbelidae. Die Gross-Schmetter-
linge der Erde, 10:803–806, pl. 93 (1933); 14:501–513, pl.
78 (1929). A. Kernen, Stuttgart
Srivastava AS (1962) A preliminary study of the life-history
and control of Indarbela quadrinotata Wlk. (Metarbeli-
dae: Lepidoptera). Proc Natl Acad Sci India
328:265–270
Tropical Ermine Moths
(Lepidoptera: Attevidae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tropical ermine moths, family Attevidae, include
48 species, mostly tropical and in the genus Atteva
(the single partially non-tropical species known
occurs across the southern United States and into
the Caribbean and Mexico); actual fauna probably
at least 60 species. The family is part of the super-
family Yponomeutoidea in the section Tineina,
subsection Tineina, of the division Ditrysia. Adults
small to medium size (20–34 mm wingspan), with
head smooth-scaled; haustellum naked; labial
palpi upcurved; maxillary palpi 1- to 2-segmented.
Wings elongated with termens rather rounded.
Maculation usually colorful (many with red or
orange forewings), with various spots on the fore-
wings (Fig.  107). Adults diurnal or crepuscular.
Larvae are leaf webbers and leaf skeletonizers on
Araliaceae and Simaroubaceae. Minor economic
species occur on Ailanthus trees in India and the
United States.
References
Clarke JFG (1965) Atteva Walker. In: Clarke JFG,
Hyponomeutidae [sic], in Catalogue of the type speci-
mens of Microlepidoptera in the British Museum (Nat-
ural History) described by Edward Meyrick, 5: 292–293.
British Museum (Natural History), London
Mathur RN (1960) Setal arrangement of Atteva fabriciella
Swederus (Yponomeutidae, Lepidoptera). Indian J Ento-
mol 21:1–5
Powell JA, Comstock JA, Harbison CF (1973) Biology, geo-
graphical distribution, and status of Atteva exquisita
(Lepidoptera: Yponomeutidae). Trans San Diego Soc
Nat Hist 17:175–186
Taylor OR (1967) Relationship of multiple mating in Atteva
punctella (Lepidoptera: Yponomeutidae). Ann Entomol
Soc Am 60:583–590
Tropical Fruit Pests and their
Management
Jorge E. Peña
University of Florida, Homestead, FL, USA
Tropical fruits are important in several produc-
tion areas of south and southeast Asia, Australia,

Tropical Ermine Moths (Lepidoptera: Attevidae),
Figure 107  Example of tropical ermine moths
­(Attevidae), Atteva niveigutta Walker from India.
Africa, the Mediterranean, the Americas and the
Caribbean region. Tropical fruits are regularly
grown in different climates from latitude 23°27”N
to 23°27”S of the equator, while some are grown
to approximately 37°N in Spain. Proximity to the
sea, sea currents, altitude, direction of prevailing
winds, rainfall and air humidity all have modify-
ing effects on these crops. Most tropical fruits are
perennial plants which persist for several years
without abrupt, major changes other than sea-
sonal leaf formation, flowering, and fruit develop-
ment. However, pineapple, papaya, and passion
fruit are grown for shorter periods of time and
their arthropod management is influenced by
their persistence in the field.
In general, tropical fruit crops provide a rel-
atively stable environment over many years,
offering continuing habitats for both pests and
natural enemies and providing opportunities for
biological control and effective pest manage-
ment programs. Avocado, mango, pineapple,
banana, passion fruit, litchi, guava, Annona spp.,
durian, mangosteen, rambutan, acerola and car-
ambola, and their most common pests are
included here.
Annona Fruits (Annonaceae Family)
The genus Annona embraces several valuable fruit
trees and is centered in the Neotropics, with
about 110 species. The most common species are
Tropical Fruit Pests and their Management
T 3927
A. muricata L., A. montana McFadden, A. glabra L.,
A. cherimola P. Miller, A. squamosa L., A. reticu­
lata L., and A. longiflora Watts. Fruits of Annona
are fleshy aggregates that arise from coalesced car-
pels and contain large seeds with reticulate
endosperm.
Most species of Annona have specific climatic
requirements for growth, flowering, and fruit mat-
uration. The origins of the tropical species, such as
the sugar apple (A. squamosa), are the warm low-
land regions of Brazil, Guyana, Venezuela, Mexico,
and the West Indies. A distinctly subtropical spe-
cies is the cherimoya (A. cherimola), which origi-
nates from the cool Andean valleys of Peru and
Ecuador at elevations of around 2,000  m. The
hybrid atemoya (A. cherimola  ×  A. squamosa),
which appeared spontaneously when parent trees
were cultivated side by side and also through man-
ual pollination, exhibits intermediate climatic
requirements for growth and fruiting.
Within the family Annonaceae, fruits of the
cherimoya, sugar apple, atemoya, and soursop
(A. muricata) have the greatest potential for uti-
lization and export in the American, Caribbean,
Asian and Australian countries. Much of the
production of commercially grown species has
spread from their indigenous areas to tropical
and subtropical parts of Australia, New Zealand,
Asia and around the Mediterranean. Thus, pro-
duction methods vary from more sophisticated
systems to less intensive, small farm or backyard
type production. The key pests are the annona
seed borers, Bephratelloides spp., B. cubensis
(Ashmead), B. pomorum, B. paraguayensis
(Crawford), and B. petiolatus Grissell and
Schauff (Hymenoptera: Eurytomidae), destroy-
ing seeds and pulp; fruit borers, Cerconota anon­
ella Sepp (Lepidoptera: Oecophoridae), Talponia
batesi Heinrich (Lepidoptera: Tortricidae) and
Thecla ortyginus (Lepidoptera: Lycaenidae); fruit
flies, the Queensland fruit fly, Bactrocera tryoni
(Froggatt), Anastrepha spp., and Ceratitis capi­
tata (Diptera: Tephritidae); and recently, the
pink hibiscus mealybug, Maconellicoccus hirsu­
tus (Green), causing defoliation.
3928
T Tropical Fruit Pests and their Management
Avocado, Persea americana Mill.
(Lauraceae family)
The avocado, Persea americana Mill. (Lauraceae),
is of Central American origin and well known to
the native inhabitants of Mexico, Central America
and northern South America. Today, avocado is
grown commercially not only in North America
and throughout tropical America and the larger
islands of the Caribbean, but also in Polynesia, the
Philippines, Australia, New Zealand, Madagascar,
Mauritius, Madeira, the Canary Islands, Algeria,
tropical Africa, South Africa, southern Spain, south-
ern France, Sicily, Crete, Israel and Egypt. The
most important pests include the tea red mite,
Oligonychus coffeae (Nietner), avocado brown
mite, Oligonychus punicae (Hirst), the persea mite,
Oligonychus perseae (Tuttle, Baker and Abbatiello),
and the avocado red mite, Oligonychus yothersi
(McGregor) (Acari: Tetranychidae), as well as the
eriophyid mite Tegolophus perseaeflorae (Keifer)
(Acari: Eriophyidae). Severe damage to the leaves
can be produced by the psyllids Trioza anceps
Tuthil and Trioza perseae Tuthill (Hemiptera:
Psyllidae), and by the large blacktip wilter, Anop­
locnemis curvipes F., injuring new flush, and by
the leaffooted bugs, Amblypelta nitida Stål and
A. lutescens lutescens (Distant) (Hemiptera: Cor-
eidae), attacking fruits. Other important species
are the avocado lace bug, Pseudacysta perseae
(Heidemann) (Hemiptera: Tingidae) (Fig.  108),
causing leaf chlorosis and necrosis, the mirids,
Dagbertus fasciatus (Reuter), D. olivaceous (Reuter),
and Rhinacloa sp. (Heteroptera: Miridae), affect-
ing flowers and fruitlets, the thrips, Scirtothrips
aguacatae  Johansen and Mojica and Scirtothrips
kupae Johansen and Mojica, Scirtothrips perseae
­Nakahara, the red-banded thrips, Selenothrips
rubrocinctus (Giard) (Thysanoptera: Thripidae),
affecting leaves and sometimes fruits. Among lep-
idopterans, several species affect production,
including the avocado seed moth, Stenoma cateni­
fer Walsingham (Lepidoptera: Oecophoridae), the
western avocado leaf roller, Amorbia cuneana
Walsingham (Lepidoptera: Tortricidae), and the
avocado loopers Anacamptodes defectaria
(Guenée), Epimeces detexta (Walker), Epimeces
matronaria (Guenée), Oxydia vesulia transponens
(Walker), and Sabulodes aegrotata Guenée (Lepi-
doptera: Geometridae), which consume foliage
and eventually chewing on small fruit.
Other important pests are the weevils,
Conotrachelus perseae Barber, Conotrachelus agua­
catae Barber, Conotrachelus serpentinas (Klug) and
Heilipus lauri Bohemann (Coleoptera: Curculion-
idae), boring into fruits and seeds.
Banana and Plantain, Musa spp.
(Musaceae Family)
Bananas and plantains (Musa spp.) are among the
most important crops in tropical and subtropical
climates. The genus Musa evolved in Southeast
Asia where numerous undomesticated Musa spe-
cies still grow as opportunistic weeds. Edible
bananas (Musa spp., Eumusa series) originated
within this region from two wild progenitors, Musa
acuminata and M. balbisiana, producing a series of
diploids, triploids and tetraploids through natural
hybridization. Additionally, man has selected for
parthenocarpy (development of fruit without pol-
lination or seeds). Hybridized bananas may be
divided into six genome groups (i.e., AA, AAA,
AAB, AB, ABB, ABBB) based on the relative contri-
butions of M. acuminata and M. balbisiana. Domes-
ticated bananas include a wide range of dessert,
cooking and brewing cultivars. The most exten-
sively grown bananas are triploids. In terms of
gross value of production, bananas and plantains
are the fourth most important global food crop.
Bananas grown for export are almost exclusively of
one variety, “Cavendish”; this cultivar accounts for
slightly more than 10% of global production.
Bananas are rhizomatous herbaceous plants rang-
ing in height from 0.8 to 15  m. A mat (=banana
stool) consists of an underground corm (rhizome)
from which one or more plants (shoots) emerge.
Adventitious roots spread extensively 4–5 m from
the parent and downward 75 cm or more; however,
 Tropical Fruit Pests and their Management
T 3929

Tropical Fruit Pests and their Management, Figure 108  Some tropical fruit pests: upper left, banana
weevil larva (photo Rita Duncan); upper right, papaya fruit fly ­(photo R. Swanson); second row left,
­papaya scale (photo M. Shepard); second row right, papaya ­leafhopper (photo Rita Duncan); third row
left, ­Annona seed borer (photo H. Nadel); third row right, a
­ vocado lacebug (photo J. Peña); bottom left,
­Caribbean fruit fly (photo Rita Duncan); bottom right, Acerola weevil larva (photo Rita Duncan).
3930
T Tropical Fruit Pests and their Management
most roots are near the soil surface. Plants repre-
sent a single shoot (pseudostem, stem, leaves, flower
and bunch). Yield is normally expressed in kg/area/
year reflecting both number and size of bunches
harvested.
Pests of the corm and pseudostem include
the banana weevil, Cosmopolites sordidus (Ger-
mar), banana pseudostem borer, Odoiporous lon­
gicollis (Olivier) and the West Indian sugarcane
borer, Metamasius hemipterus sericeus (Olivier)
(Coleoptera: Curculionidae). The following are
pests of flowers and fruits: banana thrips Herci­
nothrips bicinctus (Bagnall), Caliothrips bicinctus
Bagnall, Chaetanaphothrips orchidii (Moulton),
C. signipennis (Bagnall), Thrips hawaiiensis
(Morgan) and Tryphactothrips lineatus Hood
(Thysanoptera: Thripidae), while the banana
fruit scarring beetles, Colaspis hypochlora Lefebre
(Coleoptera: Chrysomelidae) and the “Irapua”
bee, Trigona spinipes Fabricius (Hymenoptera:
Apidae), are considered troublesome in some
areas in the Neotropics. The banana moths,
Opogona sacchari Bojer, Opogona glyciphaga
(Meyrick) (Lepidoptera: Tineidae), the banana
scab moth, Nacoleia (Notarcha, Lamprosema)
octasema (Lepidoptera: Pyralidae) damage flow-
ers and sometimes bunches. Important pests of
foliage include the bagworm, Oiketikus kirbyi
Guilding (Lepidoptera: Psychidae), Caligo spp.,
Opsiphanes spp. (Lepidoptera: Nymphalidae).
The banana aphid, Pentalonia nigronervosa
Coquerel. (Heteroptera: Aphidae) is important
as the sole vector of the bunchy-top disease.
Barbados Cherry or Acerola,
Malpighia glabra (L.)
(Malpighiaceae Family)
Barbados cherry is a tropical fruit native to
the  West Indies, Central America, and South
America. Recently, the Barbados cherry has
received attention because its fruits are excep-
tionally high natural source of ascorbic acid
(vitamin C). Its cultivation has extended
throughout the subtropics and tropics and some
of the largest plantings are in Brazil. Estimated
commercial acreage in the Caribbean region is
more than 400 acres with a potential crop value
of several million U.S. dollars. Flowering and
fruit set occurs almost continuously from April
through November in Florida, and fruits mature
in approximately 30 days. Acerola’s most impor-
tant pests are the acerola weevil, Anthonomus
macromalus Gyllenhal (=A. flavus, =A. bidenta­
tus, =A. malpighia) (Coleoptera: Curculionidae),
injuring fruits and flowers; fruit flies, Anastrepha
spp., and the Mediterranean fruit fly, Ceratitis
capitata Wiedemann (Diptera: Tephritidae), and
the coreids, Leptoglossus spp., Crinocerus spp.
(Hemiptera: Coreidae), and the stink bug, Nezara
viridula L (Hemiptera: Pentatomidae), causing
fruit deformation.
Carambola, Averrhoa carambola
L. (Oxalidaceae Family)
Known as carambola, star apple, or five corner,
this fruit tree is a 5–12  m high evergreen tree
native to southern Asia. Leaves imparipinnate,
flowers in axillary or cauliflorous panicles, pen-
tamerous. The fruit is a large berry, ovoid to ellip-
soid in outline, with five pronounced ribs, stelate
in cross section. The tree grows well in tropical
or subtropical lowland conditions and flowers
abundantly. Most of the information on pests of
carambola comes from southeastern Asia and
­Australia. Important arthropods include the car-
ambola fruit fly, Bactrocera carambolae Drew and
Hancock (Diptera: Tephritidae), whose larvae
feed on the fruit and make tunnels in the fruit;
fruit piercing moths, Gonodonta spp. and Eudo­
cima spp. (Lepidoptera: Noctuidae), pierce the
skin of the ripe or ripening fruit with their strong
proboscis, the damage resulting in crop loss or
unmarketable fruit; the armored scale, Morgan­
ella longispina (Morgan) (Hemiptera: Diaspidi-
dae), feeds on buds and bark causing severe die
back; the stink bug, Nezara viridula (L.), extracts

fruit fluids leaving a small puncture and eventual
fruit deformation; and the false spider mite,
Brevivalpus phoenicis (Geijskes) (Acarina: Tenu-
ipalpidae), causes bronzing of the fruit.
Durian, Durio zibethinus Murray
(Bombacaceae Family)
Durian, a common fruit in Southeast Asia, origi-
nated in Borneo and Sumatra, and is held in high
esteem from Sri Lanka and southern India to
New Guinea. The ripe fruits, or rather the arils
which form the edible part, are generally eaten
fresh. Its strong and unmistakable smell is pres-
ent in every market and street stall during the
fruiting season. The fruit also can be preserved,
deep frozen or consumed in ice creams, cakes
and cookies. The fruit is a globose, ovoid or ellip-
soid capsule, up to 25 cm long and 20 cm diam-
eter, green to brownish, covered with numerous
broadly pyramidal, sharp, up to 1-cm-long
spines; usually with five thick, fibrous valves.
Seeds are up to 4 cm long and completely cov-
ered by a white or yellowish, soft, very sweet aril.
The tree is propagated by seeds, or superior cul-
tivars by budding on seeding stock. Thailand is
the largest producer with 444,500 tons in 1987,
followed by Indonesia.
The key pests of durian are Hypomeces squa­
mosus F. (Coleoptera: Curculionidae), a polypha-
gous weevil in which the adult stage feeds on
leaves, causing extensive defoliation of young
plants; the durian psyllid, Allocaridara malayensis
(Crawford) (Hemiptera: Psyllidae), inserts eggs
into young leaves, and both nymphs and adults
feed on the underside of the leaf; the durian borer,
Conogethes punctiferalis (Guenée) (Lepidoptera:
Pyralidae), damages both young and mature fruits
by boring into the pulp. The newly hatched larva
of the durian seed borer, Mudaria luteileprosa
Holloway (Lepidoptera: Noctuidae), feeds initially
on the skin of the fruit and later bores into the
husk and then into the seeds. The mite Eutetrany­
chus africanus (Tucker) (Acari: Tetranychidae)
Tropical Fruit Pests and their Management
T 3931
feeds on the upper side of the leaf, especially along
the mid-vein, causing withering spots that later
spread over the whole leaf.
Guava, Psidium guajava L.
(Myrtaceae Family)
The guava, Psidium guajava L., occurs naturally
from southern Mexico to South America and the
Caribbean. The guava is a small tree that is grown
worldwide in the tropics and warm subtropics for
its edible fruit. Guavas can flower and bear fruit
continuously in the tropics, however, there are
normally two crops a year. In Florida and Puerto
Rico, there is a large crop in early to mid-summer
(June and July), and a smaller crop in late winter
(February). In Hawaii, the small harvest peak
occurs in April to May and the heavy peak in
­September and November. In India and Malaysia,
the main crop is in mid-winter and the lesser crop
during the rainy season (July–September). Fruits
mature 90–150 days after flowering depending on
the variety or clone of the fruit and cultural and
weather conditions. The large white flowers attract
a large variety of pollinating insects including
many species of bees. In many tropical regions the
honey bee, Apis mellifera L., is the most important
pollinator species.
Guavas are either eaten fresh, or used in juice,
ice cream, jellies, pastes or preserves. Key pests
involve fruit flies of the genera Anastrepha and
Bactrocera, and several species of fruit boring wee-
vils, such as Conotrachelus psidii Marshall. Fruit
flies injure the fruit by ovipositing eggs and the
developing larvae consume the pulp, leaving the
fruit unmarketable. A secondary pest is Heliopeltis
theobromae Miller (Miridae), which feeds on many
parts of the plant, including the fruit. Damage
to the fruit results in necrotic lesions which render
the fruit unmarketable. Many species of mealy-
bugs, including Ferrisia virgata (Cockerell), Plano­
coccus citri (Risso), Planococcus pacificus Cox,
Pseudococcus citriculus Cox, Pseudococcus nipae,
Planococcus minor (Maskell), and Pseudococcus
3932
T Tropical Fruit Pests and their Management
lilacinus Cockerell affect guava. Normally these
insects do not damage the host severely, but large
populations cause the fruit to become misshapen
and deformed. For instance, honeydew produced
by mealybugs often results in sooty mold, which
lowers the fruit’s market value. The red-banded
thrips, Selenothrips rubrocinctus (Giard) and Scir­
tothrips dorsalis Hood, also attack guavas by feed-
ing on the leaves and fruit and cause russetting or
bronzing of the plant surface.
Mites can cause serious damage, and they
include Oligonychus yothersi (McGregor), Panony­
chus sp., Eotetranychus sp., and Oligonychus biha­
rensis (Hirst). These mites are reported to feed on
leaves, causing leaves to become dull green, and
then bronzed. The mites, Tegolophus guavae and
Brevipalpus spp., cause damage to fruits and ten-
der leaves.
Litchi and Longan (Sapindaceae
Family)
The litchi (Litchi chinensis Sonn.) and longan
(Dimocarpus longan Lour.) are closely related spe-
cies belonging to the family Sapindaceae. Of
Southeast Asian origin, they thrive in subtropical
areas with cool dry winters and warm wet sum-
mers, but may be grown in tropical areas at high
elevation. Around the world, litchis have been suc-
cessfully grown commercially in latitudes from
15° to 35°. The litchi is a traditional fruit in China,
and it occupies a special place in Chinese culture.
Indo–China is the center of origin for this species
and many old specimen trees have been identified.
Litchi and longan fruits are best when eaten fresh,
but they also can be processed by canning, juicing
or drying into litchi nuts. In Asia they are usually
harvested as whole panicles in order to maintain
freshness, and are sold in street markets or at road-
side stalls within a few days of harvest.
Apart from China and India, large litchi
industries have been developed in Taiwan, Thailand,
Vietnam, Madagascar, South Africa and Réunion.
Smaller but expanding industries exist in ­Australia,
Bangladesh, Mauritius, Mexico, the Seychelles,
Spain and the USA (California, Florida and
Hawaii).
In general, longans can be grown successfully
wherever litchis are cultivated. Although both
­species flower at about the same time, longans
take longer than litchis to mature. Major world
­producers are China (400,000  tons), Thailand
(150,000 tons) and Vietnam (20,000 tons).
Litchi and longan are adapted to the warm
subtropics and produce the best crops when win-
ters are short, dry and cool, but frost-free. Such
climatic conditions initiate the development of
flower panicles. The inflorescences emerge during
late winter and the flowers open in early spring.
Most cultivars set fruit far in excess of what an
individual tree can carry through to maturity and
will shed the excess at various times during fruit
development. Longan flowers about 2–3  weeks
later than litchi, and matures 4–8  weeks later.
­Harvesting fruit as whole panicles has the effect of
pruning and stimulates new leaf growth after har-
vest. It also reduces tree size. Ideally, trees should
produce one or two vegetative flushes after har-
vest. The aim is to have the second or third flush
commence in winter. If conditions are cool during
the early part of the flush, development of the new
growth will be floral. However, if warm weather is
encountered, the new growth will produce leaves.
Litchi and longan often are cultivated in the same
geographical areas, and many pests are common
to both crops.
Pests include the fruit borers Conopomorpha
sinensis Bradley, Conopomorpha litchiella Bradley
(Lepidoptera: Gracillariidae), Cryptophlebia
peltastica Meyr., Cryptophlebia leucotreta Meyr.,
Cry­ptophlebia bactrachopa Meyr. (Lepidoptera:
Tortricidae), and in the New World, Crocidosema n. sp.
(Lepidoptera: Tortricidae). These insects lay new
eggs on the fruit anytime after fruit set, as well as
on new leaves and shoots. Larvae can bore into
leaf buds and fruits. Fruit-piercing moths (Lepi-
doptera: Noctuidae) attack a range of fruits
throughout Southeast Asia, the South Pacific and
Australia. The larvae of fruit-piercing moths

develop on a variety of host plants. In the Pacific
Islands, Eudocima (Othreis) fullonia (Clerck),
Eudocima salaminia (Cramer) and Eudocima
­jordani (Holland) are primary feeders on litchi
fruit on the wet tropical coast of Queensland in
Australia. Unlike most lepidopterous pests, of
which the larva is the damaging stage, in this case
it is the adult that causes the damage through its
feeding on the fruit. The loopers Oxyodes scrobicu­
lata F. and Oxyodes tricolor Guen. (Lepidoptera:
Noctuidae) occupy similar niches in Thailand and
Australia, respectively. The caterpillars feed on the
foliage of litchi trees and can cause severe defolia-
tion. Although they will eat leaves of any age, they
prefer the younger ones. The litchi longicorn bee-
tle, Aristobia testudo (Voet), is a serious pest of
both litchi and longan in Guangdong Province in
China. In Taiwan, the white spotted longicorn bee-
tle, Anoplophora maculata (Thomson), has a one
year life cycle. These beetles girdle branches by
chewing 10  mm strips of bark. The larvae bore
into the xylem and create tunnels up to 60 cm long
in the wood. Several bugs belonging to the family
Tessaritomidae attack litchis and longans through-
out China, Southeast Asia and Australia. Tessari­
toma papillosa Drury occurs in southern China,
Vietnam, Thailand, Burma, the Philippines and
India, although there are reports that Tessaritoma
javanica Thunberg and Tessaritoma quadrata Dis-
tant are the species found on litchi in India. In
litchis and longans, adults and nymphs feed on
terminals, which may be killed, and also on flow-
ers and fruit, causing these to fall.
The litchi erinose mite, Aceria litchii (Keiffer),
also known in China as litchi hairy mite, hairy spi-
der, or dog ear mite, occurs throughout China and
Taiwan, India, Pakistan, Hawaii and Australia. The
litchi erinose mite attacks new growth, causing a
felt-like erineum to be produced on the leaflets.
This may form as several blisters, but if the infesta-
tion is severe, it may eventually cover the entire
leaflet, causing it to curl. Whole terminals may be
deformed. The erineum is at first silver-white,
changing as it ages to light brown and then dark
reddish brown. The longan erinose mite, Aceria
Tropical Fruit Pests and their Management
T 3933
longana Boczek and Knihinicki, is a sporadic but
major pest of longan in Thailand. A. longana is
specific to longan, severely affecting the terminals
and flowers. The longan gall mite, Aceria dimo­
carpi (Kuang), is associated with longans in China
where it is recorded as causing erineum on leaves
and also witches’ broom symptoms. The litchi leaf
midge, Dasyneura sp., is regarded as one of the
major pests of litchi in China, and Litchiomyia
chinensis Yang and Luo has been reared from galls
collected on litchi leaves in Guangdong.
Mango, Mangifera indica L.
(Anacardiaceae Family)
The mango most likely originated in Southeast
Asia, particularly in the Malay Archipelago. How-
ever, it was probably first grown as a food crop in
India, where its cultivation is thought to have com-
menced at least 4,000 years ago. Mangoes are now
grown as an important crop all over the world, in
both tropical and subtropical areas. Mangoes may
be eaten ripe or green, or the fruit is juiced or pro-
cessed into preserves, chutney, frozen puree, or
dried. World production of mangoes in 2000 was
estimated to be about 24.5 million tons. World-
wide, mango is affected by many pests. For instance,
mango flowers are attacked by a variety of insects
such as midges, leafhoppers, caterpillars and thrips.
These include leafhoppers (Hemiptera: Cicadelli-
dae) infesting mango flowers throughout Asia,
such as Idioscopus clypealis Lethierry, Idioscopus
niveosparsus Lethierry, Idioscopus magpurensis
Pruthi and Amritodius atkinsoni Lethierry. The
mango blister midge or mango gall midge (Dip-
tera: Cecidomyiidae), Erosomyia mangiferae Felt,
infests mangoes in the West Indies. Five cecid-
omyiid species, including Erosomyia indica Grover
and Prasad, are reported to attack mango flowers
and to cause severe damage in India, while Dasyn­
eura mangiferae (Felt) does the same in Hawaii.
Numerous species of lepidoptera have been
found to infest mango flower panicles in all pro-
duction areas, but in few cases have the species
3934
T Tropical Fruit Pests and their Management
involved been identified. In Florida, Pococera atra­
mentalis Lederer (Pyralidae) and Platynota ros­
trana (Walker) (Tortricidae) are the two most
damaging species of a complex that also includes
Pleuroprucha insulsaria (Guenée) (Geometridae),
Tallula spp. (Pyralidae) and Racheospilla gerularia
(Hübner). In the Philippines, the tip borer, Chlu­
metia transversa Walker (Noctuidae), is second
only to mango hoppers as a pest of flowers. The
geometrids, Eupithecia sp., Chloropteryx glaucip-
tera Hampson and Oxydia vesulia (Cramer), as
well as Penicillaria jocosatrix Guenée (Noctuidae),
also can be found feeding on mango panicles.
Other blossom pests are Frankliniella bispinosa
(Morgan) and Frankliniella kelliae (Sakimura) in
Florida, the western flower thrips, Frankliniella
occidentalis (Pergande), in Israel, and the chili
thrips, Scirtothrips dorsalis Hood, in Thailand.
Because of the high price paid for unblem-
ished fruit, fruits need to be protected from a range
of insects that may cause physical damage or
loss, or merely affect its outward appearance. Flies
of the Tephritidae are pests of mango in many
parts of the world. In the Neotropics, Anastrepha
spp.,   A.  obliqua (Macquart), the Mexican fruit
fly,  A. ludens (Loew), A. serpentina (Wiedemann),
A. striata Schiner, A. suspensa (Loew), A. ocresia
Walker, A. distincta Greene, A. fraterculus Wiede-
mann, and A. chiclayae Greene are considered
important pests. Bactrocera tryoni (Frogatt),
B. neohumeralis (Hardy), B. jarvisi (Tryon), B. zonata
(Saunders), B. frauenfeldi Schiner and B. dorsalis
(Hendel) are all reported to attack mango. The Med-
iterranean fruit fly, Ceratitis capitata, is reported
to  attack mango throughout the world, whereas
the  marula fruit fly, Ceratitis cosyra (Walker), and
the Natal fruit fly, Ceratitis rosa Karsch, are impor-
tant in Africa.
The mango seed weevils, Sternochetus
mangiferae (F.) (Coleoptera: Curculionidae), are
widely distributed in Africa, Asia, Australia, the
Pacific Islands and in some Caribbean islands,
whereas Sternochetus gravis (F.) and Sternochetus
frigidus (F.) occur in India and Bangladesh. Seed
weevils generally lay eggs in small green fruit, and
the larvae tunnel to the seed, where they feed and
develop. Deanolis sublimbalis Snellen (Lepidoptera:
Pyralidae), the mango seed borer, is also an impor-
tant pest of mango fruits in the Philippines,
­Vietnam, China, Thailand, Indonesia and Papua
New Guinea. The distinctive red-banded larvae
feed on and bore through the pulp to the seed.
Fruitspotting coreid bugs, such as the yellowish-
green coreid bugs Amblypelta lutescens lutescens
(Distant) and Amblypelta nitida Stål, and the tip
wilter, Anoplocnemis curvipes (Fabricius), can be
serious pests of young mango trees in South Africa.
Amblypelta lutescens feeds on the young fruit, caus-
ing black lesions to develop and the fruit to fall.
Pest of leaves and buds include gall midges
(Diptera: Cecidomyiidae) such as Protocontarinia
matteiana Kieffer and Cecconi, Erosomyia spp.,
Procontarinia schreineri Harris, Amradiplosis echi­
nogalliperada Mabi and P. matteiana. The galls dry
up and fall out, leaving a typical “shot-hole” effect.
Red-banded thrips, Selenothrips rubrocinctus
(Giard), and the Mediterranean mango thrips,
Scirtothrips mangiferae Priesner, feed on the leaf,
especially adjacent to the midrib, where they cause
a silvering that develops into necrosis, eventually
leading to leaf drop. The mango bud mite, Aceria
mangiferae Sayed is reported to attack the buds of
terminals, and spider mites belonging to the genus
Oligonychus (O. mangiferae Rahman and Sapra, O.
punicae (Hirst), and O. yothersi McGregor) feed on
the upper surface of mango leaves.
The mango scale, Aulacaspis tubercularis
(Newstead), is regarded as a key pest mostly
because it infests the fruit. Among the mealybugs,
Rastrococcus invadens Williams, and the margar-
odid Drosicha stebbingii (Green) (Margarodidae)
remain as important pests of leaves in different
mango growing areas.
Mangosteen, Garcinia mangostana
L. (Guttiferae Family)
Mangosteen is known only as a cultivated species,
although there have been occasional observations

of wild specimens in Malaysia. The scarcity of
mangosteen orchards, limited fruit supply and the
fruit’s short shelf life are major marketing prob-
lems. The long juvenile period of 10–15  years,
which discourages commercial production, con-
tributes to much of the limited fruit supply. The
mangosteen fruit is a globose and smooth berry,
turning dark purple at ripening. It is a crop of the
humid tropics, often found in association with
durian. The fruit has a diameter of 4–7  cm. The
edible part is the sweet white aril that envelops the
seeds within the pericarp.
Floral initiation to anthesis takes about
25  days and the fruit ripens 100–120  days later.
The most serious pests are Hyposidra talaca
(Walker) (Lepidoptera: Geometridae), a highly
polyphagous insect. Hyposidra talaca is a typical
looper, causing defoliation in tropical lowlands
and highlands. The citrus leafminer, Phyllocnistis
citrella (Lepidoptera: Phyllocnistidae), mines
leaves of mangosteen, causing leaf deformation
and often leading to early fall. Sictoptera cucul­
lioides Guenée (Lepidoptera: Noctuidae) is
reported to feed voraciously on young flushes of
mangosteen.
Papaya, Carica papaya L.
(Caricaceae Family)
Papaya, Carica papaya L., is a major tropical fruit
cultivated through the tropical and Neotropical
regions of the world between 32°N and 32°S.
Although papaya was probably cultivated by early
civilizations in the New World, no botanical
records are available prior to the arrival of Columbus
to America. This herbaceous plant is also known
as papaw, paw paw, kapaya, kepaya, lapaya, tapaya,
papayao, papaya, papaia, papita, lechosa, fruta
bomba, mamon, mamona, mamao, and tree melon.
Papaya is cultivated mainly for its edible fruit, but
medicinal and industrial uses also have been
documented.
Fruit flies (Diptera: Tephritidae) are the only
group of insects that actually penetrate the pulp or
Tropical Fruit Pests and their Management
T 3935
seeds. Twenty-six species from seven genera, Anas­
trepha (two species), Bactrocera (17 species), Cera­
titis (three species), Dacus, Euphranta, Myoleja,
and Toxotrypana (one species each) attack papaya
fruits. Toxotrypana curvicauda Gerstaecker is the
most important fruit fly species attacking papaya
in the Americas and Caribbean Basin, whereas
Bactrocera papayae (Drew and Hancock) is one of
the most threatening pests to papaya in Australia.
Anastrepha spp., C. capitata (Wiedemann), C. catoirii
Guerin-Meneville, and C. rosa Karsch also are
known to attack papaya.
Arthropods affecting the foliage and trunk
of papaya include the white peach scale, Pseu­
daulacaspis pentagona (Targioni-Tozetti), the
papaya scale, Philephedra tuberculosa Nakahara
and Gill, and the papaya mealybug, Paracoccus
marginatus Williams and Granara de Willink.
Several species of mites feed on papaya. They
include the carmine mite, Tetranychus cinnabar­
inus (a key pest), the red and black flat mite,
Brevipalpus phoenicis (an occasional pest), and
the papaya leaf edge roller mite, Calacarus
­brionese. Damage by the broad mite, Polyphago­
tarsonemus latus (Banks) (Tarsonemidae), is con-
fused with virus-like symptoms. Nine cicadellid
species from three genera (Empoasca, Poecil­
oscarta and Sanctanus) can affect papaya, such as
Empoasca papayae Oman, which transmits
bunchy-top, E. stevensi Young, and E. insularis
Oman. Aphids do not colonize papaya plants
and are considered minor pests, but ­several spe-
cies, Aphis coreopsidis (Thomas), Aphis nerii
Boyer de Fonscolombe, Aphis gossypii Glover,
Aphis spiraecola Patch, Myzus persicae (Sulzer),
and Toxoptera aurantii (Boyer de Fonscolombe),
can be found on papaya plants. Several aphid
species [M. persicae, M. euphorbiae, A. spiraecola
(=A. citricola), A. gossypii, A. craccivora, A. nerii,
R. maidis, and T. auranti (Boyer de Fosc)] are
capable of transmitting papaya ringspot virus.
Among the defoliators, hornworms (Lepidoptera:
Sphingidae), Eryinnis alope (Drury), E. ello,
and  E. lassuxi merianae Grote, are considered
important.
3936
T Tropical Fruit Pests and their Management
Passion Fruit (Passifloraceae
Family)
Passion fruits belong to the genus Passiflora (fam-
ily Passifloraceae), which has a wide genetic base.
While some species are undomesticated, others are
cultivated as ornamental plants, for nourishment
and for medicinal purposes. The majority of Passi-
flora are indigenous to the tropical and subtropical
regions of South America. Of the 400 known spe-
cies of Passiflora, about 50 or 60 bear edible fruits.
A few species are economically important, e.g.,
Passiflora edulis Sims., botanical form flavicarpa
Deneger, the yellow passion fruit, whose juice and
pulp are used extensively as ingredients of bever-
ages, salads, fruit cocktails and desserts. The major
producers of passion fruits are found in South
America, mainly Brazil, Colombia, Peru and Ecua-
dor. Commercial plantations of passion fruits are
found also in Australia, Hawaii, India, New Guinea,
Kenya, South Africa, Sri Lanka and Costa Rica.
Passiflora edulis f. flavicarpa, P. edulis (purple pas-
sion fruit), and P. alata (sweet passion fruit) are the
main species cultivated in the world. Passiflora
ligularis (granadilla) and P. quadrangularis (badea)
are cultivated in the Andean region of South
­America and in Central America.
Although the passion fruit crop has great
economic potential, its establishment and expan-
sion have been hindered by various problems.
For example, passion fruit is attacked by a wide
host range of diseases, insects and mites. Some
pest species cause significant losses, reaching
the  status of key pests or secondary pests. They
include lepidopterous defoliators such as three
heliconiine species, Dione juno juno Cramer,
Agraulis vanillae vanillae Linnaeus, and Eueides
isabella huebneri Ménétries (Nymphalidae). Many
species of bugs attack passion fruit; the majority
belong to the Coreidae (leaf-footed bugs), such as
Diactor bilineatus Fabricius, Leptoglossus spp., and
Holhymenia spp. Diactor bilineatus is the most
common species in Brazil and Venezuela, and
is  known as the passion fruit bug because it
feeds  only on fruit of Passiflora spp. Among the
Holhymenia, Holhymenia clavigera (Herbst.) and
H. histrio (Fabricius) are reported attacking
­passion fruit. Leptoglossus gonagra Fabricius and
L. australis Fabricius are reported from several
passion fruit producing regions.
Flies of the genera Anastrepha Schiner
(Tephritidae) and Lonchaea Fallén (Lonchaeidae)
cause economic losses. Anastrepha consobrina
(Loew), A. ethalea (Walker), A. grandis (Macquart),
A. kuhlmenni Lima, A. lutzi Lima and A. pseudop­
arallela (Loew) are the most frequent species fol-
lowed by Anastrepha pallidipennis Guerne on
yellow passion fruit. The oriental fruit fly, Bactro­
cera dorsalis (Hendel), melon fly, Dacus cucurbitae
Coquillett, and the Mediterranean fruit fly, Cerati­
tis capitata Wiedemann, are known to attack pas-
sion fruit in Hawaii. The Queensland fruit fly,
Dacus tryoni (Froggatt), is the most important
insect pest of passion fruit in Australia.
Neosilba pendula (Bezzi) and Dasiops sp.
(Lonchaeidae) attack flowers and buds of passion
fruit. The species of Dasiops include D. curubae
Steykal, D. inedulis Steykal and D. passifloris
McAlpine. Other flies that may also feed upon
flower and buds are Lonchaea cristula McAlpine
(Lonchaeidae) and Zapriothrica salebrosa Wheeler
(Drosophilidae).
Several species of mites have been reported
from passion fruit including Brevipalpus phoenicis
(Geijskes) (Tenuipalpidae) and the red spider
mites, Tetranychus mexicanus (McGregor) and
T.  desertorum Banks (Tetranychidae), causing
­general discoloration of the leaves and necrosis,
culminating in leaf drop. The broad mite, Polyphag­
otarsonemus latus (Banks), induces malformations
in developing leaves, which later dry and drop. It
may attack flowering buds, causing a reduction
in the number of flowers.
Pineapple, Ananas comosus (L.)
Merr. (Bromeliaceae Family)
The pineapple, Ananas comosus (L.) Merr., is a self-
sterile herbaceous, perennial, monocotyledonous

plant originating in the New World. The commer-
cial cultivars are placed in five distinct groups, i.e.,
“Cayenne,” “Spanish,” “Queen,” “Pernambuco” and
“Perolera.” It is currently grown in many countries
with tropical and subtropical climates. Most pine-
apple pests are endemic to the new countries and
adapted to utilize the pineapple to support their
life-cycles.
More than 100 species of plant-parasitic nem-
atodes have been recorded in association with
pineapple roots, and between three and five spe-
cies are usually found in most pineapple fields.
The  key nematode pests include the root-knot
nematode (Meloidogyne javanica and M. incog­
nita), the reniform nematode (Rotylenchulus reni­
formis) and the lesion nematode (Pratylenchus
brachyurus). The key nematode pests of pineapple
are all endoparasites. They either establish a per-
manent feeding site within the root and become
sedentary, e.g., root-knot and reniform nematodes,
or they live inside roots but remain migratory,
e.g.,  lesion nematodes. Key arthropod pests are
the pineapple leathery pocket mite/pineapple fruit
mite, Steneotarsonemus ananas (Tryon), Dolicho­
tetranychus floridanus (Banks), and the sym-
phylids Hanseniella (Symphyla: Scutigerellidae),
e.g., H. unguiculata, H. ivorensis, and Scutigerella
sakimurai (Symphyla: Scolopendrellidae). Steneo­
tarsonemus ananas is important because of its
association with the fruit diseases, interfruitlet
corking, leathery pocket and fruitlet core rot/
black spot. The pineapple flat mite, D. floridanus,
attacks plants of all ages. Damage is primarily
to  the whitish leaf bases, which develop brown/
black necrotic lesions and appear progressively
dehydrated, with feeding mites around lesion
peripheries, or as orange patches on leaf bases.
The symphylids H. unguiculata, H. ivorensis
and S. sakimurai feed on young meristematic tis-
sues causing newly established plants to stop root
development and causing severe witches’ broom
symptoms. Other important pests are the onion
thrips or yellow spot thrips, Thrips tabaci Linde-
man, responsible for yellow spot disease of pine-
apples, the pink pineapple mealybug, Dysmicoccus
Tropical Fruit Pests and their Management
T 3937
brevipes (Cockerell), associated with the devastat-
ing disease, pineapple mealybug wilt, the pineap-
ple scale, Diaspis bromeliae (Kerner), infesting the
lower pineapple leaves, the pineapple caterpillar,
Thecla basilides (Geyer), causing larval galleries
and rendering the fruit unmarketable, and the
white grubs, Lepidiota grata, Rhopaea magnicornis,
Adoretus ictericus, and the melolonthids, Macro­
phylla ciliata and Asthenopholis subfasciata,
destroying the root system.
Rambutan, Nephelium lappaceum
Blume (Sapindaceae Family)
Rambutan is a tropical relative of litchi, with a dis-
tribution that ranges from southern China through
the Indo-Chinese region, Malaysia, and Indonesia
to the Philippines. As the name suggests (the Malay
word “rambut” meaning hair), the fruit is glabrous,
resembling a burr. Rambutan, while highly prized
in its region of origin, remains a minor fruit inter-
nationally. The fruits are consumed fresh or
canned. The rambutan fruit is an ellipsoid to sub-
globular schizocarp, up to 7  cm  ×  5  cm, usually
consisting of one nutlet. The skin color varies from
yellow to purplish red. The seed usually is covered
by a thick, sweet, juicy, white to yellow, translucent
sarcotesta, which is the edible part.
The main flowering period occurs during the
dry season. Fruits ripen about 110  days after
bloom. The most important pests are the durian
borer, Conopomorpha (=Acrocercops) cramerella
(Snellen) (Lepidoptera: Gracillariidae). This insect
tends to damage only the part of the fruit next
to  the fruit stalk. The cockchafer beetle, Adoretus
(=Lepadoretus) compressus (Weber) (Coleoptera:
Scarabaeidae), feeds on the interveinal areas
close to the center of the leaf. Adults of Apogonia
cribricollis Burmeister (Coleoptera: Scarabaeidae)
are active at night, feeding on foliage from the
leaf  margin inwards. Chalcocelis albiguttatus
(Snellen) and Parasa lepida (Cramer) (Lepi-
doptera: Limacodidae) cause severe defoliation
of rambutan trees.
3938
T Tropical Fruit Pests and their Management

Integrated Pest Management (IPM) undamaged fruit of high quality; thus, the lack
for Tropical Fruit of knowledge of economic thresholds, or the low
existent economic thresholds, requires control
Tropical fruit crops provide a relatively stable programs to focus on preventing damage by
environment over many years, offering continuing these pests.
habitats for both pests and natural enemies, and
providing opportunities for biological control and
effective pest management programs. Any attempt
Chemical Control
to develop integrated control programs in fruit
crops must take into account the following: (i)
Pesticides have been significant for protecting
knowledge of native or resident arthropod fauna;
tropical fruit from insect attack and increas­
(ii) arthropod fauna affecting the tree crop in its
ing tropical fruit productivity, therefore the con-
area of origin or domestication; and (iii) presence
trol of fruit and foliar insect pests tends to be
of natural enemies. The basis for integrated pest
heavily dependent on chemical insecticides/aca-
management includes the pest’s biology and
ricides. Information regarding proper timing,
­ecology, sampling and monitoring techniques,
spray volumes, and knowledge of the pest com-
economic thresholds and the application of man-
plex is available for some crops such as pineap-
agement tactics, i.e., chemical, biological, autocidal,
ple, and scarce for others such as papaya. Regular,
plant resistance, etc.
heavy sprays for controlling fruit flies and leaf-
hoppers in papaya can cause heavy outbreaks of
mites and other pests. Widespread use of nonse-
Sampling and Monitoring
lective pesticides continues to be the rule, but
currently there is a trend toward evaluating a
Sampling and monitoring methods for tropical
new generation of pesticides, adoption of selec-
fruits are well established for some direct pests
tive spraying, timing of spray applications, and
such as fruit flies and fruit borers, as well as for
determining the effect of pesticides on predators
some indirect pests (i.e., banana weevil) and defo-
and parasitoids. In contrast, there is minimal to
liators. However, the inability to relate results of
nonexistent information on the effect of pesti-
sampling to infestation of the fruit at the time of
cides on pollinators. For instance, the deleteri-
harvest is still a problem. Attempts have been made
ous effects on pollinators can be reduced by
to develop sampling techniques for several pests
timing spray applications in passion fruit,
of mango, avocado and banana; however for some
according to the cultivar. Purple passion, whose
pests and crops, adequate sampling techniques are
flowers open during the morning hours, should
not available. This, of course, may be a reflection of
be sprayed during late afternoon, while the yel-
the place where the crop is grown, the purpose of
low cultivar, whose flowers open in the after-
tree cultivation (export vs. internal consumption)
noon, should be sprayed in the morning.
and grower economic solvency (Australia, USA,
South Africa, Israel) vs. growers from other regions
of the world.
Attractants (Pheromones)

Economic Thresholds Use of sexual attractants (pheromones) is mostly

limited to fruit flies, while little information is
As export commodities, tropical fruit crops have available for other insect groups, such as curcu-
a consistently high value, with highest prices for lionids and Lepidoptera.

Crop Sanitation
Crop sanitation is an important factor for maintain-
ing low banana weevil densities in banana farms,
and is used as a tentative effort to control important
pests of avocados (i.e., weevils), annona (annona
seed borer) and mango (mango seed weevil).
Biological Control
Biological control has great potential as a major
tactic for regulating pest populations in fruit
orchards. The ability to apply biological control
effectively has increased in recent decades because
of greater knowledge of the arthropod fauna of
some tropical fruits (citrus, avocado, pineapple
and mango). While biocontrol agents are recorded
for most pests of other tropical fruit crops, con-
centrated efforts to use bio-regulators are rarely
observed. For instance, efforts toward developing
systems for biocontrol of pink mealybug, Maco­
nellicoccus hirsutus, and carambola fruit fly, Bac­
trocera carambolae, in the Caribbean were not
initiated until these pests were major threats to
crops such as citrus. If a stenophagous insect (i.e.,
avocado weevils, papaya fruit fly, avocado thrips
and annona fruit moths) is the major constraint
to a single commodity, efforts for biological con-
trol are half-hearted. The exception to this rule is
the current strong effort toward ­biocontrol of
banana weevil and the search for natural enemies
of avocado thrips. With time, it is likely that more
extensive use will be made of biological agents to
control pests of tropical fruit crops.
Host Plant Resistance
Host plant resistance offers considerable promise
as a tactic in pest management. Even though it
appears that most efforts are concentrated toward
plant pathogens, use of this tactic merits atten-
tion for some crops and some pest species. Resis-
tance to arthropods in tropical fruit germplasm
Tropical Fruit Pests and their Management
T 3939
collections should be a high priority. Most efforts
are directed at insect vectors (papaya and pine-
apple) and pests of avocado, mango and guava.
Several fruits, i.e., durian and acerola, continue to
be largely unnaturalized, and improved selec-
tions are rare.
Cultural Practices
Untreated backyard trees and neglected plantings
are considered to be major sources of pests, such
as fruit flies. For instance, in Australia, hygiene
and attention to alternative host plants that can
increase pest pressure on the custard apple
orchard are important. Mature fruit infested with
yellow peach moth or with fruit fly should be col-
lected and destroyed. Preferred fruit fly hosts like
guava and loquat should not be planted in or near
the orchard. Cultural practices generally do not
offer a direct means for controlling pests, but used
properly they can enhance natural enemy activity
or retard pest population growth to a degree that
is important in integrated control programs.
References
Aguiar-Menezes E, Menezes EB, Cassino PCR, Soares M
(2002) Passion fruit. In: Peña JE, Sharp JL, Wysoki M
(eds) Tropical fruit pests and pollinators. CABI,
Wallingford, pp 361–390
Gold CS, Pinese B, Peña JE (2002) Pests of banana. In: Peña JE,
Sharp JL, Wysoki M (eds) Tropical fruit pests and polli-
nators. CABI, Wallingford, pp 13–56
Gould WP, Raga A (2002) Pests of guava. In: Peña JE, Sharp JL,
Wysoki M (eds) Tropical fruit pests and pollinators.
CABI, Wallingford, pp 295–314
Ooi PAC, Winotai A, Peña JE (2002) Pests of minor tropical
fruit. In: Peña JE, Sharp JL, Wysoki M (eds) Tropical
fruit pests and pollinators. CABI, Wallingford,
pp 315–330
Pantoja A, Follett PA, Villanueva J (2002) Pests of papaya. In:
Peña JE, Sharp JL, Wysoki M (eds) Tropical fruit pests
and pollinators. CABI, Wallingford, pp 131–156
Peña JE, Nadel H, Barbosa-Pereira M, Smith D (2002) Polli-
nators and pests of Annona. In: Peña JE, Sharp JL,
Wysoki M (eds) Tropical fruit pests and pollinators.
CABI, Wallingford, pp 197–222
3940
T Tropical Fruitworm Moths (Lepidoptera: Copromorphidae)
Petty G, Stirling G, Bartholomew DP (2002) Pests of pineap-
ple. In: Peña JE, Sharp JL, Wysoki M (eds) Tropical fruit
pests and pollinators. CABI, Wallingford, pp 157–196
Waite GK (2002) Pests and pollinators of mango. In: Peña JE,
Sharp JL, Wysoki M (eds) Tropical fruit pests and polli-
nators. CABI, Wallingford, pp 103–130
Waite G, Hwang JS (2002) Pests of litchi and longan. In: Peña JE,
Sharp JL, Wysoki M (eds) Tropical fruit pests and polli-
nators. CABI, Wallingford, pp 331–360
Wysoki M, van den Berg MA, Ish-Am G, Gazit S, Peña JE,
Waite G (2002) Pests and pollinators of avocado. In:
Peña JE, Sharp JL, Wysoki M (eds) Tropical fruit pests
and pollinators. CABI, Wallingford, United Kingdom,
223–294
Tropical Fruitworm Moths
(Lepidoptera: Copromorphidae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tropical fruitworm moths, family Copormorphi-
dae, are a small family of 58 species, mostly tropi-
cal; actual fauna probably exceeds 100 species.
The family is part of the superfamily Copromor-
phoidea in the section Tineina, subsection
Tineina, of the division Ditrysia. Adults small to
medium size (12–37  mm wingspan), with head
somewhat smooth-scaled; haustellum naked;
labial palpi prominent and porrect; maxilary palpi
3- to 4-segmented (rarely 1-segmented). Wing
venation with forewing veins long and typically
equidistant near the termen; wings typically
rounded along forewing termen. Maculation
mostly dull gray with dark markings, and many
have forewing scale tufts. Adults nocturnal. Larvae
are leaf feeders using a leaf web, or are borers (one
feeds beneath bark), but few biologies are known.
Host plants include Berberidaceae, Ericaceae,
Moraceae, Podocarpaceae, and Rubiaceae.
References
Clarke JFG (1955) Copromorphidae. In JFG Clarke, Cata-
logue of the type specimens of Microlepidoptera in the
British Museum (Natural History) described by Edward
Meyrick, 2: 509–531. British Museum (Natural History),
London
DeBenedictis JA (1984) On the taxonomic position of Ella-
bella Busck, with descriptions of the larva and pupa of
E. bayensis (Lepidoptera: Copromorphidae). Journal of
Research on the Lepidoptera 23:74–82
DeBenedictis JA (1985) The pupa of Lotisma trigonana and
some characteristics of the Copromorphidae (Lepi-
doptera). Journal of Research on the Lepidoptera
24:132–135
Heppner JB (1984) Revision of the Oriental and Nearctic
genus Ellabella (Lepidoptera: Copromorphidae). Jour-
nal of Research on the Lepidoptera 23:50–73
Heppner JB (1986) Revision of the New World genus Lotisma
(Lepidoptera: Copromorphidae). Pan-Pacific Entomol-
ogist 62:273–288
Tropical Lattice Moths
(Lepidoptera: Arrhenophanidae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tropical lattice moths, family Arrhenophanidae,
total 30 species, mostly Neotropical but recently
with some Southeast Asian additions; actual fauna
probably exceeds 50 species. The family is part of
the superfamily Tineoidea, in the section Tineina,
subsection Tineina, of the division Ditrysia. Adults
small to medium size (12–69 mm wingspan), with
robust bodies and roughened head scaling; haust-
ellum reduced or absent; maxillary palpi absent;
antennae serrate to bipectinate. Maculation varies
from light colored (often yellow) with translucent
and colored wing marks, to dark and somber col-
ored. Adult activity nocturnal but some are diur-
nal (e.g., species in Taiwan). Biologies are unknown
except for one Neotropical species with casebear-
ing larvae that feed on fungi.
References
Bradley JD (1951) Notes on the family Arrhenophanidae
(Lepidoptera: Heteroneura), with special reference to the

morphology of the genitalia, and descriptions of one new
genus and two new species. Entomologist 84:178–185
Davis DR (1984) Arrhenophanidae. In: Heppner JB (ed)
Atlas  of Neotropical Lepidoptera. 2. Checklist: Part 1
(Micropterigoidea-Immoidea) 6. W. Junk, The Hague
Davis DR (1991) First Old World record of Arrhenophanidae.
Trop Lepidoptera 2:41–42
Tropical Longhorned Moths
(Lepidoptera: Lecithoceridae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tropical longhorned moths, family Lecithoceridae,
total about 1,038 described species, mostly tropical
Oriental, but also with one group in the Palearctic;
actual fauna probably exceeds 1,500 species. There
are four subfamilies: Ceuthomadarinae, Oditinae,
Lecithocerinae, and Torodorinae. The family (pre-
viously known as Timyridae) is part of the super-
family Gelechioidea in the section Tineina,
subsection Tineina, of the division Ditrysia. Most
species are in Lecithocerinae (475 sp.). The most
colorful and largest species are in the tropical
subfamily Torodorinae. Adults small (5–30  mm
wingspan), with head mostly smooth-scaled, and
antennae mostly long; haustellum scaled; labial
palpi long; maxillary palpi 4-segmented and folded
over haustellum base (rarely reduced to one seg-
ment). Maculation varies from dull to brightly
colored and variously marked. Adults are mostly
diurnal and many have the habit of holding the
antennae together to the front when at rest. Larvae
may mostly be leaf litter feeders or leaf tiers, but few
species are known biologically. A few varied host
plants are recorded, such as Fagaceae, Myrtaceae,
Rosaceae, and Rubiaceae (Fig. 109).
References
Clarke JFG (1965) Timyridae. In: Clarke JFG, Catalogue of
the type specimens of Microlepidoptera in the British
Tropical Plume Moths (Lepidoptera: Oxychirotidae)
T 3941
Tropical Longhorned Moths (Lepidoptera:
­Lecithoceridae), Figure 109  Example of tropical
longhorned moths (Lecithoceridae), Lysipatha
diaxantha Meyrick from Taiwan.
Museum (Natural History) described by Edward Mey-
rick, 5:1–255. London: Br. Mus. (Nat. Hist.)
Gozmány LA (1978) Lecithoceridae. In: Amsel HG, Gregor F,
Reisser H (eds) Microlepidoptera Palaearctica, 5:1–306,
93 pl. G. Fromme, Vienna (in German)
Wu C-S (1997) Lepidoptera. Lecithoceridae. In: Fauna Sinica.
Insecta, vol. 7. Science, Beijing, 302 pp
Wu C-S, Park K-T (1999) A taxonomic review of the family
Lecithoceridae (Lepidoptera) in Sri Lanka. Tinea
16:61–72; Korean J Syst Zool 15:1–9, 205–220; Insecta
Koreana 16:1–14, 131–142
Tropical Plume Moths
(Lepidoptera: Oxychirotidae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tropical plume moths, family Oxychitoridae,
include only six species, all Indo-Australian and
South Pacific. Some specialists include this family
as part of the Tineodidae. The family is in the
superfamily Pterophoroidea in the section Tineina,
subsection Tineina, of the division Ditrysia. Adults
small (10–12  mm wingspan), with head scaling
average; haustellum naked; labial palpi porrect;
maxillary palpi 4-segmented. Wings extremely
linear, with long fringes, or wider and with both
3942
T Tropical Slug Caterpillar Moths (Lepidoptera: Dalceridae)
wings split into two plumes each. Maculation
shades of brown or gray, with coordinated spot-
ting or banding in the split-wing species. Adults
may be crepuscular. Larva of one species feeds on
seeds of white mangrove (Avicenniaceae); the
remainder are unknown biologically.
References
Clarke JFG (1986) Family Oxychirotidae. In: Pyralidae
and Microlepidoptera of the Marquesas Archipelago.
­Smithson Contrib Zool 416:14–16
Common IFB (1970) Oxychirotidae. In: Insects of Australia.
Melbourne University Press, Melbourne, p 835
Common IFB (1990) Family Tineodidae. In: Moths of
­Australia, [part]. Melbourne University Press, Melbourne,
pp 322–325
Heppner JB (1997) Oxychirotidae. Lepidopterorum Catalo-
gus, (n.s.). Fasc. 62. Association for Tropical Lepidoptera,
Gainesville, 8 pp
Tropical Slug Caterpillar Moths
(Lepidoptera: Dalceridae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tropical slug caterpillar moths, family Dalceridae,
include 84 Neotropical species (only one sp.
occurs north of Mexico, in southern Arizona).
Two ­subfamilies are known: Acraginae and Dal-
cerinae. The family is in the superfamily Cos-
soidea (series Limacodiformes) in the section
Cossina, subsection Cossina, of the division Dit-
rysia. Adults small to medium size (11–50  mm
wingspan), with head small and scaling rough-
ened; labial palpi 2-segmented and very short;
maxillary palpi vestigial; antennae short and
bipectinate. Body robust. Wings quadratic and
rounded; hindwings notably ovoid (Fig.  110);
frenulum sometimes absent. Maculation mostly
brown hues with few markings but can be colorful,
with yellow, orange, or pink, or lustrous white and
silvery. Adult activity uncertain; possibly only
nocturnal or crepuscular. Larvae slug-like, often
with translucent gelatinous wart-like surface;
feeding as leaf feeders (early instars as leaf skele-
tonizers), but few are known biologically. Various
host plants are used and some larvae are  polypha-
gous. Few have any economic status.
References
Epstein ME (1996) Dalceridae Dyar, 1898. pp 79–81 In: Revi-
sion and phylogeny of the limacodid-group families,
with evolutionary studies on slug caterpillars (Lepi-
doptera: Zygaenoidea). Smithson Contrib Zool 582:
1–102
Hopp W (1928) Beitrag zur Kenntnis der Dalceriden. Dtsch
Entomol Z Iris 42:283–287
Miller SE (1994) Systematics of the Neotropical moth family
Dalceridae (Lepidoptera). Bull Mus Comp Zool
153:301–495
Orfila RN (1961) Las Dalceridae (Lep. Zygaenoidea) argenti-
nas. Rev Invest Agric 15:249–264, 1 pl
Seitz A (ed) (1938–39) Familie: Dalceridae. Die Gross-
Schmetterlinge der Erde 6:1303–1304 (1938);
1305–1312, pl. 168, 185 (1939). A. Kernen, Stuttgart
Tropical Theileriosis
A tick-transmitted disease caused by the proto-
zoan Theileria annulata.
 Piroplasmosis
Tropical Slug Caterpillar Moths (Lepidoptera:
Dalceridae), Figure 110  Example of tropical slug
caterpillar moths (Dalceridae), Acraga coa (Schaus)
from Mexico.
 Trunk and Canker-Causing Fungi
T 3943

Tropiduchidae large head tuft (no eye-caps on the antennal

bases); haustellum is short, scaled basally; labial
A family of insects in the superfamily Fulgoroidae palpi 3-segmented, short and porrect; maxillary
(order Hemiptera). They sometimes are called palpi minute and 1-segmented. Wing venation
planthoppers. is very reduced, with frenular bristles as the
 Bugs wing coupling. Maculation is generally somber
but often with iridescences. Adults are diurnally
active. The few larvae known are leafminers,
usually trumpet-shaped mines or blotch mines,
Trout Stream Beetles on a variety of host plants.
Members of the family Amphizoidae (order
Coleoptera). References
 Beetles
Braun AF (1972) Tischeriidae of America north of Mexico
(Microlepidoptera). Mem Am Entomol Soc 28:1–148
Diskus A (1998) Review of the Tischeriidae (Lepidoptera) of
True Katydids Central Asia. Acta Zool Lituanica 8:(3)23–33
Grandi G (1929) Contributo alla conoscenza della Tischeria
A subfamily (Pseudophyllinae) of katydids in the gaunacella Dup. ed appunti sulla Tischeria complanella
Hbn. (Lepidoptera – Tischeriidae). Boll Lab Entomol
order Orthoptera: Tettigoniidae. Bologna 2:192–243, 5 pl
 Grasshoppers, Katydids and Crickets Hering O (1926) Die Blattminierer-Gattung Tischeria in
ihren palaearktischen Arten. Entomol Jahrb 35:99–106,
1 pl
Sato H (1993) Tischeria leafminers (Lepidoptera, Tischerii-
Trumpet dae) on deciduous oaks from Japan Jpn J Entomol
61:547–556
The respiratory horn or tube of the mosquito
pupa.
Trumpet-Net Caddisflies

Trumpet Leafminer Moths Members of the families Polycentropodidae and

(Lepidoptera: Tischeriidae) Psychomyiidae (order Trichoptera).
 Caddisflies
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA Truncate
Trumpet leafminer moths, family Tischeriidae, Cut off squarely.
total 81 known species from all regions except
Australia, but the Nearctic has most of the
known species (48 sp.). The family forms a
monobasic superfamily, Tischerioidea, in the Trunk and Canker-Causing Fungi
section Nepticulina, of the division Monotrysia,
infraorder Heteroneura. Adults small (6–11 mm Fungi transmitted to plants by insects
wingspan), with head rough-scaled, with very  Transmission of Plant Diseases by Insects
3944
T Trypanosomes
Trypanosomes
Clarence M. Lee1, Earlene Armstrong2
1
Howard University, Washington, DC, USA
2
University of Maryland College Park, MD, USA
Trypanosomes are microscopic unicellular pro-
tozoa that are ubiquitous parasites of plants,
invertebrates, and vertebrates. These parasites
have existed for more than 300 million years
and have evolved with their natural hosts. Most
of the trypanosomes cause no harm to their
hosts and are found in locations throughout
the world. Some, however, cause serious diseases
in their hosts and are of major medical and
­veterinary significance. Only a few species of
trypanosomes are pathogenic to man. These
trypanosomes are not only found in sub-Saharan
Africa, where they infect both man and live-
stock, but also occur in Canada, Latin America,
and extend to the southern borders of the
United States.
The pathogenic trypanosomes of mammals
are called hemoflagellates. These trypanosomes
require the blood of their host (human, live-
stock, etc.) in order to undergo changes per-
taining to their life cycles. In addition, the
parasite may be transmitted to its host by
­various techniques, depending on the species
of  the parasite. For example, Trypanosoma
equiperdum, a trypanosome known to infect
horses, is  transmitted via venereal contact.
However, the vast majority of the different spe-
cies of ­trypanosomes affecting mammals are
transmitted via an insect vector.
The most important insect vectors associated
with trypanosomiasis (disease caused by protozoa
belonging to the genus Trypanosoma) in verte-
brates are the tsetse flies belonging to the genus
Glossina. There are 33 known and recognized spe-
cies of this genus. These vectors can be further
divided ecologically into three major groups: the
riverine flies of the palpalis group; the savanna
flies of the morsitans group; and the forest flies of
the fusca group.
Tsetse flies can be distinguished from other
flies by the presence of a needle-like forward
projecting proboscis, a hatchet-like cell in the
middle of the wings and a lateral plumose like
arista on the antennae. They are closely related
to the muscoid (i.e., house flies, stable flies) flies
but may be given their own family name,
Glossinidae.
Unlike most flies that are oviparous, the
female tsetse fly retains the larva in the uterus and
gives birth to one 3rd instar larva at a time. During
gestation, the larva is fed from so-called uterine
milk-like glands found in the body. When the
female larviposits, the larva burrows quickly in the
soil and transforms quickly into a pupa. Adult
emergence is dependent on the soil temperature
and moisture conditions. Adult tsetse flies mate
only once and a female produces about 10 off-
spring during her life span. Both sexes are active
bloodsuckers.
Rarely are tsetse flies found in open country
because all need some tree/vegetation cover. They
are mostly confined to a specific type of habitat
and the physical conditions prevailing therein.
The flies feed on those animals most readily avail-
able in their specific habitat, and therefore carry
trypanosomes harbored by their preferred hosts.
As a result, infection rates and kinds of trypano-
somes vary from one fly habitat to another.
Another important insect vector associated
with trypanosomiasis in vertebrates is the assas-
sin bug, cone-nose bug, or kissing-bugs belong-
ing to the family Reduviidae of the order
Hemiptera (true bugs). They are characterized
by having two pairs of wings; the forewings have
leathery basal portions and a membranous dis-
tal portion. The second pair of wings is mem-
branous. Hemiptera belonging to this family
have piercing sucking mouthparts adapted for
feeding on other arthropods or blood. The most
important genera of reduviid bugs with some
medical importance are Triatoma, Panstrong­
lyus, and Rhodnius which serve as vectors of
Trypanosoma cruzi, the causative agent for
­Chagas’ disease.

General Life Stages of
Trypanosomes
Trypanosomes appear in four basic forms or stages
as they undergo changes in the life cycle. These
forms or stages differ from species to species, in
that some species may exhibit only 2 of the four
forms and others may exhibit all four forms. Each
form has specific structures that enable it to adapt
to its environment. One form is the amastigote or
leishmanial stage. This stage has a kinetoplast,
which is a structure that is always located at the
place of entry into the cell of the flagellum and is
opposed to the basal body of the later. The kineto-
plast is further composed of a blepharoplast and
parabasal body. This structure is analogically simi-
lar to the structure of the mitochondria, which is
the powerhouse of most types of cells. In addition
to a kinetoplast, the amastigote stage has a nucleus.
Although the orientation of the kinetoplast can be
detected by using the flagellum as a landmark, the
leishmanial stage does not have a flagellum. A sec-
ond stage is the promastigote or leptomonad stage.
This stage is found within the tissues of the infected
host. In this stage, a flagellum is present. From this
stage, the parasite can and does change back and
forth between the amastigote and the leptomonad
stage in a phenomenon known as transition or
morphogenesis. A third stage is the epimastigote
or the crithidial stage. The unique characteristic or
defining feature of this stage in the history of
hemoflagellates is that its undulating membrane
or flagellum originates anteriorly to the nucleus.
Finally, the last stage is the trypomastigote or try-
panosomal stage. The unique or defining feature
of this stage is that its undulating membrane origi-
nates posterior to the nucleus.
In addition to the morphological differences,
these stages can also show metabolic differences.
For example, another interesting aspect to the life
cycle of the trypanosomes involves the cytochrome
oxidase system. The cytochrome oxidase system is
one that requires the presence of the metal iron
(Fe) in order to work. The only stage that uses this
system (i.e., the cytochrome oxidase system) is the
Trypanosomes
T 3945
epimastigote stage or form. Once the epimastigote
stage is placed in a culture that contains other
sources of nutrients apart from iron, there is an
immediate change or transformation that occurs.
The epimastigote form of the parasite immediately
changes to the trypomastigote stage, which does
not use the cytochrome oxidase system. The try-
pomastigote stage then use the other forms of
nutrients in the culture in order to survive.
Pathogenic Trypanosomes in
Humans
The three major species of this parasite that are
extremely pathogenic to humans are Trypanosoma
rhodesiense, Trypanosoma gambiense, and Try­
panosoma cruzi. These parasites were named based
on, or according to, either the region they were
first found or by the person who first found them.
All are hemoflagellates, and thus require the blood
of their host in order to undergo their life cycles.
Furthermore, the three species also have one or
two of the same life cycle stages or forms present.
Notwithstanding, different vectors transmit them
and all three parasites run a totally different course
of infection in man.
T. rhodesiense and T. gambiense are found pri-
marily in Africa while T. cruzi is located through-
out Latin America and extends to the southern
borders of the United States of America.
Trypanosoma rhodesiense
Trypanosoma rhodesiense is the causative agent for
East African sleeping sickness or Rhodesian try­
panosomiasis and is found primarily in the eastern
region of Africa. It produces a virulent form of
sleeping sickness and often results in death within
a matter of weeks if not treated.
The principal insect vectors (tsetse flies)
responsible for the transmissions of T. rhode­
siense are Glossina morsitans, Glossina pallidipes
and Glossina swynnertoni. When feeding on an
3946
T Trypanosomes
infected host, the flies obtain the trypanosomal
stage of the protozoa, which undergoes a period
of development in the midgut region and even-
tually transforms into the epimastigote stage.
The epimastigote stage then migrates to the insect’s
salivary glands and then changes to the elon-
gated infective (metacyclic) trypanosomal stage.
This stage can now be passed to another host
during a blood meal and can initiate infection
or  disease. The transformations usually are
­completed in about 3 weeks.
Once in the human blood, the parasite multi-
plies rapidly. In most infected individuals, there is
an enlargement of the lymph nodes (Winterbot-
tom’s sign) in the post-cervical region. Irregular
fever, headache, joint and muscle pains, and a rash
characterize the disease. T. rhodesiense may be
found in is the blood, lymph nodes and tissues of
humans.
Trypanosoma gambiense
Trypanosoma gambiense is the causative agent of
the disease known as West African sleeping sick-
ness and is found in the western part of Africa.
T.  gambiense is essentially transmitted between
humans and tsetse flies sharing riverine vegetation
habitats. In the case of T. gambiense, two tsetse flies
(Glossina palpalis and Glossina tachinoides) serve
as the primary vectors and are capable of trans-
mitting the trypanosome.
West African sleeping sickness runs a more
chronic course of infection in humans. In the first
or early phase of the disease, infected individuals
show similar clinical and pathological symptoms
when infected with T. rhodesiense. However, the
second or late phase of the disease is unique to
T. gambiense. This phase involves severe damage to
the central nervous system, and may be accompa-
nied by other physical and mental impairment
(mental retardation, speech impediments, swell-
ing of the brains, etc.). At this time, the terminal
sleeping stage develops and gradually the patient
becomes more and more lethargic.
A person can be infected for months or even
years without expressing obvious symptoms of the
disease. When symptoms do appear, the disease is
already at an advanced stage and, without treat-
ment can lead to death. During the early or febrile
stage of the sleeping sickness caused by T. gambi­
ense, the organism occurs in the blood and lymph
node of the infected individual. In the late stages
where there is a development of cerebral symp-
toms, and the organisms can be found in the cere-
brospinal fluid.
In infections with T. rhodesiense or T. gambi­
ense, the presence of trypanosomes in chancre
fluid, lymph node aspirates, blood, bone marrow,
or, in the late stages of infection, cerebrospinal
fluid (in the case of T. gambiense), using micro-
scopic examination and other assays (such as test-
ing for specific antibodies in the blood) are helpful
in diagnosing trypanosomiasis.
In trypanosomiasis with T. rhodesiense or
T.  gambiense, treatment should be started as soon
as possible and is based on the infected person’s
symptoms and laboratory results. The drug regi-
men depends on the infecting species and the
stage of infection. Pentamidine isethionate and
suramin (under an investigational New Drug Pro-
tocol from the CDC Drug Service) are the drugs
of choice to treat the hemolymphatic stage of West
and East African Trypanosomiasis, respectively.
Melarsoprol is the drug of choice for late disease
of T. gambiense with central nervous system
involvement.
Tsetse flies do not normally fly far from their
breeding sites (i.e., streams, lakeshores, lowland
forests with dense growth of shrubs and trees, etc.)
and are attracted to moving objects during the day.
Control methods for the tsetse flies have included
the removal of breeding sources, the use of a vari-
ety of insecticides, and well as traps.
Trypanosoma cruzi
Trypanosoma cruzi was first discovered in 1909 in
Brazil by the scientist Carlos Chagas, in the midgut

of its insect vector the kissing bug (Triatoma infes­
tans). It is known to infect man and a wide range
of domestic and wild species, including dogs, cats
and rodents.
Chagas disease (named after Dr. Chagas) or
American Trypanosomiasis is caused by Trypano­
soma cruzi and is mostly prevalent in Brazil,
Argentina, Uruguay, Chile, Venezuela, Central
America and the Caribbean and afflicts approxi-
mately 15–20 million people. It is a disease pri-
marily affecting low-income people living in rural
areas. Chagas disease is also the leading cause of
cardiac failure for men age 20–40 years in Brazil
due to population and workforce movements into
area infested with the insect vector. Houses built
of adobe, mud, or thatch with cracks in the walls
provides a suitable habitat and breeding habitat
for the insect vectors.
Transmission of the trypanosomes depends
on the presence of the parasite, vectors, reservoirs,
and the host being present in the same location.
Important reservoir animals in the United States
are raccoons, opossums and armadillos. Also, in
addition to animal reservoirs, insect vectors (Tria­
toma infestans, Panstrongylus megistus, Rhodnius
prolixus) belonging to the family Reduviidae may
also transmit the parasite. These bugs tend to
inhabit cool, dark and damp areas, which makes
underdeveloped communities with dilapidated,
inadequate or simply unsanitary housing espe-
cially at risk for the infection.
Transmission of the parasite occurs when
reduviids or kissing bugs that live in the cracks
and crevices of substandard housing ingest the
parasite in the blood from infected humans or
animals. The protozoan Trypanosoma cruzi mul-
tiplies in the digestive tract of the insect and is
eliminated in the feces on a person’s skin, usually
while the individual is sleeping at night. The indi-
vidual often rubs the contaminated feces into a
bite wound, an open cut, the conjunctiva or other
mucous membranes. In addition, transmission
through blood transfusion and the placenta have
been reported. Animals may also become infected
with the protozoa via similar methods, or by
Trypanosomes
T 3947
actually eating infected bugs. Transmission does
not occur through the bite of the insect vector.
Some individuals may be infected and not
show any symptoms of the disease until many
years after infection (chronic form). The most
recognized symptom of acute Chagas disease
(especially in children) is the Romana’s sign, or
the swelling of the eye on one side of the face.
Other symptoms may include fever, fatigue,
enlarged liver and spleen and swollen lymph
nodes, followed by convulsions and cardiac
involvement. In infants and very young children
with acute Chagas disease, cardiac arrest and
death may result.
Beside the Romana’s sign, and because many
individuals do not show symptoms of the disease,
xenodiagnosis (process whereby a small sample is
injected into the body of an animal and after a
period of time, the animal is tested for the amas-
tigote form) may be able to determine the pres-
ence of the protozoan. Another form of laboratory
diagnosis involves the culture of tissue aspirates
especially from the lymph nodes on culture plates
(N.N.N. culture plates).
No vaccination or drug is both safe and effec-
tive in the prevention and treatment of Chagas
disease. Some drugs (anti-inflammatory doses of
glucocorticoids and other supportive measures)
may help to alleviate the symptoms associated
with Chagas disease.
The usual method of insect control is the
application of residual insecticides to the inte-
rior surfaces and roofs of the houses. In rural
areas where the bugs may live and breed in sub-
standard housing, plastering the walls to cover
up cracks and crevices, or replacing homes with
bricks and cement blocks can significantly con-
tribute to the elimination of the insects inside of
the home. The use of bed nets while sleeping has
also shown to be effective in preventing bites
from the bug. Outside, removal of the breeding
sites of animals where the insects are found may
also help to reduce the population of the insect
vector, thereby reducing possible contact with
the human host.
3948
T Trypanosomes
Trypanosomes in Animals
Some trypanosome species have been reported from
wild and domesticated animals. These trypanosomes
may be transmitted biologically or mechanically by
various biting insects. Glossina or tsetse fly have been
shown to transmit Trypanosoma rhodesiense, T.
gambiense, T. brucei, T. congolense, T. vivax, T. evansi
and T. suis. While insects such as tabanids have been
shown to mechanically transmit T. evansi in animals,
T. equiperdum in horses and camels is transmitted
by direct blood contact during copulation. Some
other trypanosomes, such as T. thelieri and T. cervi,
are found in animals in the United States, but these
species of the parasite are not pathogenic.
Of the various diseases associated with trypano-
somes in which wild and domesticated animals are
involved, T. brucei produces a disease called nagana
which infects a wide range of animals, especially cat-
tle. This trypanosome normally produces chronic
infections in animals and may also produce different
clinical signs. A severe acute case may be seen in
horses, donkeys, dogs, goats and camels. In cattle, a
chronic but sometimes fatal form of infection exists
when the animals are infected by T. brucei.
When livestock are infected with T. brucei,
they are mass-treated with drugs such as ethidium,
isomethamidium or berenil. These drugs are effec-
tive, both for treatment and for prophylaxis, but
may also be mutagenic. Slaughtered cattle fed these
drugs may only be used for human consumption
several months after drug treatment in order to
avoid any residual effect of the drugs.
Recent Findings and Issues
Associated with the Trypanosomes
Despite some progress with the trypanosomes,
resurgence of the parasite remains a concern. Dur-
ing the nineteenth and twentieth centuries, try-
panosomiasis was among the vector-borne diseases
that prevented the development of large areas in
the tropics, especially Africa. Fortunately, by 1910,
it  was shown that trypanosomes require blood
sucking insect vectors, and over the next 50 years
prevention and control programs were applied to
curb the vectors. These programs placed emphasis
on the elimination of the vector breeding sites, envi-
ronmental hygiene and the limited use of chemical
insecticides. However, the success of curbing the
vectors was short lived, because by 1970 a reemer-
gence of the vectors was seen and later intensified,
over the next 20  years. Trypanosomes now infect
over two million people each year.
Several factors have been implicated for the
increase and reemergence of trypanosome related
diseases. These factors include the following:
Civil and Political Unrest
Many of the affected African countries are cur-
rently experiencing wars, leading to the disruption
of the available forms of controlling both the
spread of the vector, and the parasite. War has also
aided in the disruption of the ecosystem, and the
displacement of the vectors from their native
breeding grounds. In addition, many of the citi-
zens of the affected countries have also been dis-
placed, and are affected by the ongoing poverty.
Competing National Health
Priorities
Currently, most of the available local resources are
being put into research involving the prevention
and cure of AIDS and malaria. Due to the efforts
to solve the problems related to these diseases,
funding for trypanosomiasis is limited.
Lack of Funding Support to Aid in
the Availability of New Drugs,
Vector Control and Diagnostic
Tests
There has been very limited funding to support
new drugs, vector control, and diagnostic tests.
Due to the high level of poverty in most of the

affected countries, most individuals cannot
afford to buy the drugs to treat their illnesses. It
is estimated that less than 10% of the infected
individual are treated. Furthermore, there are no
vaccines to protect the uninfected population
from the parasite, because the parasite is able to
mutate in order to evade the immune system.
Recently, several organizations including
the World Health organization, the World Bank
and some pharmaceutical companies have
decided to look into the problem of the reemer-
gence of trypanosomiasis. They have decided to
employ the following methods to control the
disease: increase research on vaccines, provide
environmentally safe insecticides, educate the
masses on the parasite and how to deal with it,
and increase the availability of drugs to the
infected areas so that people can afford them.
Only by these concerted efforts will we be able to
have a significant affect on trypanosomiasis.
 Tsetse Flies
 Glossina spp. (Diptera: glossinidae)
 Chagas Disease or American Trypanosomiasis
 Sleeping Sickness or African Trypanosomiasis
References
Barrett MP (1999) The fall and rise of sleeping sickness.
­Lancet 353:1113–1114
Beaty B, Marquardt WC (1966) The biology of disease vectors.
University Press of Colorado, Boulder, 632 pp
Bogitsh BJ, Cheng TC (1990) Human parasitology. Saunders
College, Philadelphia, 435 pp
Lambrecht FL (1985) Trypanosomes and hominid evolution.
Bioscience 35:640–646
Mulligan HW (1970) The African trypanosomiasis. Wiley,
New York, 950 pp
Welburn SC, Fevre E, Coleman P (1999) Sleeping sickness
rediscovered. Parasitol Today 15:303–305
Trypanosomiasis
A disease of vertebrate animals caused by
trypanosomes.
 Trypanosomes
 Chagas Disease or American Trypanosomiasis
 Sleeping Sickness or African Trypanosomiasis
Tsetse Flies, Glossina spp. (Diptera: Glossinidae)
T 3949
Trypsin Modulating Oostatic
Factor
(TMOF) In female mosquitoes, the decapeptide
hormone TMOF is synthesized by the ovarian fol-
licle after a blood meal, affects the midgut cells,
and regulates digestion.
Tsetse Flies, Glossina spp.
(Diptera: Glossinidae)
David A. Dame1,2
1
University of Florida, Gainesville, FL, USA
2
University of Bristol, Bristol, England
Tsetse flies (Glossina spp.), pronounced “set-see” or
“tet-see,” are found only in Africa where they range
discontinuously from coast to coast, limited primar-
ily by environmental and ecological factors. They
infest 37 countries and about 10 million km2 of sub-
Saharan Africa. Their negative impact on the poten-
tial for economic development is immense, and they
often have been blamed for the widespread poverty
that exists in tropical and sub-tropical Africa.
Tsetse flies have a significant impact on human
activities because they are obligatory blood feeders
(Fig. 111) and they transmit blood parasites of the
genus Trypanosoma, which cause sleeping sickness.
When untreated or treated too late, sleeping sick-
ness is a fatal disease. Because many tsetse species
feed on humans and domestic animals, as well as
on the wild animals that serve as immune reser-
voirs of the parasites, the potential for transmission
can be very high. The incidence in fly populations
of trypanosomes that cause animal trypanosomo-
sis (trypanosomiasis), for example, often exceeds
20% and sometimes is as high as 90%.
Animal Sleeping Sickness
The major impact of animal sleeping sickness,
nagana, is to preclude maintenance of domestic
animals. Thus, this disease has restricted cattle
3950
T Tsetse Flies, Glossina spp. (Diptera: Glossinidae)
Tsetse Flies, Glossina spp. (Diptera: Glossinidae),
Figure 111  Adult tsetse fly, Glossina morsitans,
engorged with blood. (Photo by D.F. Lovemore.)
­ roduction in the tsetse-infested areas to less than
p
15% of the carrying capacity of the land. Without
draught animals, inhabitants have been limited to
subsistence level farming because it is necessary to
till the land by hand. Without cattle and other
domestic animals, severe protein deficiency is wide-
spread. The estimated annual cost and losses in
potential animal and crop production is $4 billion.
Preventive or curative drugs for control of
nagana in livestock are only partially effective and
often uneconomical due to the development of
resistance. Trypanotolerant livestock, such as the
N’ Dama cattle in western Africa, have provided
partial relief, but under heavy fly challenge these
small cattle also succumb to the parasite. Immuni-
zation against trypanosomes has not as yet been
successful due to the antigenic plasticity of the
parasites. Thus, the primary means of preventing
transmission is by elimination of contact between
vectors and hosts by control of the vectors. Tsetse
flies are the only significant vectors of trypanoso-
mosis, although some limited mechanical trans-
mission results from the feeding activities of other
biting flies (Stomoxys, Tabanus, etc.).
Human Sleeping Sickness
Human sleeping sickness, transmitted by tsetse
flies from man to man in western and central
Africa (Trypanosoma gambiense) and from animal
reservoirs to man in eastern and southern Africa
(Trypanosoma rhodesiense), has a lower incidence
than animal trypanosomiasis. This is because of
the relatively fewer encounters between flies and
humans than between flies and livestock, and also
because of the much lower rate of T. gambiense
and T. rhodesiense infections in fly populations. In
1999, over 45,000 new human cases were reported,
but due to incomplete reporting it is estimated
that the actual human incidence was probably
closer to 300,000–500,000. Historically, millions
have been killed by trypanosomosis. Curative
drugs are harsh, but can be effective with early
diagnosis. Neurological disorders are common
following recovery from infection. Due to civil
unrest and disruption, combined with reduced
control effort in many infested regions, the 60 mil-
lion individuals estimated to be at risk of infection
are subject to increased likelihood of severe dis-
ease outbreaks.
Tsetse Biology
Vector control is complicated by such a wide dis-
tribution of the flies, which usually are found in
broad belts that are more or less continuous and
often cross international boundaries. They can be
difficult to detect in areas where the fly popula-
tions are advancing or at low density. Furthermore,
there are over 20 distinct vector species, although
not all are important vectors and often several spe-
cies co-exist in the same areas (Table 16).
Members of the morsitans group, which
inhabits savannah grasslands, and the palpalis
group, which is generally found in lacustrine and
riverine situations, are the primary vectors of
both human and animal trypanosomosis.
Because of ecological requirements, the palpalis
group is generally restricted to areas near the
dense vegetative cover found in aquatic situa-
tions, whereas species of the morsitans group
have a wider range of ecological niches and are
more widely dispersed.

Tsetse Flies, Glossina spp. (Diptera: Glossinidae), Table 16  Habitat relationships of Glossina spp.: savan-
nah (morsitans), riverine (palpalis), and forest (fusca) group tsetse flies
Morsitans Palpali
austeni calignea
longipalpis fuscipes fuscipes
morsitans centralis fuscipes martini
morsitans morsitans fuscipes quanzensis
morsitans submorsitans pallicera pallicera
pallidipes pallicera newsteadi
swynnertoni palpalis gambiensis
  palpalis palpalis
  tachinoides
   
   
   
   
   
All species are larviparous, not laying eggs
but producing living young that have been nur-
tured in the uterus of the female fly for several
days. They deposit only one offspring at a time
and, even though the adults occasionally survive
for as long as 90–100 days in nature, their biotic
potential is quite low compared to that of other
dipteran species (Fig.  112). The larvae usually
burrow into the soil or other suitable substrate,
where they pupate and develop for 3–4 weeks or
more before emerging as adults. Thus, at any given
time a significant portion of the fly population is
underground, a fact that plays an important role
in control strategy.
The adults move about in a diurnal pattern,
governed to a great extent by temperature. For
example, in the summer in southern Africa,
G. m. morsitans feeds in the mornings when the
temperature is moderate, seeks shelter during
midday when the temperature is high and the
insect exhibits negative phototaxis, and resumes
feeding as the temperature declines in the latter
part of the day. At night the flies rest. Nutritional
Tsetse Flies, Glossina spp. (Diptera: Glossinidae)
T 3951
Fusca
brevipalpis
fusca congolensis
fusca fusca
fuscipleuris
haningtoni
longipennis
medicorum
nashi
nigrofusca hopkinsi
nigrofusca nigrofusca
schwetzi
severini
tabaniformis
vanhoofi
requirements cause the flies to seek blood meals
about every third day, and the males also actively
visit host animals in search of mates feeding
there. In this process, the sexually appetitive
males move about several times daily, often rest-
ing on host animals grazing or traversing the
bush. In the course of these activities, the flies
alight on numerous resting sites in their preferred
habitat. The preferred resting sites vary some-
what for the different species.
Tsetse Behavior and Ecology in
Relation to Control
The association of tsetse flies with particular
­vegetation types has played a major role in deter-
mining control practices. Riverine species of the
palpalis group are generally found within a short
distance of their breeding sites, in or close to
the riverine vegetation canopy that provides pro-
tection from sunlight, high temperature, and
lower  humidity of the surrounding, more open
3952
T Tsetse Flies, Glossina spp. (Diptera: Glossinidae)
Tsetse Flies, Glossina spp. (Diptera: Glossinidae),
Figure 112  Adult female tsetse fly depositing fully
developed larva.
v­ egetation. This habitat affords the fly an environ-
ment replete with a variety of hosts, and inciden-
tally provides direct contact with humans and
domestic animals when they come to the water.
Partial or complete removal of the riverine vegeta-
tion results in the reduction or elimination of
these tsetse flies. However, in more humid areas,
species of the palpalis group may be found well
away from surface water. Glossina tachinoides, for
example, has been observed to breed in perido-
mestic habitats, where bush encroachments around
villages have allowed flies to find suitable resting
and larviposition sites well away from the typical
riverine situation. Similar observations with spe-
cies of the morsitans group have revealed their
preferences for selected resting sites and their
dependence upon certain characteristics of the
habitat for survival. Ruthless removal or discrimi-
native clearing of selected portions of the habitat
results in major reductions of fly density because
the flies cannot then find suitable protective cover
when environmental stresses are maximal.
Similarly, feeding behavior characteristics of
the tsetse fly have provided a means for reducing
population density with a corresponding reduc-
tion in the risk of trypanosomosis. Most tsetse
species feed on a variety of animals but prefer cer-
tain hosts, sometimes riverine. For example, in
Zimbabwe, G. m. morsitans feeds on numerous
hosts, but prefers bushpig, warthog, bushbuck, and
kudu. Thus, by selective reduction of these four
species, the fly density could be reduced along
with the incidence of trypanosomosis.
However, for economic, environmental and
aesthetic reasons, game reduction and wide-scale
bush clearing are no longer acceptable control
measures.
Awareness of specific tsetse resting niches
spurred the development of selective application
methods for the organic insecticides that first
became readily available in the 1940s. Because
most species have well defined resting site prefer-
ences, such as the lower boles of trees of certain
diameters, application of persistent insecticides to
these sites provided excellent control without
resort to broadspread applications. Furthermore,
since the flies have a long life span, during which
the majority probably move less than 1,000  m
from their origin, not all resting sites needed to be
sprayed to achieve a high level of control. Flies
below ground in the pupal stage eventually emerge
and sooner or later come to rest on a treated sur-
face. Treatment of 10–20% of the preferred resting
sites in some tsetse habitats was sufficient to elimi-
nate or substantially reduce the fly population
when the toxicant persisted for several months.
Approaches to Fly Management
Glossina spp. are extremely susceptible to insecti-
cides. Aerial applications of very low rates of

­nonpersistent aerosols repeated at 2–3 week inter-
vals have been used to initially control the ambi-
ent fly population and then the flies that have
recently (0–15 days) emerged, thereby precluding
reproduction and eliminating the fly population
after six or seven spray cycles. Alternatively, selec-
tively placed helicopter applications of persistent
insecticides have been used with dramatic results.
These applications were discriminative in that they
included only those habitats that offer refuge for
the fly in the dry season, when tsetse fly distribu-
tion typically is more restricted. Most of the appli-
cation was deposited on the leaves of the upper
canopy, where tsetse rest at night. These residual
types of application were particularly effective in
areas with discrete wet and dry seasons.
But the broadspread application of pesticides
has given way to the use of attractants and trap-
ping to expose the flies to spot treatments of pesti-
cides. Both visual and olfactory components are
involved in tsetse host-seeking behavior. In the
1970s, animal emanations attractive to tsetse flies
were found to be highly effective for trapping sev-
eral species of tsetse, especially when combined
with suitable visual attractants. By utilizing a per-
sistent insecticide in conjunction with attractant
devices, significant population reductions can be
achieved in a matter of months. Such trapping
provides a relatively inexpensive method of con-
trol, and because the pesticide is incorporated into
the attracting device the probability of environ-
mental contamination is low.
However, the attractant approach does not
guarantee elimination of the vector, and thus the
disease, even though fly population density in
most situations can be reduced to well below the
threshold level necessary to maintain regular
transmission. Extensive study and operational
level trials of the sterile insect technique have
demonstrated the feasibility of this approach for
area-wide elimination of tsetse where geographi-
cally isolated fly populations already have been
reduced to low density. Used to eliminate Glossina
austeni from the main island in Zanzibar, the inhi-
bition of natural reproduction with sterile fly
Tube Moths (Lepidoptera: Acrolophidae)
T 3953
releases after reducing fly density by trapping is an
environmentally friendly method of control that
has potential application for most of Africa.
 Trypanosomes
 Sleeping Sickness or African Trypanosomiasis
 Histroy of Insects
References
Buxton PA (1955) The natural history of tsetse flies. H. K. Lewis,
London, +47 plates, 816 pp
Food and Agriculture Organization (1992) Programs for the
control of African animal trypanosomiasis and related
development. FAO Animal Production and Health paper
100. In: Proceedings of Symposium, Harare, Zimbabwe.
www.fao.org/docrep/004/to559e/to599e00.htm
Leak SGA (1998) Tsetse biology and ecology: their role in the
epidemiology and control of trypanosomosis. CABI,
Wallingford, 592 pp
Mulligan HW (ed) (1970) The African trypanosomiases.
George Allen and Unwin, London, 950 pp
World Health Organization (1998) Control and Surveillance
of African trypanosomiasis. Technical Report Series
No. 881, vi + 113 pp. www.who.int/health-topics
Tube-Making Caddisflies
Members of the families Polycentropodidae and
Psychomyiidae (order Trichoptera).
 Caddisflies
Tubercle
A small raised area or extension of the integument.
In caterpillars, a hair often originates from these
raised areas.
Tube Moths (Lepidoptera:
Acrolophidae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Tube moths, family Acrolophidae, total 270 species
in the New world, mostly in the large genus
3954
T Turgor

Acrolophus; actual fauna likely exceeds 350 spe-

cies. The family is part of the superfamily Tine-
oidea, in the section Tineina, subsection Tineina,
of the division Ditrysia. Two subfamilies are used:
Amydriinae and Acrolophinae (formerly included
in Tineidae). Adults small to medium size
(9–60  mm wingspan), with rather robust bodies
and roughened head scaling and usually large
recurved labial palpi; haustellum naked (unscaled);
maxillary palpi minute, 2-segmented. Maculation
is mostly somber hues of brown or black, some-
times with some spotting and other markings.
Adults are mostly nocturnal, but some may be cre- Tube Moths (lepidoptera: A ­ crolophidae),
puscular. Larvae are root feeders, mostly of grasses, ­Figure 113  Example of tube moths
and construct long silken tubes to feed on host- ­(Acrolophidae), Acrolophus plumifrontellus
plant roots. A few are economic, mainly as turf ­(Clemens) from Florida, USA.
grass pests (Fig. 113).

funnel with a wire mesh insert that supports the

References
Becker VO, Robinson GS (1981) Neotropical taxa referable to
Acrolophus (Lepidoptera: Tineidae). Syst Entomol
6:143–148
Davis DR, Milstrey EG (1988) Description and biology of
Acrolophus pholeter (Lepidoptera: Tineidae), a new
moth commensal from gopher tortoise burrows in
­Florida. Proc Entomol Soc Washington 90:164–178
Hasbrouck FF (1964) Moths of the family Acrolophidae in
America north of Mexico (Microlepidoptera). Proc US
Natl Mus 114:487–706
Hinton HE (1955) On the taxonomic position of the Acrolo-
phinae, with a description of the larva of Acrolophus
rupestris Walsingham (Lepidoptera: Tineidae). Trans R
Entomol Soc London 107:227–231
Turgor
The distension of living tissue, usually plant tissue,
due to internal pressures (hydration).
plant material above a reservoir containing alco-
hol or another preservative. An incandescent light
bulb is  suspended above the funnel to provide a
source of heat and drying, encouraging the move-
ment of the arthropods. As the arthropods move
about, particularly as they move deeper into the
funnel to escape drying of the plant material, they
slip down the funnel into the reservoir containing
liquid, where they are retained for identification.
This technique is useful for many arthropods, but
not for those that may fly to escape, or those that
are very fragile and perish from desiccation before
they can escape the plant material. A cover is often
provided to eliminate escape by insects capable of
flight, and to more efficiently direct the heat
­generated by the light bulb. A Tullgren funnel is a
modified Berlese funnel, with the difference being
the light bulb, but the distinction is not usually
appreciated and most Tullgren funnels are called
Berlese funnels.

Tullgren Funnel
An extraction devise used to separate and extract
small arthropods from leaf litter or similar mate-
rial. A Tullgren funnel normally consists of a
Tularemia
Also known as rabbit fever, this is a serious infec-
tious disease caused by the bacterium Francisella
 Turfgrass Insects of the United States: Biology and Management
tularensis. The disease is endemic in North
America, and parts of Europe and Asia. The pri-
mary vec­tors  are ticks and deer flies, but occa-
sionally the disease can also be spread through
other arthropods. Animals such as rabbits and
muskrats serve as reservoir hosts. The disease is
named after Tulare County, California, where in
1911 the disease was studied in squirrel and
human populations.
 Ticks
Tumbling Flower Beetles
Members of the family Mordellidae (order
Coleoptera).
 Beetles
Tungidae
A family of fleas (order Siphonaptera).
 Fleas
Turfgrass Insects of the United
States: Biology and Management
R. Chris Williamson1, Rick Brandenburg2
Sarah Thompson2
1
University of Wisconsin, Madison, WI, USA
2
North Carolina State University, Raleigh, NC,
USA
Turfgrasses are grown throughout the United
States, covering over 30 million acres (12.2 mil-
lion hectares). As urban environments have
grown, the use of turfgrass in the U.S. has
increased over the past several decades. Subse-
quently, large areas of land have been developed
with dense, dark green, uniform turf providing
numerous practical, recreational, and ornamen-
tal uses. Uses for turfgrass include dense turf for
soil stabilization and erosion prevention; run-
ways for rural airports; cemeteries; parks and
T 3955
recreational facilities for relaxation, picnics and
general family activities; sports facilities and
complexes including baseball, cricket, football,
lawn bowling, polo, soccer, tennis and, especially,
golf courses. Turfgrasses often are considered the
most intensively managed plantings in urban
landscapes. It is estimated that $45 billion is spent
per year in the U.S. for turfgrass culture in its
many forms.
Turfgrass can be designated as either cool-
season or warm-season grasses depending on their
climatic adaptations. These two categorical desig-
nations can be further divided into four distinct
turfgrass adaptation zones in the U.S. including (i)
cool, humid; (ii) cool, arid or semi-arid; (iii) warm,
humid; and (iv) warm, arid or semiarid. Despite
these partitioned zones, there is considerable over-
lap of the species of turfgrass grown in various
regions of the U.S. As a result, it is rather difficult
to effectively provide an accurate description for
the boundaries of specific insect pests and nearly
impossible to give a comprehensive classification
for all turfgrass pests including disease pathogens,
insects and weeds.
Some insect pests are host specific, feeding
only on certain turfgrass species or types, while
others are non-discriminate, infesting a diversity
of grass and broadleaf plant materials. An insect
pest such as the European chafer typically only
infests cool-season areas, whereas mole crickets
and fire ants infest warm-season turfgrasses.
Preference of an insect pest can be either for a
host (e.g., turf-type or species) or it may be a
reflection of the geographic range of the pest.
Destructive turfgrass insects can be divided into
three primary groups according to the habitat in
which the destructive life stage spends its life in
the turfgrass ecosystem. They include (i) leaf and
stem, (ii) thatch, and (iii) root zone/soil. This
method of grouping is highly valuable because
specific control tactics or strategies implemented
for each group have a direct bearing on the effec-
tiveness or satisfaction of control for the respec-
tive insect pest. Some insects are capable of
occupying more than one habitat during its
3956
T Turfgrass Insects of the United States: Biology and Management
development, and may even occupy all three
habitats during its various life stages. Thus, a
modified designation of turf habitats has been
suggested including (i) foliage and stem, (ii)
crown and thatch, and (iii) soil.
Effective control of any pest (plant pathogen,
insect or weed) can be accomplished ­successfully
only with a comprehensive understanding of
both the host and the pest. Factors such as growth
habits and cultural requirements of the host
(turfgrass) must be understood. Knowledge of
the biology, behavior, ecology, life history for the
host and pest are critical for making decisions.
Symptomology or type of damage caused by the
pest(s), accurate identification of the pest, infor-
mation regarding the time of year, growth stage
of the host and the pest, and environmental con-
ditions under which pest damage is most likely to
occur are all important factors that also should
be understood. This information is the founda-
tion for the Integrated Pest Management (IPM)
philosophy. IPM is a commonsense approach to
pest management that is effective and environ-
mentally responsible. IPM relies on a combina-
tion of preventative and corrective measures to
keep pest densities below levels that would cause
unacceptable damage. IPM includes sampling
and monitoring, accurate pest identification,
decision-making, appropriate intervention, fol-
low-up, and detailed record keeping. In terms of
the appropriate intervention tactic, several con-
trol options are available including biological,
chemical, cultural, and plant resistance. IPM is a
decision-making process that does not preclude
the use of pesticides, however, it does not  rely
upon chemical control as its first line of defense.
The ultimate goal of IPM is to manage pests effec-
tively, economically, and with minimal risks to
people and the environment. For this ­reason,
turfgrass managers must constantly be aware of
potential pest problems that they may experi-
ence. The listing that follows provides vital infor-
mation for the major insect and mite pests
affecting turfgrass in the US (Figs. 114 and 115).
Foliar and Stem Inhabitants:
Surface Chewing and Sucking
Insects
Armyworms (Lepidoptera: Noctuidae)
Armyworms get their name because of their gre-
garious nature of crawling in large numbers from
one field or feeding site to another after they have
exhausted their food supply. Although these pests
are often sporadic, they do have the potential for
outbreaks. Most armyworm larvae are thick-
bodied, hairless, striped caterpillars that chew on
the foliage of turfgrass. There is one armyworm
species that frequently attacks turfgrasses in both
the northern and southern United States, the
“common” or “true” armyworm.
Armyworm, Pseudaletia unipuncta
(Hawthorn)
Frequently referred to as the “common” or “true”
armyworm in order to differentiate it from other
armyworm species, the armyworm is a native
species that is distributed throughout the United
States and southern Canada east of the Rockies.
Armyworm adults are evenly pale-brown to
grayish-brown moths with a wingspan of approx-
imately 38–40 mm. The distinct white spot in the
center of their front wings readily identifies them.
The hind wing is dirty white. The female adult
moths lay pearly white eggs, 0.5 mm diameter, in
masses containing 20 to several hundreds of eggs.
Young larvae, more than 2  mm long, are pale
green. Mature larvae range from 35 to 50 mm in
length, grayish to greenish-brown, with two pale-
orange stripes along each side of the body and
another pale-colored, broken stripe down the
middle of the back. The head capsule is honey-
combed with dark lines. Pupae are reddish-
brown, about 16–19 mm long and shaped like a
football.
 Turfgrass Insects of the United States: Biology and Management
T 3957

Turfgrass Insects of the United States: Biology and Management, Figure 114  Some important turfgrass
pests: top left, green June beetle; top right, Japanese beetle; second row left, fall armyworm; second row
right, bronzed cutworm; third row left, a June beetle larva (white grub); third row right, black turfgrass
ataenius adults and larva; bottom row left, glassy cutworm; bottom row right, black cutworm.
3958
T Turfgrass Insects of the United States: Biology and Management

Turfgrass Insects of the United States: Biology and Management, Figure 115  Additional important
­turfgrass pests: top row left, billbug adult; top row right, billbug larva; second row left, variegated
­cutworm; second row right, tropical sod webworm; third row left, tawny mole cricket adult; third row
right, southern mole cricket adult; bottom row left, immature chinch bug; bottom row right, red imported
fire ant.
 Turfgrass Insects of the United States: Biology and Management
Armyworm caterpillars feed on a wide range
of grasses. They especially like barley, corn, millet,
oats, rice, rye and wheat. When such food supplies
are depleted, they will attack nearby turfgrass.
Young larvae initially feed on tender foliage result-
ing in a skeletonized appearance. Third instar and
older larvae are primarily nocturnal and consume
all or part of the leaf.
Armyworms overwinter as partially grown
larvae or pupae in the southern half of the U.S.
and possibly as partially grown larvae in the
northern half. Infestation in the North may also
be the result of spring migration flights of adults.
In the temperate United States, there are typi-
cally two generations (broods) per year. The
number of annual broods depends primarily on
latitude. The first generation is a result of annual
moth migration in the spring (i.e., late April
through May). Once the eggs are laid, they typi-
cally hatch in as few as 3 days. Larvae usually go
through six instars over a period ranging from
20 to 48 days. Pupation occurs in the soil and the
duration of the pupal stage averages 15  days.
Adult armyworm moths are nocturnal, with
most flight activity occurring within 2  hours
after sunset. A second generation occurs during
June and July. In the southern regions, four to
five generations may occur. Infestations in turf-
grass are often most severe following drought
conditions. Populations have a tendency to fluc-
tuate widely from generation to generation and
year to year.
Fall Armyworm, Spodoptera
frugiperda (J. E. Smith)
The fall armyworm is found throughout much of
the South and is a frequent problem in turfgrass,
especially in the Southeast westward into Texas,
New Mexico, Arizona and southern California. It
does not overwinter outside of Florida and the
immediate Gulf Coast area, and must disperse to
reinfest areas each year. Populations usually do
T 3959
not reach the more northern areas until very late
summer or fall.
Fall armyworm moths have a wingspan of
about 38  mm and the forewings are generally a
dark gray and mottled in appearance. There is a
white spot near the tip of the forewing and a light
diagonal mark in the middle of each wing. The
back wings are white. The eggs are laid in clusters
of 50–100 and are initially greenish white, but
soon turn dark. The egg clusters often look gray
and fuzzy from the scales of the female’s wings.
The caterpillars are green to brown, to almost
black. The head is marked by a typical inverted “Y”
on the “face” or front. There is a longitudinal dark
stripe that runs the length of the body and a fainter,
pale mid-dorsal stripe. Each abdominal segment
has four small black dots. The fully grown larvae
are 35–50 mm long. The pupa is 13 mm long and
is found in the soil. It is reddish-brown, somewhat
football shaped, and becomes black prior to emer-
gence of the moth.
Fall armyworms feed on a wide range of
plants, but prefer grasses of all types. However,
this pest is most commonly associated with ber-
mudagrasses in the southern U.S. They can and
do feed on both cool and warm season turfgrasses
and are often most likely to attack lush, green,
dense areas of turf. Fall armyworms are very com-
mon problems in areas that have recently been
sodded or sprigged. The small larvae skeletonize
the leaf blades while larger larvae may consume
all above-ground plant parts. The turf also may
turn brown and look dead from drought stress.
The larvae often move from heavily damaged
areas into new food sources. Warm season turf
usually recovers from such feeding, but if it occurs
late in the season, the turfgrass may be stressed
going into the winter.
Fall armyworm moths are active at night
and may be attracted to lights. They lay eggs on
a wide range of objects, usually light-colored,
that are adjacent to turf areas. These sites may
include fence posts, metal buildings, flagpoles,
the underside of leaves of various landscape
plants, gutters, etc. Eggs hatch quickly in warm
3960
T Turfgrass Insects of the United States: Biology and Management
temperatures and the small larvae spin down on
silken thread to the turf surface and begin feed-
ing. Small caterpillars feed at any time of the
day, but larger ones feed more at night to avoid
predation by birds. The fall armyworms will
feed for 2–3 weeks and then burrow into the soil
to pupate. New moths emerge 2 weeks later and
the cycle starts again. Multiple infestations can
occur in the same location and population as
high as 100 per square meter have been observed.
The number of generations per year depends
upon location and migration of the moths.
Migration varies each year depending upon
weather conditions, which are responsible for
enhancing the migration of the moths. In the
extreme South, four or more generations may
occur and the damage from the larvae may
begin in the spring. In locations further north,
only one generation will occur and it may not
be seen until August or September. Wet springs
sometimes increase the likelihood of fall army-
worm outbreaks.
Chinch Bugs (Hemiptera: Lygaeidae)
Chinch bugs damage turfgrass by sucking plant
juices from stems (i.e., leaf sheaths) and crowns,
causing gradual yellowing and eventual dead
patches of turf. Damage occurs predominantly
during hot, dry periods of time in mid- to late
summer. Sunny areas are often most heavily
infested. There are four chinch bug species that are
important turfgrass pests in the United States (i)
the hairy chinch bug, (ii) the common chinch bug,
(iii) the “buffalograss” chinch bug, and (iv) the
southern chinch bug.
Hairy Chinch Bug, Blissus
leucopterus hirtus Montandon
The hairy chinch bug occurs across the eastern
Canadian provinces and from the northeastern
United States to the Middle Atlantic states south to
Virginia and west to Minnesota.
Chinch bugs have gradual metamorphosis,
thus the immature (nymph) life stage is similar in
physical appearance and feeding habits to the
adult, however, there is variation in size, color and
wing development. There are five nymphal stages;
the first instar nymphs are tiny, approximately
2.5 mm long, bright red with a white band across
the abdomen. As the nymphs develop and mature,
their color changes from bright red to orangish-
brown and ultimately black once they reach the
fifth instar. Hairy chinch bug adults are approxi-
mately 6.0–6.4  mm long and 1.0  mm wide, and
females typically are slightly larger than males.
Adults range in color from grayish-black to black
and white and often are covered with fine hairs
and the legs are typically a dark, burnt-orange tint.
There is a triangular-shaped marking in the mid-
dle of the outer edge of each wing. Populations of
hairy chinch bugs may consist of mostly long-
winged (macropterous) or short-winged (brac-
hypterous) individuals, or contain both wing
forms. The long-winged chinch bugs have wings
that extend to the tip of the abdomen, and short-
winged chinch bugs have wings that extend only
halfway to the tip. The adults lay eggs that are tiny,
elongate, and bean-shaped; initially they are white,
but become orange-red within a few days prior
to hatching.
The hairy chinch bug is one of the most
important insect pests of northern turfgrasses,
especially home lawns. It prefers cool-season
turfgrasses including creeping bentgrass, fine
fescues, Kentucky bluegrass, and perennial
ryegrass. However, hairy chinch bugs will feed
also on zoysiagrass, a warm-season turfgrass
species that occasionally occurs where cool-­
season turfgrasses dominate. Both the adults and
nymphs cause damage to turfgrass plants by
inserting their piercing-sucking mouthparts into
stems and crowns, extracting plant juices while
pumping toxic salivary fluids into the plant. Sub-
sequently, turfgrass plants are damaged by the
loss of plant fluids as well as the clogging of the
 Turfgrass Insects of the United States: Biology and Management
conducting tissues within the stems. Generally,
hairy chinch bug occurs sporadically in scat-
tered aggregations rather than uniformly dis-
tributed across the turf. Damage typically occurs
during hot, dry periods in mid- to late summer
when turf is commonly experiencing drought
stress symptomology. Additionally, hairy chinch
bug prefers open, sunny areas of turf that have
heavy thatch accumulation as well as high per-
centages of perennial ryegrass and fine-leaf fes-
cue. Initial damage often appears as irregular
patches of wilted, yellowish-brown turf that fre-
quently is mistaken for drought stress. As popu-
lations grow, often reaching 200–300 bugs per
0.1 m2, feeding damage intensifies and damaged
patches of turf begin to coalesce into large areas
of dead or dying turf that does not recover
regardless of irrigation or rainfall.
Typically there are two generations per year
in the temperate United States; however, in the
most northern portion, as well as Canada, there
is only one generation per year. The adults over-
winter in the turfgrass thatch, leaf litter, and sim-
ilar sites. They become active in the early spring
as temperatures reach 10°C. Thereafter, the adults
feed and mate for approximately 2 weeks before
females begin laying eggs in mid-April to May.
In  areas where there is only one generation per
year, egg-laying may be delayed by several weeks
and occurs over an extended period. Females lay
as many as 20 eggs per day for a period of about
2–3 weeks. Eggs typically are laid in leaf sheaths
or in the thatch. Because insects are cold-blooded
animals, they are dependent on temperature, thus
the developmental rate of eggs and nymphs var-
ies within species and geographic range. Eggs
that are laid during April may require as long as a
month to hatch, and eggs laid in midsummer
may hatch in as few as 7–10  days. Where two
generations occur, the first generation typically
matures in 4–6  weeks, usually by mid-July. The
second-generation adults then begin laying eggs
from mid-July through late August. These eggs
hatch soon thereafter, and the nymphs complete
development by September or October. As cooler
T 3961
temperatures prevail, the adults seek out pro-
tected sites to overwinter. The most extensive
damage to turf commonly occurs during periods
of heat and drought stress, typically in late July
and August when the first generation adults are
actively feeding and laying eggs.
Common Chinch Bug, Blissus
leucopterus leucopterus (Say)
The common chinch bug is an occasional pest of
turf, especially in the Great Plains region. It feeds
primarily on small grains and other field crops,
however, sometimes it damages turfgrass, espe-
cially when located in close proximity to maturing
small grain fields. Several turfgrass species that are
likely to be attacked by the common chinch bug
include creeping bentgrass, fescues, Kentucky
bluegrass, perennial ryegrass, and zoysiagrass. This
species closely resembles the hairy and the buffa-
lograss chinch bugs both in appearance and
damage.
Buffalograss Chinch Bug, Blissus
occiduus
The buffalograss chinch bug was first identified in
Nebraska feeding and causing damage on buffa-
lograss. Upon its discovery, it was understood that
the buffalograss chinch bug was limited to buffa-
lograss as a host. However, it has recently been
reported damaging zoysiagrass, and may have the
potential also to feed on and damage several other
turfgrasses and small grain crops. This species
closely resembles other chinch bugs species in
appearance and damage.
Southern Chinch Bug, Blissus
insularis Barber
The southern chinch bug is a major pest through-
out the range of its primary host, St. Augustinegrass.
3962
T Turfgrass Insects of the United States: Biology and Management
Distribution is generally from the Carolinas down
through all of Florida and west to Texas. They also
can be found in California, Mexico and throughout
the Caribbean. Like other chinch bugs, they damage
the turfgrass by sucking out plant juices.
Southern chinch bugs are similar to other
chinch bugs, but slightly smaller than the hairy
chinch bug. The adults are about 1 mm wide and
3–3.5  mm long and are black with shiny white
wings. Most characteristics are similar to other
chinch bugs including the presence of long- and
short-winged adults.
The southern chinch bug is one of the most
important insect pests of home lawns in the
deep South. Virtually all St. Augustinegrass will
be infested with southern chinch bugs, but not
necessarily at damaging population levels.
Southern chinch bugs will feed also on ber-
mudagrass, centipedegrass, bahiagrass, and zoy-
siagrass. As with the other species of chinch
bugs, their feeding on stems, crowns, and sto-
lons removes plant juices, but also injects a
toxin. This causes the grass to turn yellow and
often die. Populations often are aggregated and
damage appears in patches. Drought or heat-
stressed areas of lawns are areas that usually are
attacked first and most severely.
There are probably two to three generations
in the most northern areas of the southern
chinch bug range. Further south in northern
Florida and the Gulf Coast area, three to four
generations are common. In south Florida, seven
or more generations can occur. Overwintering
in the most northern areas is primarily as adults
while all stages are present in the more southern
areas.
Cutworms (Lepidoptera: Noctuidae)
Cutworms are plump, smooth, dull-colored cater-
pillars that hide in the turf profile in burrows or
aerification holes during the day, emerging at night
to feed on the foliage and leaf sheaths of turfgrass
plants.
Black Cutworm, Agrotis ipsilon
(Hufnagel)
The black cutworm is considered the most destruc-
tive cutworm that attacks turfgrasses. It is a major
pest of creeping bentgrass putting greens, tees, and
occasionally fairways throughout the United States
and worldwide. Black cutworm larval feeding
damage typically results in small, irregular sunken
patches or pockmarks that often are mistaken for
golf ball marks. Subsequently, black cutworm
damage reduces the smoothness and uniformity
of the putting green surface. Because aesthetics
and playability are high priorities for golf course
superintendents, multiple insecticide applications
are done each growing season to control this
important turfgrass insect pest.
Adult black cutworm are robust, hairy (scaly)
moths with a wingspan of approximately 35–45 mm.
The forewings are dull-brown to grayish-black,
and slightly lighter in color or pale toward the tip
of the wings. A distinctive, black, dagger-shaped
marking is located in the center of each fore-
wing, approximately 6  mm from the tip. The
hindwings are considerably lighter, uniformly
cream to dirty white, with darker veins. Black
cutworm adult moths typically hold their wings
flat over the back in a triangular position when
resting. Males can be differentiated easily from
females by their comb or feather-like antennae,
whereby female moth antennae are filiform or
slender and thread-like.
Black cutworm females lay eggs predomi-
nantly singly near the tip of grass blades. Eggs are
approximately 0.5 mm in diameter. They are cream
colored initially, later becoming darker as the
embryo develops. Larvae are hairless with the
exception of a few scattered bristles. The dorsal
side, above the spiracles, ranges in color from gray
to black, and the ventral side is typically lighter
gray. Spiracles are typically black and extend from
the prothorax to the terminal abdominal segment.
As a whole, the body of a black cutworm larva is
without distinct stripes or marking except for an
indistinct, pale stripe down the middle of the
 Turfgrass Insects of the United States: Biology and Management
­ orsal side. Under magnification, the cuticle (skin)
d given time because black cutworm populations
has a pebble-like surface, and is generally greasy in
appearance. Like many other caterpillars, there are
three pairs of true legs on the thorax and five pairs
of fleshy prolegs on the abdomen. Neonate larvae,
less than 24 h old, are approximately 3.5 mm long
whereas mature larvae range from 30 to 45  mm
long and are approximately 7 mm wide. Black cut-
worm larvae typically have six instars, however,
they sometimes have seven. Upon maturity, black
cutworm larvae pupate in the turf profile predom-
inantly in the soil, and occasionally in the thatch
associated with the turf. Pupae are reddish-brown
to dark brown in color and are about 19 mm long.
The black cutworm is distributed throughout
most of North America, as well as in Europe, Asia,
Africa and elsewhere. Depending on geographic
location, latitude and temperature, there can be
two to six generations per year. In the southern
U.S., in states such as Louisiana and Alabama,
there are five to six overlapping generations,
whereas in the northern U.S., in states such as
Minnesota and Wisconsin, there may be only one
or two generations per year. The black cutworm
has difficulty surviving subfreezing soil tempera-
tures, thus, it may be unable to overwinter in some
years north of the transition zone (a narrow range
between the cool-season temperate region and
warm-season zone, extending from southern Illi-
nois, Missouri and Ohio to Tennessee and North
Carolina). As a result, spring infestations in north-
ern areas begin with the arrival of migratory adults
from southern states. Black cutworm moths can
be carried several hundred miles in a few days by
strong southerly winds. In Wisconsin, the first
spring migrants typically arrive in late April to
early May; damage from their offspring begins
appearing in early to mid-June. Damage from the
second generation (brood) starts appearing late
July through early August. Occasionally a third
generation will appear in late summer or early fall
if temperatures are conducive, otherwise it is
understood that third generation adults will
migrate south as temperatures are less favorable.
Multiple larval sizes (instars) may be present at a
T 3963
tend to spread out their emergence and egg-laying
as the season progresses. In addition, the first gen-
eration appearance of black cutworm in states
located in the northernmost temperate U.S. may
have a later arrival of migrating adults than states
in the southernmost location of the temperate
U.S.  In the southernmost states (e.g., Alabama,
Louisiana, Mississippi and Georgia), first genera-
tion larvae may be present as early as February
and March and cutworm problems may persist
into November and December. In North Carolina,
adults have been captured in pheromone traps
every month of the year except January. Turfgrass
in Florida and Gulf Coast areas may experience
problems with cutworms all year. Areas with warm
season turfgrass that are closer to the transition
zone may experience cutworms as early as March
and April through late October.
Both black cutworm moths and larvae are
nocturnal. Adults do not cause any turf damage,
however, they do feed by sucking nectar from
flowers. Soon after emergence, adult females call
(attract) males by releasing a sex pheromone
(chemical sex attractant). Once fertilized, female
moths begin laying eggs. Individual females can
lay as many as 1,200–1,600 eggs over a 5- to 10-day
period. Eggs are predominantly attached to the
tips of grass blades singly. Eggs typically hatch in
3–6 days depending on temperature. Once hatched,
the young larvae (first and second instars) begin
feeding on leaf blades, both day and night. Young
larvae feed on both the top and bottom sides of
the of leaf blades in a skeletonizing manner. As
larvae develop and mature, older larvae (third to
sixth instars), they become nocturnal (feeding
only during the scotophase) as well as developing
a subterranean habit, forming silk-lined burrows
in the turf thatch or soil. On golf course turf, the
larvae will commonly occupy aerification holes,
spike marks, or golf ball injury sites. Black cut-
worm larvae hide in the aforementioned burrows
during the daylight, and venture out to feed at
night. The larvae typically pass through six molts,
maturing in 20–40 days. Young larvae do not cause
3964
T Turfgrass Insects of the United States: Biology and Management
measurable damage, however, large larvae are
highly destructive, consuming relatively large
amounts of turfgrass foliage in a single night. Once
black cutworm larvae reach maturity, pupation
occurs within the larval burrow or the turfgrass
profile. After approximately 14–21 days, the adult
moth emerges.
Most black cutworm larvae feeding occurs
from around midnight until just before dawn. On
golf course putting greens, wandering larvae can
move approximately 20  m or more in a single
night. This ability to move helps explain why golf
course putting greens and tees are sometimes
­reinfested soon after being treated with a short-
residual insecticide. It is likely that black cutworm
larvae are moving onto putting greens from the
surrounding area.
Bronzed Cutworm, Nephelodes
mimians Guenée
The bronzed cutworm is only an occasional pest of
home lawns and golf course turf, and unlike the
black cutworm, they rarely damage golf course
putting greens and tees. Bronzed cutworm is dis-
tributed across the northern half of the U.S. east of
the Rocky Mountains, as far south as Tennessee.
Adult bronzed cutworms are similar in size
to black cutworm, however, they lack the black
dagger-shaped mark on the wings. The forewings
are highly variable in color ranging from brown
to purplish-gray to maroon, and there is a wide,
darker-brown band across the middle of each
forewing. The hindwings are buff-colored similar
to the black cutworm. Bronzed cutworm eggs
resemble black cutworm eggs. Larvae are fat-
bodied, light to dark brown dorsally and lighter
ventrally, and they have a distinctive bronze
sheen. Larvae also have a light-yellow stripe that
extends longitudinally the entire length of the
body on the center of the dorsal side, with another
pale longitudinal stripe on each side of the body.
Spiracles are black and are located on each tho-
racic and abdominal segment. Fully developed,
mature ­larvae are 35–45 mm long. Bronzed cut-
worm and black cutworm pupae look similar in
color and size.
Although the bronzed cutworm has been well
studied in field crops, little is understood about its
biology in turf. Unlike most turf-infesting cut-
worm species, the bronzed cutworm has only one
generation per year. Adult moths emerge, mate,
and lay eggs in late summer or early fall. The eggs,
however, do not hatch until the following spring.
After eggs hatch in April, larvae begin feeding and
developing until fully developed in mid- to late
May, when most damage occurs. As bronzed cut-
worm larvae reach maturity, they burrow into the
soil and form pupal cells where they remain until
pupation in mid-August. Thereafter, new adult
moths emerge in approximately 30 days.
Variegated Cutworm, Peridroma
saucia (Hübner)
The variegated cutworm is an occasional pest in
lawns and golf course roughs, especially in rural
areas where turfgrass areas are bordered by field
crops where infestations may originate. It occurs
throughout both North and South America.
Variegated cutworm moths have yellowish
to brownish forewings that frequently have a row
of small black dashes on the leading edge of the
wing. Similar to the bronzed cutworm, they lack
the black dagger-shaped marking present on
black cutworm moths. Variegated cutworm moth
hindwings are whitish, with dark-shaded veins.
Variegated cutworm eggs are similar in size and
color to black cutworm eggs. However, variegated
cutworm eggs are laid in groups of several hun-
dred eggs in a single layer on foliage. Mature lar-
vae are approximately 35–46 mm long and vary
in color from pale gray to dark brownish-gray. A
row of pale yellow dots and dashes extend longi-
tudinally on the dorsal side of the body, and a
distinct brownish W-shaped marking is apparent
on the eighth abdominal segment, as well as a
yellowish or orange area near the terminal
 Turfgrass Insects of the United States: Biology and Management
abdominal segment. The larvae also have a rather
indistinct, black, yellowish or orange marking
that extends longitudinally on both sides. Pupae
are similar to both bronzed and black cutworm.
The variegated cutworm has from three to six
generations per year depending on geographic
location. Adult moths emerge from overwintered
pupae in March and April. Larvae from eggs
deposited by the first generation moths are typi-
cally fully developed by late May. The subsequent
generations occur from June to November, with
the last generation producing overwintering
pupae. A complete generation, egg to adult, typi-
cally requires 8–9 weeks. Compared to other cut-
worm species, the variegated cutworm is less
subterranean and nocturnal, thus is sometimes
feeds fully exposed during daylight, especially on
cloudy days.
Sod Webworms
There are more than 20 species of sod webworms
that feed on turfgrasses in North America, how-
ever, only about three or four species are pests in
specific geographical regions. Among the more
common sod webworm species that attack turf-
grasses in the northern U.S. are the bluegrass web-
worm, Parapediasia teterrella (Zincken); the larger
sod webworm, Pediasia trisecta (Walker); and the
western lawn moth, Tehama bonifatella (Hulst).
All of the aforementioned sod webworms species
at one time were grouped together in the genus
Crambus. Because their biology is similar, they can
be discussed together. The tropical sod webworm,
Hertopetogramma phaeopteralis (Guenée), has a
wide distribution only in the southeastern U.S.
and will be discussed separately.
In general, sod webworms are relatively small
larvae that live in silk-lined tunnels in the turf
canopy, specifically in the thatch and soil, hence
the name “webworms.”
Adult sod webworms are small, buff-colored
moths that have wingspans that range in size
from 19 to 25 mm. The forewings are primarily
T 3965
whitish, dull gray to tan, with longitudinal stripes
as well as other indistinct markings of brown,
black, gold, silver, and even yellow. Such mark-
ings are used to identify individual species.
Hindwings are typically lighter, whitish to light-
gray, with delicate fringes on the outer margins
of the wing. When resting, the wings are usually
folded over the body. Possibly the most distin-
guishing characteristic of sod webworm moths
is the presence of two small, snout-like projec-
tions that extend forward from the front of the
head. These snout-like projections are merely
mouthparts, but are the reason why sod web-
worm moths are frequently referred to as “snout
moths.” Moreover, the combination of folded
wings and the snout enable sod webworm adults
to be distinguished from other turfgrass moths.
Sod webworm eggs are extremely tiny, oval to
barrel-shaped, with fine, longitudinal ribbing on
the surface. Ribbing is distinctive for each spe-
cies. Sod webworm larvae range in color from
beige to gray to brown to greenish, depending
on species. Nearly all sod webworm species have
characteristic dark, circular spots and coarse
hairs scattered randomly over the body. Fully
developed larvae are typically 16–25  mm long.
Pupae are “torpedo-shaped,” approximately
10–13  mm long, and vary in color from tan to
dark brown.
Several species of sod webworms are distrib-
uted throughout the temperate U.S., however,
damage appears to be greatest in the Midwest and
the eastern U.S. Sod webworms attack and dam-
age several turfgrass species including creeping
bentgrass, Kentucky bluegrass, perennial ryegrass,
as well as fine-leaf and tall fescues, however, they
will also feed and cause damage on other grasses
that are considered weeds. Certain turfgrasses,
such as perennial ryegrass and fescues that con-
tain endophytes, are relatively resistant to sod
webworms. Sod webworm larvae hide in silk-
lined burrows in the turf canopy, emerging at
night to feed on turfgrass foliage. Feeding damage
results in leaves and stems being chewed off just
above the crown; thereafter, the plant material is
3966
T Turfgrass Insects of the United States: Biology and Management
pulled into the burrow where it is consumed. Ini-
tial signs of sod webworm feeding damage typi-
cally appears as general thinning of the turf,
followed by small irregular patches of brown,
closely cropped grass. Close inspection of the
damaged area reveals silk-lined tunnels and
clumps of green insect frass (fecal pellets) near or
around the burrow. When infestations are high
and damage escalates, the small irregular patches
begin coalescing into large irregular patches of
brown, closely cropped grass. Early symptoms of
sod webworm damage are typically masked, espe-
cially when the turf is dormant from drought
stress, and as a result the damage rapidly becomes
apparent after the turf recovers from the environ-
mental stress and the sod webworm damaged area
fails to recover. Moreover, sod webworm damage
frequently is mistaken for several fungal diseases,
golf ball damage, golf shoe (spikes) damage, as
well as black cutworm damage.
Sod webworms in the northern U.S. over-
winter as partially grown larvae in silk-lined
chambers in the turf canopy. In the early spring
when soil temperatures become conducive, sod
webworm larvae resume feeding and growing,
eventually pupating. Thereafter, adults typically
emerge in 10–20 days, depending on species and
temperature. Immediately after adult emergence,
mating occurs, and females typically begin laying
eggs by the following night. The adults are noc-
turnal, active at dusk or after dark. Adult females
are rather unique in their oviposition behavior.
They fly rather close to the turf surface (30–60 cm
above), erratically for short distances, fluttering
or hovering over the turf dropping approximately
60 eggs like bombs from a military aircraft. Each
female lives for about 2 weeks or less, laying sev-
eral hundred eggs during her lifetime. The
dropped eggs do not contain any sticky substrate
for adhesion, therefore, they tend to settle into
the turf canopy where they are rarely seen. Eggs
typically hatch in about seven days, and there are
usually six to eight instars. Newly hatched and
early instar larvae feed by scraping surface tis-
sues from leaf blades. Soon thereafter, larvae
drop  to the ground to form the silk-lined bur-
rows or tunnels. As larvae develop and mature,
they feed predominately at night. A complete life
cycle, egg to adult, requires 6–10  weeks, and
depending on geographic location, most temper-
ate region sod webworm species have two to
three generations per year.
Adult tropical sod webworms do not roll their
wings around their bodies when they are at rest.
Instead they hold them in more of a delta-winged
fighter plane configuration. The dingy brown
moths have a wingspread of about 20 mm. The lar-
vae is a dingy cream color, but will take on a green
appearance when the larvae are feeding. They
develop through seven or eight instars, reaching a
maximum length of 19 mm. The head is yellowish
brown. The larvae feed only at night and require
about 25–45 days to complete development. Trop-
ical sod webworms attack and damage all species
of warm season turfgrass. Highly maintained ber-
mudagrass is attacked most often and damaged
most severely. The larvae give the turf a ragged,
notch appearance from their feeding and eventu-
ally the turf will take on a close-cropped appear-
ance and turn yellow. Damage is often first noticed
near flower beds and shrubs. Damage is common
in southern Florida in the spring and throughout
the rest of its range in the Southeast by late sum-
mer. Generations may continue well into the fall
and damage often is mistaken for fall armyworm
feeding.
Crown and Thatch Inhabitants:
Burrowing Insects
The larval stage of numerous types of billbugs and
weevils damage turfgrasses by burrowing into the
stems (leaf sheath) or by damaging the crowns
(apical meristems). The apical meristem is the
most vulnerable part of the plant because it is
the  source that contains the growing points
whereby roots, shoots, and leaves originate. Subse-
quently, when burrowing insects attack turfgrasses,
plant death often results.
 Turfgrass Insects of the United States: Biology and Management
Annual Bluegrass Weevil, Listronotus
maculicollis (Dietz)
The annual bluegrass weevil, formerly called the
hyperodes weevil, is a serious pest of closely cut
annual bluegrass (Poa annua) on golf courses,
bowling greens, and tennis courts in the north-
eastern U.S. Although both the adults and larvae
cause damage to turfgrasses, adult damage is
minor compared to larval damage.
Annual bluegrass weevil adults are small,
3.5–4.0 mm long, generally black or dark charcoal-
gray beetles. The body is covered with fine,
yellowish hairs and scales that typically wear off
as the beetle ages. Thus, older adults often appear
shiny black. Newly emerged adults are light
reddish-brown, and often do not darken for several
days. The thorax is approximately one-third as
long as the abdomen, and the head is prolonged
into a blunt (broad and short) snout. As a result,
the annual bluegrass weevil is regularly confused
with other turf-infesting billbugs that are similar
in morphological characteristics. However, annual
bluegrass weevil can be accurately differentiated
by its shorter and broader snout; billbugs have a
longer, narrower snout. Annual bluegrass weevil
antennae are attached at the tip of the snout and
can be folded back along the side of the snout in
a compact groove. Annual bluegrass weevil eggs
are rice-shaped, approximately 1  mm long,
rounded at both ends, yellow initially but even-
tually becoming smoky gray to black before
hatching. Eggs are laid between leaf sheaths of
annual bluegrass. Females typically lay two to
three eggs end to end within the leaf sheath.
­Larvae are creamy white, legless, with a distinct
sclerotized brown head capsule. Larvae are
approximately 1 mm long when newly hatched,
and about 5  mm long when fully grown. There
are five instars, and all are similar in appearance,
differing only in size. Pupae are approximately
3.5  mm long, whitish at first, but later become
reddish brown before the adults emerge. The
snout, legs and wing pads are visible on the pupa,
but are folded close to the body.
T 3967
The only host that annual bluegrass weevil
attacks is closely cut annual bluegrass. Although
damage is only minor, the adults chew notches or
holes in grass blades. The larva is the primary
damaging life stage. Young larvae feed and tunnel
within the plant stems. As larvae develop and
become too large to feed within plant stems, they
burrow out and feed externally on the crown of
the plant. One larva can kill several plants during
its lifetime. Damage typically begins along the
edges of golf course fairways, especially those bor-
dering wooded areas or other overwintering sites,
as well as around the edges of putting greens and
tees. Damage first appears as yellowish-brown,
wilting or scattered dead patches of turf that even-
tually coalesce into larger dead areas as larvae
develop and mature. The tunneled stems easily
break off near the crown of the plant. Large infes-
tations have the potential to cause severe damage
to golf course putting greens, tees and fairways,
especially where annual bluegrass is prevalent.
The annual bluegrass weevil has one to two
generations per year depending on geographical
locations; in more northern areas of its range it
has only one generation per year. Adults overwin-
ter in refuges such as leaf litter under trees, tufts
of tall fescue, or other sheltered sites including
golf course roughs where the turf is typically
higher. Adults become active in the spring (mid-
April), when they begin to crawl or fly to closely
cut annual bluegrass hosts to begin feeding. Adult
annual bluegrass weevil typically hide in the foli-
age during daylight, and later climb up turfgrass
plants to feed at night. In early May, adults begin
laying eggs. The eggs typically hatch in 4–5 days,
depending on temperature. Immediately thereaf-
ter, the newly hatched larvae begin burrowing
within the grass stems until they reach the third
instar. Older larvae, third to fifth instars, burrow
out of the plant to feed along the exterior, primar-
ily on the plant crown. Upon maturation, annual
bluegrass weevil larvae pupate sometime in mid-
to late June in earthen cells just under the soil
surface. The second generation adults emerge in
late June or early July to feed, mate, and lay eggs.
3968
T Turfgrass Insects of the United States: Biology and Management
In areas where there are two generations per year,
most populations pupate by late August and adults
emerge sometime in September, and migrate back
to overwintering sites.
Billbugs (Coleoptera: Curculionidae)
Billbugs are one of the most misdiagnosed pests
of turfgrass. Turfgrass managers often confuse
billbug damage with symptoms of drought stress,
disease or other insect damage such as chinch
bugs and white grubs. There are four species of
billbugs that are considered major insect pests
within their range in the U.S. These species
include the bluegrass billbug, Denver billbug,
Phoenician billbug, and the hunting billbug. Bill-
bug damage is similar to that of weevil damage.
Both the adults and larvae feed and cause damage
to turf, however, adult damage is minor compared
to larval damage.
Bluegrass Billbug, Sphenophorus
parvulus Gyllenhal
The bluegrass billbug is among the most serious
pests of Kentucky bluegrass and perennial ryegrass
in the temperate U.S. It is distributed throughout
most of the U.S. and southern Canada where cool-
season turfgrasses are grown. Damage frequently
results in areas of brown, dead turf.
Adult bluegrass billbugs are characteristic
billbugs that have a long, slender, beak-like snout.
They are approximately 7–8 mm long, excluding
the length of the snout. Adults are hard-bodied,
sclerotized, usually slate gray to black in color,
and may sometimes appear brownish from dried
soil adhering to their body. Newly emerged adults
are initially reddish-brown, but eventually become
dark after a few days. Bluegrass billbug eggs are
elongate, bean-shaped, translucent white eggs
approximately 1.6  mm long. Larvae are plump,
legless, creamy white grubs with a sclerotized
brown head capsule. All larval instars are similar
except for size; early instars (first and second)
range in size from 1.3 to 2.4 mm long and mature
larvae (fifth instar) are approximately 6–10  mm
long. Pupae are approximately 8.5  mm long,
creamy colored, gradually changing to reddish
brown prior to adult emergence. The pupa has
several morphological characteristics of the adult,
the snout and legs are tucked under the thorax,
and the wings are folded along the side of the
abdomen.
Kentucky bluegrass is the preferred host of
the bluegrass billbug, but it also will feed on and
cause damage to perennial ryegrass as well as
occasionally fine-leaf and tall fescues, especially
when they are near heavily infested Kentucky
bluegrass sites. Damage is usually worst from
late June to early August, especially when turf is
undergoing heat and drought stress. Although
damage is only minor, the adults chew notches
or holes in grass blades. The larva is the primary
damaging life stage. Young larvae feed and tun-
nel within the plant stems. As larvae develop and
become too large to feed within plant stems, they
burrow out and feed externally on the crown of
the plant. One larva can kill several plants during
its lifetime. Damage first appears as yellowish-
brown, wilting or scattered dead patches of turf
that eventually coalesce into larger dead areas as
larvae develop and mature. The tunneled stems
easily break off near the crown of the plant.
Lower populations of bluegrass billbugs typi-
cally produce scattered brown patches of turf,
whereas heavier infestations can completely
destroy areas of turf.
Adult bluegrass billbugs overwinter practi-
cally everywhere, in areas including thatch, soil
crevices, under bark mulch or leaf litter, as well as
other sheltered locations. However, it has been
reported that crevices between the sidewalks and
lawns is a preferred winter refuge. Adults become
active in late April to mid-May when soil tempera-
tures reach approximately 18°C. Once active, they
are frequently seen crawling over sidewalks, curbs
and driveways on warm spring days as they are
seeking out suitable turfgrass in which to feed
 Turfgrass Insects of the United States: Biology and Management
and lay eggs. After mating, adult female bluegrass
billbugs begin laying eggs into small crevices cre-
ated by adult feeding, chewed in grass stems just
above plant crowns. Eggs typically are laid singly,
and occasionally in groups of two or three. Each
female can lay up to 2–5 eggs per day, and as many
as 200 in her lifetime. Nearly all eggs are laid by
early July, however, some females may continue
laying eggs as late as August. Eggs usually hatch in
approximately 6  days, and young larvae begin
feeding within the grass stems, later burrowing
down to feed on the plant crown as they mature.
Infested turfgrass plants are hollowed out and
packed with a powdery frass. As the bluegrass bill-
bug larvae become too large (second or third
instar) to feed within the turfgrass stems, they bur-
row out and move to the soil to feed externally on
both the crowns and roots. An accurate indicator
of bluegrass billbug activity is the presence of fine,
whitish, sawdust-like frass near the feeding site.
Larvae are most abundant in the soil from early
June to early August, and they typically require
35–55 days to mature, depending on temperature.
Thereafter, they pupate in small earthen cells in
the soil. The adults emerge in approximately
8–10 days. Thus, adults are abundant in late sum-
mer and fall, briefly feeding before seeking out
overwintering sites as cooler temperatures prevail.
Occasionally, some early emerging adults may
begin to lay eggs for a second generation, however,
resulting larvae do not develop fast enough to
mature before the onset of winter.
Denver Billbug, Sphenophorus
cicatristriatus Fahraeus
Compared to other billbug species, little is known
about the biology and life history of the Denver
billbug. However, damage from this insect pest
has been reported in Colorado, Kansas, and
­central and western Nebraska. It is considered
the most serious pests of Kentucky bluegrass in
­Colorado. Damage frequently results in areas of
brown, dead turf.
T 3969
Adult Denver billbugs are considerably
larger than either the bluegrass or hunting bill-
bug, reaching 8–12.5  mm long. The Denver
­billbug adult is differentiated from the other
two species by its larger size and the presence of
distinctive, double-lobed markings on the wing
covers. The Denver billbug may overwinter as
an adult, but is more likely to spend the winter
as a mid-to-late stage larva. After a spring feed-
ing period by the larvae, eggs are laid by adults,
and subsequent larvae develop over the sum-
mer. Larvae are plump, legless, creamy white
grubs with a sclerotized brown head capsule. All
larval instars are similar except for size, early
instars (first and second) range in size from 1.3
to 2.4 mm long and mature larvae (fifth instar)
are approximately 6–10  mm long. Pupae are
approximately 9.0  mm long, creamy colored,
gradually changing to reddish brown prior to
adult emergence. The pupa has several morpho-
logical characteristics of the adult, the snout
and legs are tucked under the thorax, and
the  wings are folded along the side of the
abdomen.
Kentucky bluegrass is the preferred host of
the Denver billbug, but it will also feed on and
cause damage to perennial ryegrass. Damage
typically occurs in the fall and early spring. Dam-
age symptoms of the Denver billbug are compa-
rable to that of the bluegrass and hunting billbug.
The larva is the primary damaging life stage.
Young larvae feed and tunnel within the plant
stems. As larvae develop and become too large to
feed within plant stems, they burrow out and
feed externally on the crown of the plant. One
larva can kill several plants during its lifetime.
Damage first appears as yellowish-brown, wilt-
ing or scattered dead patches of turf that eventu-
ally coalesce into larger dead areas as larvae
develop and mature. The tunneled stems easily
break off near the crown of the plant. Lower
populations of bluegrass billbugs typically pro-
duce scattered brown patches of turf, whereas
heavier infestations can completely destroy areas
of turf.
3970
T Turfgrass Insects of the United States: Biology and Management
Phoenician Billbug, Sphenophorus
phoeniciensis Chittenden
The Phoenician (or Phoenix) billbug occurs pri-
marily in southern California and Arizona. The
adults and larvae have a typical billbug appear-
ance. The adult Phoenician billbug has an
M-shaped raised area on the pronotum. It is pri-
marily a pest of bermudagrass and zoysiagrass,
particularly in those areas that are stressed or
poorly maintained.
The injury from Phoenician billbug feeding is
greatest during the summer months, at times of
maximum temperatures and drought stress. The
larval stage is the principal stage that causes dam-
age. The small larvae usually feed inside the plant
stems. The larvae continue to feed and once they
become larger, they feed outside the stem around
the crown and stolons of the plant. Larvae can kill
a plant (or several plants) but usually the ber-
mudagrass is growing quite rapidly during the
summer and damage goes unnoticed until fall.
Damage usually appears as stressed turf that turns
yellowish-brown and wilts, which is easily mis-
taken for drought stress. Scattered dead patches
may occur later in the season or be observed the
following spring as the bermudagrass fails to grow.
The damaged stems break off easily at the crown
of the plant. Populations often are highest and
damage most severe in sunny, drought-prone
locations.
Hunting Billbug, Sphenophorus
venatus vestitus Chittenden
The hunting billbug closely resembles the bluegrass
billbug but is slightly larger and has parenthesis-
like markings on the back of the thorax. This bill-
bug species prefers warm season turfgrass species
including but not limited to bermudagrass and
zoysiagrass. On occasion, hunting billbug will
damage Kentucky bluegrass. The hunting billbug
is primarily a pest of the southeastern U.S., how-
ever, it is also found in the mid-Atlantic states as
well as further west and north into Missouri,
­Kansas and southeast Nebraska.
Adult hunting billbugs are characteristic
­billbugs that have a long, slender, beak-like snout.
They are approximately 6–11 mm long, excluding
the length of the snout. Adults are hard-bodied,
sclerotized, usually slate gray to black in color, and
may sometimes appear brownish from dried soil
adhering to their body. Hunting billbug eggs are
elongate, bean-shaped, translucent white eggs
approximately 1.6  mm long. Larvae are plump,
legless, creamy white grubs with a sclerotized
brown head capsule. All instars are similar except
for size; early instars (first and second) range in
size from 1.3 to 2.4  mm long and mature larvae
(fifth instar) are approximately 7–10  mm long.
Pupae are approximately 8.5  mm long, creamy
colored, gradually changing to reddish brown
prior to adult emergence. The pupa has several
morphological characteristics of the adult; the
snout and legs are tucked under the thorax, and
the wings are folded along the side of the
abdomen.
Damage is usually greatest from mid-June
through early August during the period of maxi-
mum heat and drought stress. The larva is the
principal damaging life stage. Young larvae feed
and tunnel within the plant stems. As larvae
develop and become too large to feed within plant
stems, they burrow out and feed externally on
the crown of the plant. One larva can kill several
plants during its lifetime. Damage first appears as
yellowish-brown, wilting or scattered dead patches
of turf that eventually coalesce into larger dead areas
as larvae develop and mature. The tunneled stems
easily break off near the crown of the plant. Lower
populations of hunting billbugs typically produce
scattered brown patches of turf, whereas heavier
infestations can completely destroy areas of turf.
As is the case with the Denver billbug, little is
known about the biology of this pest. The hunting
billbug has been reported to overwinter as dor-
mant adults in the soil. Adults become active in
late April to mid-May when soil temperatures
reach approximately 18°C. Once active, they are
 Turfgrass Insects of the United States: Biology and Management
seen frequently crawling over sidewalks, curbs,
and driveways on warm spring day as they are
seeking out suitable turfgrass in which to feed and
lay eggs. After mating, adult female bluegrass bill-
bugs begin laying eggs into small crevices created
by adult feeding, chewed in grass stems just above
plant crowns. Eggs typically are laid singly, and
occasionally in groups of two or three. Each female
can lay up to 2–5 eggs per day, and as many as 200
in her lifetime. Nearly all eggs are laid by early July,
however, some females may continue laying eggs
as late as August. Eggs usually hatch in approxi-
mately 3–10 days, and young larvae begin feeding
within the grass stems, later burrowing down to
feed on the plant crown as they mature. Infested
turfgrass plants are hollowed out and packed with
a powdery frass. As the bluegrass billbug larvae
become too large (second or third instar) to feed
within the turfgrass stems, they burrow out and
move to the soil to feed externally on both the
crowns and roots. An accurate indicator of blue-
grass billbug activity is the presence of fine, whit-
ish, sawdust-like frass near the feeding site. Larvae
are most abundant in the soil from early June to
early August, and they typically require 35–55 days
to mature, depending on temperature. Thereafter,
they pupate in small earthen cells in the soil. The
adults emerge in approximately 8–10  days, thus
adults are abundant in late summer and fall, briefly
feeding before seeking out overwintering sites as
cooler temperatures prevail.
Soil Inhabitants: Root-Infesting Insects
White Grubs (Coleoptera: Scarabaeidae)
White grubs are the most widespread, and consid-
ered the most destructive, insect pests of turf-
grasses in the continental U.S. Most species of
white grubs damage turfgrass by chewing off the
roots near the soil surface. Most often, white grub
damage occurs during periods of hot and dry
weather. Subsequently, turf loss can be relatively
abrupt and severe. To compound this problem,
vertebrate predators such as armadillos, badgers,
T 3971
birds, moles, raccoons, skunks and various other
animals may dig up infested areas of turf in search
of grubs. In many cases these animals cause more
damage than the grubs themselves.
Because white grubs feed on the roots below
ground, they often go undetected until measur-
able loss to the root system has occurred. More-
over, grubs can be relatively difficult to control
because soil insecticides must penetrate the turf
canopy and thatch layer in order to effectively
make contact with the grubs located in the soil. To
achieve maximum control, turfgrass managers,
through appropriate application equipment, adju-
vants or surfactants, gravity, and irrigation or
natural rainfall, must effectively place respective
insecticides into the target zone where the grubs
are located.
The larval stage (grub) typically is the damag-
ing life stage to turfgrass, however, some species of
beetles cause damage to ornamental plant materi-
als as adults. White grubs are stout-bodied beetle
larvae. About 15 species are pests of turfgrasses in
North America, with about 10 species considered
to be important: Aphodius grubs, Asiatic garden
beetle, black turfgrass ataenius, European chafer,
green June beetle, Japanese beetle, May beetles,
northern and southern masked chafers, and Ori-
ental beetle. These species of white grubs are gen-
erally similar in appearance, habits, and the damage
they cause. An overview of the biology of individ-
ual species follows.
Aphodius Grubs, Aphodius granaries
(L.) and Aphodius paradalis Le Conte
Two species that belong to the genus Aphodius are
occasional pests of turfgrass, especially golf course
fairways. Aphodius grubs are relatively small grubs
compared to most other white grubs. They closely
resemble black turfgrass ataenius grubs, and
because they are frequently found in association
with black turfgrass ataenius, often they are con-
fused or misidentified. Although they seem to be
less frequently associated with turf than black
3972
T Turfgrass Insects of the United States: Biology and Management
turfgrass ataenius, they are capable of causing seri-
ous damage to turf.
Adults are typically black with a reddish tinge,
reddish-brown legs, and pale antennae. The adults
have two triangular projections on the outer edge
of the tibia and hind leg, whereas black turfgrass
ataenius lack these projections. Aphodius eggs are
tiny (less than 0.7 mm when fully hydrated), and
pearly white. Larvae are typically white grubs,
however, they are considerably smaller than most
other common turf-infesting species. Newly
hatched first instars are approximately 2.4  mm
long, and are difficult to see. Second instar larvae
are about 5 mm long and third instars are approxi-
mately 7.0  mm long. Fully mature third instars
often are mistaken for young grubs of other spe-
cies such as European chafers, Japanese beetles,
and masked chafers. A distinguishing morpholog-
ical characteristic that differentiates the two spe-
cies of Aphodius larvae, as well as black turfgrass
ataenius and other white grubs, is the raster pat-
tern. The raster pattern is a distinctive pattern of
hairs, spines, and bare spaces on the raster located
on the ventral side of the last abdominal segment,
anterior of the anus. The raster of Aphodius grubs
has two rows of short spines forming a distinctive
V-shaped pattern, whereas black turfgrass atae-
nius grubs have a random arrangement of spines
as well as two distinctive, pad-like structures at the
tip of the abdomen, anterior of the anal slit.
Both the adults and larvae of Aphodius feed
primarily on decaying organic matter, especially
animal manure. However, occasionally they will
feed on living roots of cool-season turfgrasses
such as annual bluegrass, creeping bentgrass, and
Kentucky bluegrass. Aphodius grubs cause spo-
radic, severe damage predominantly to golf courses
in the temperate U.S. Damage to home lawns is
uncommon. The initial symptoms of Aphodius
larval damage are patches of thin or wilted turf-
grass that resemble drought stress, however, the
turf does not respond or recover with the applica-
tion of irrigation. As turfgrass root loss continues,
the turf typically dies in irregular patches that
eventually coalesce into larger dead areas. Heavily
infested areas of turf can be rolled up similar to a
loose piece of carpet. Upon close inspection or
sampling, the grubs, pupae, and adults can be
found under the dead patches of turf in the soil.
Irrigated turfgrass with a high proportion of
annual bluegrass are especially susceptible. Popu-
lations of as many as 200–300 m−2 are not uncom-
mon. In addition, vertebrate predators frequently
forage for grubs, resulting in additional turf
damage.
The life history of Aphodius is poorly under-
stood. Observations from Ohio, Michigan and
Ontario, Canada suggest that there is only one
generation per year with adults becoming active
during the first warm days of spring; egg-laying
apparently begins 2–3  weeks earlier than that of
black turfgrass ataenius. However, other published
reports indicate the possibility that two annual
generations may be possible, especially in the more
southern parts of the species range. Nonetheless,
because Aphodius species are frequently associ-
ated with black turfgrass ataenius, similar biologi-
cal attributes may be extrapolated to effectively
manage Aphodius.
Asiatic Garden Beetle, Maladera
castanea (Arrow)
The Asiatic garden beetle is a relatively minor pest
of turfgrass, however, it can be locally abundant
and damaging, especially in the temperate north-
eastern U.S.
Asiatic garden beetle adults are dull chestnut-
brown, with a velvety appearance and a slight iri-
descent sheen. The beetles range in size from 8 to
11 mm long and 5–6.4 mm wide. The elytra (wing
covers) do not quite reach the tip of the abdomen,
leaving the terminal two segments of the abdomen
exposed. The ventral side of the Asiatic garden
beetle adult is partially covered with yellow hairs,
and each visible segment of the abdomen has a
row of backward-pointing yellow hairs that extend
across the width of the body. The dorsal side of the
elytra is bald with the exception of a row of fine
 Turfgrass Insects of the United States: Biology and Management
hairs on the outer margins. Another distinctive
morphological characteristic is the presence of
scattered, small hairs on the dorsal (top) side of
the head. Asiatic garden beetle eggs are pearly
white, oval and are approximately 1 mm in diam-
eter. After becoming hydrated from soil moisture,
they become almost spherical. The eggs are typi-
cally laid in clusters of 3–19 eggs that are loosely
held together by a gelatinous secretion. Newly
hatched first instars are approximately 1.4  mm
long and reach 19  mm long when fully mature.
They are like most other white grubs, having a
C-shaped body, a brown head capsule, and six
jointed legs. However, the body color of Asiatic
garden beetle larvae typically remains somewhat
lighter than in other white grub species. The
important distinguishing feature is the single,
transverse curved row of spines on the raster,
together with a Y-shaped anal opening. The hind
legs have tufts of hairs, and extremely small claws
relative to those on the pro- and meso-legs (front
and middle legs, respectively). The presence of a
whitish, enlarged, bulbous morphological struc-
ture (the stipes) on each maxilla beside the jaws is
another distinctive feature of Asiatic garden beetle
grubs. The pupa is approximately 7–10 mm long,
and appears white initially but turns tan as it
matures. Initially the pupa is enclosed in the final
instar skin, which soon splits and is pushed back
over the terminal portion of the abdomen; thus,
it  lies exposed in an earthen cell created by the
larva. This characteristic is common also in the
European chafer and May beetles.
Asiatic garden beetle grubs feed on the roots
of all cool-season turfgrasses as well as weeds,
woody ornamentals, herbaceous perennials, and
vegetables. Adult Asiatic garden beetles prefer box
elder, butterfly bush, cherry, Devil’s walkingstick,
Japanese barberry, oriental cherry, peach, rose,
strawberry, sumac, and viburnum. Asiatic garden
beetle larvae feed on the roots of various turfgrass
species, causing typical white grub injury resulting
in thinning, wilting, irregular dead patches of turf.
Well or highly maintained turf that is irrigated regu-
larly and is located near weedy areas containing
T 3973
adult Asiatic garden beetles’ preferred food sources
is more likely to be infested. Compared to other
white grub species such as Japanese beetles, an
equal number of Asiatic garden beetle grubs is
typically less destructive. It is likely that this is a
result of the fact that Asiatic garden beetle grubs
typically feed deeper in the soil profile, thus leav-
ing more of the turfgrass root system intact. Where
Asiatic garden beetle infestations are heavy, it is
not uncommon to observe more than 100 grubs/
m2, resulting in severe damage. Not only do Asiatic
garden beetle grubs cause damage, but the adults
feed on more than 100 species of woody and her-
baceous ornamental plant material. When beetles
are abundant, preferred plants can be stripped of
foliage and flowers.
Asiatic garden beetle has a univoltine (one
life cycle per year) life cycle similar to the Japanese
beetle. Adults are most abundant from mid-July
to mid-August. Adult females burrow into the
turf canopy to lay eggs in the soil at about
2.5–5 cm in depth. Each female is capable of lay-
ing up to 60 eggs in her approximately 30-day
lifetime. Once laid, eggs typically hatch in about
10 days; immediately thereafter the young larvae
commence feeding on the tender, succulent roots
of turfgrass and decaying organic matter until
sometime in the fall when the first measurable
frost occurs. The majority of Asiatic garden bee-
tle grubs will have attained the final instar (third)
by the first frost, however, approximately 25%
will overwinter as second instars. As the soil
­temperatures continue to decline, the grubs will
continue to burrow deeper into the soil profile,
ultimately overwintering approximately 20–43 cm
below the turf surface in a semi-dormant, non-
feeding state. Sometime in mid- to late April, the
grubs will move slowly back up to the root zone
where they will begin feeding until mid-June.
Thereafter, mature grubs will begin preparing
earthen cells or cavities 4–10 cm below the turf
surface where they will pupate. Pupation occurs
mainly from mid-June through mid-July, and
typically lasts for approximately 10  days. New
adults remain in the pupal cell for a few days
3974
T Turfgrass Insects of the United States: Biology and Management
until they become fully sclerotized (hardened)
and their color changes from whitish to chestnut-
brown. Soon after, the adults burrow upward and
emerge from the soil to feed, mate, and lay eggs in
susceptible areas of turf.
Black Turfgrass Ataenius, Ataenius
spretulus Haldeman
Although sporadic in occurrence, the black turf-
grass ataenius causes severe damage to golf courses
in the temperate U.S., especially where cool-season
turfgrasses are grown. They are also occasional
pests where bentgrass greens are utilized in warm
season turfgrass areas of the U.S. Black turfgrass
ataenius has many of the same biological charac-
teristics as several other white grub species, how-
ever, its season life cycle differs in that there are
typically two generations per year throughout
much of its range. In the more southern areas of
the U.S., its life cycle is poorly understood, but
more than two generations may occur in some
areas.
Adult black turfgrass ataenius are relatively
small, shiny black beetles ranging in size from 3.6
to 5.5  mm long and approximately half as wide.
There are distinct longitudinal grooves on the
elytra. Newly emerged adults are reddish-brown
initially, and darken in a few days. Eggs are minute,
less than 0.7 mm in diameter after absorbing water
from the soil, and pearly white. Larvae are typical
white grubs in appearance, however, they are con-
siderably smaller than other turfgrass-infesting
species. Newly hatched larvae are quite small,
approximately 2.4  mm long, thus they are rela-
tively difficult to see. Second and third instars are
about 5 mm and 7.0 mm long, respectively. Fully
mature black turfgrass ataenius grubs are mistaken
frequently for young grubs (first instars) of several
other white grub species such as European chafer,
Japanese beetle, and both northern and southern
masked chafers. However, black turfgrass ataenius
larvae can be distinguished easily by the two dis-
tinctive, pad-like structures located at the terminal
end on the ventral side of the abdomen anterior to
the anal slit. Upon maturation, black turfgrass
ataenius grubs pupate into small, approximately
4.2–5.7  mm long, pupae that are initially cream
colored, but eventually become reddish-brown
before the adult beetle emerges. A distinctive char-
acteristic of black turfgrass ataenius pupae is that
the wings and legs are folded close to the body.
Black turfgrass ataenius larvae typically attack
and cause damage to the roots of annual bluegrass,
creeping bentgrass, and Kentucky bluegrass on
golf courses. They also feed on decaying organic
matter, and the adults feed on manure and decay-
ing organic matter. Because black turfgrass atae-
nius grubs feed on the roots of turfgrasses, the first
symptoms appear as patches of thin or wilted turf
that resembles drought stress, however, the turf
does not recover with the application of irrigation
or rainfall. As damage and subsequent root loss
increases, the turf typically dies in irregular patches
that eventually coalesce into larger dead areas.
Heavily infested areas can be pulled or rolled up
similar to loose carpet. Upon close inspection of
the turf, large numbers of larvae, pupae and adults
can be observed in the soil under the turf. Black
turfgrass ataenius seems to prefer, and are most
common in, areas of turf that are close-cut, with a
moist, compacted layer of thatch. Additionally,
golf course fairways that have a high proportion of
annual bluegrass composition are especially sus-
ceptible. Because black turfgrass ataenius grubs
are relatively small, they typically are found in
higher densities than most other white grub spe-
cies, with populations of 215–325 m−2 not uncom-
mon. Accenting the damage associated with black
turfgrass ataenius grubs, vertebrate predators fre-
quently forage for grubs, resulting in additional
turf damage.
Depending on geographic location, black
turfgrass ataenius has one to two generations
per year. There is typically only one generation per
year in the Great Lakes states, New York, northern
New England, Ontario, and other parts of its range.
Adults reportedly overwinter along the edges of
wooded areas along the perimeter of golf courses.
 Turfgrass Insects of the United States: Biology and Management
The adult beetles seek refuge in leaves, pine nee-
dles, grass clippings, and other debris in the upper
2.5–5 mm of the soil. Most of the overwintering
black turfgrass ataenius adults have mated. Subse-
quently, in the early spring, from late March to
early April, the adults become active and can be
observed in swarms flying over golf course putting
greens and fairways on warm afternoons as well as
around lights at night. Soon thereafter, black turf-
grass ataenius adults begin laying eggs in early
May continuing until mid-June. Black turfgrass
ataenius eggs are laid in clusters of approximately
11–12 eggs within cavities formed by the female
near the soil-thatch interface. Eggs typically hatch
within 7  days, and the larvae immediately begin
feeding on fine, succulent roots and organic mat-
ter. This first generation of grubs typically is pres-
ent from late May until early July, with damage
commonly appearing in late June. Larvae require
approximately 4 weeks to mature; thereafter, they
burrow down into the soil profile to pupate and
emerge as adults sometime in late June through
early July. Upon emergence, these beetles mate and
begin laying eggs in July through early August,
producing a second generation of grubs which
typically causes damage in August and early
­September. These grubs develop, mature, and
pupate by late August or early September, produc-
ing adults that mate and emigrate to overwinter-
ing sites in the late fall. Generations appear to
overlap and more than one life stage is common at
a given time since the adults lay eggs over a period
of several weeks. In geographic areas where there
is not enough time to complete development of a
second generation, these beetles mate but will not
lay eggs. In areas of southern California, there is
great variation from year to year in the occurrence
of black turfgrass ataenius. Damaging populations
of grubs do not occur until late in the summer in
most years, but occasionally early summer dam-
age may occur. Frequent insecticide applications
for cutworms as well as high temperatures in the
summer may reduce the likelihood of black turf-
grass ataenius infestation on putting greens in the
southern areas of the U.S.
T 3975
European Chafer, Rhizotrogus
majalis (Razoumowsky)
The European chafer is a native of Europe, where it
is a serious turfgrass pest. In the U.S. as well, it is a
turfgrass insect pest, primarily in the northeast.
Where European chafer occurs, often it is consid-
ered the most damaging grub species. European
chafer grubs are considerably larger than most
other white grub species, especially Japanese bee-
tle larvae. Thus, they commonly are more destruc-
tive than equal numbers of other species. In
addition, they typically feed later into the fall and
resume feeding earlier in the spring than other
grub species.
European chafer adults are medium-sized,
light-reddish beetles measuring approximately
13–15  mm long, with a slightly darker head and
pronotum. The posterior edge of the dorsal side of
the pronotum has a narrow band of light-yellow
hairs, and the ventral side of the thorax is covered
with pale yellow hairs. The terminal portion of the
abdomen protrudes beyond the elytra, and they
have distinct longitudinal grooves and minute
punctuations. Both European chafers and May
beetles resemble one another, however, European
chafers are slightly smaller and they lack a tooth
on the tarsal claws of the mesothoracic legs. Addi-
tionally, the European chafer has more distinct
grooves on the elytra. Newly laid eggs are oval,
shiny, milky white initially, but become dull gray
after a few days. As they absorb water from the
soil, the eggs become spherical, swelling to approx-
imately 2.3–2.7 mm in diameter prior to hatching.
European chafer larvae are typical C-shaped white
grubs, with a yellowish-brown head and six dis-
tinct, jointed legs. The larvae can be differentiated
easily from other white grub species by the raster
pattern. It has two distinct, nearly parallel rows of
small spines that diverge outward at the tip of the
abdomen, similar to a slightly open zipper. The
raster pattern, in combination with a Y-shaped
anal slit, readily distinguishes European chafer
­larvae from other turfgrass-infesting white grub
species in the temperate U.S. First instar European
3976
T Turfgrass Insects of the United States: Biology and Management
chafer grubs are initially translucent white, though
the terminal portion of the abdomen becomes
dark after feeding. Fully mature larvae are approx-
imately 23 mm long. Both the prepupa and pupa
resemble most other white grub species. They are
approximately 16 mm long, smaller than May bee-
tle pupae, yet larger than Japanese beetle pupae.
European chafer pupae shed the larval exoskele-
ton, whereas Japanese beetle and Oriental beetle
pupae lie within the shed larval skin.
European chafer larvae feed on the roots of all
cool-season turfgrasses, as well as numerous grassy
and broadleaf weed species in pastures and nurs-
eries. The grubs cause thinning, wilting, and sub-
sequent irregular patches of turf that can be readily
pulled back or rolled up from the soil like a roll of
carpet. Population densities of 18–28 grubs/m2 are
not uncommon in lawns and golf course turf.
Damage by European chafer grubs typically
appears in September, especially when the turf is
already stressed by both heat and drought. More-
over, damage also can be observed in the spring
when the grubs resume feeding on the previously
weakened turf. Although European chafer adults
occasionally will sample the margins of tree leaves,
they rarely cause any measurable damage.
The European chafer has a life cycle that
closely resembles those of other white grub spe-
cies such as Japanese beetle and May beetle. In
northern portions of Michigan and New York,
adult European chafers begin emerging in mid-
June and are most abundant from late June until
mid-July, and terminate by late July. In areas fur-
ther south, such as New Jersey, Ohio and Pennsyl-
vania, adult activity typically occurs about 2 weeks
earlier. Adults are most active on warm, clear
nights when the temperature is above 19°C, and
on favorable nights large numbers of adults begin
emerging from the turf canopy near sunset. The
adults fly to nearby trees, swarming about by the
thousands. After a courtship period of approxi-
mately one hour, mating pairs begin to make their
way to the turf canopy, ultimately returning into
the soil before sunrise. Female European chafer
adults continue to return to trees several times to
re-mate during their 1- to 2-week lifetime. Each
female lays 20–40 eggs in her life. Eggs are typi-
cally laid singly at 5–10  cm depth in the moist
soil.  Eggs hatch in approximately 2  weeks, and
most hatch by late July. There are three instars of
European chafer grubs; first instars are predomi-
nant until mid-August, second instars are present
in early September, and third instars continue to
feed and develop into November. Similar to other
white grubs species, European chafers move down
into the soil profile just below the frost line to
overwinter. In the spring, when soil temperatures
become conducive, the grubs return to the upper
2.5–5 cm near the soil-thatch interface to vigorously
feed until late May. In early June the European cha-
fer larvae begin moving down into the soil profile,
to a 5–25 cm depth, to form earthen cells to pupate.
The prepupal life stage requires approximately
2–4  days, while the pupal stages typically takes
about 2 weeks. Thereafter, adults begin emerging
in mid-June.
Green June Beetle, Cotinus nitida L
The green June beetle is a native of the eastern
U.S., and is widely distributed east of the Missis-
sippi river, north to St. Louis, Missouri, and south
to Texas. They are most common in the southern-
most edge of the temperate region where cool-
season turfgrasses are grown. Because of their
relatively large size, both the green June beetle
adults and grubs regularly attract attention where
they are abundant. Adult green June beetles are
rather prolific fliers that are mistaken often for
wasps as they swarm in a “buzzing” manner over
the turf in mid-summer. Green June beetle grubs
are relatively large compared to other turfgrass-
infesting white grub species.
Adult green June beetles are considerably
larger than Japanese beetles. They are approxi-
mately 19–25 mm long and 12.5 mm wide. They
vary in color on the dorsal side of the body and
elytra from dull brown with longitudinal stripes of
green, to uniform, velvety forest green. The outer
 Turfgrass Insects of the United States: Biology and Management
margins of the elytra range in color from tan to
orange-yellow. The ventral side of the body is shiny
metallic green or gold. Newly laid eggs are dull
white, approximately 1.5 mm in diameter. As the
eggs absorb water from the soil, they become
larger, 3  mm in diameter, and more spherical in
shape. First instar grubs are approximately 6–7 mm
long, second instars are 15–17 mm long, and fully
mature larvae are relatively large (45–48 mm long),
robust, and more parallel-sided compared to other
white grub species. Green June beetle grubs have
short, stubby legs and mouthparts in relation to
their overall body size. Upon maturation, the green
June beetle forms a cocoon-like cell composed of
soil particles held together by a sticky secretion,
within which pupation occurs. Green June beetle
pupae are large, approximately 25  mm long and
12.5 mm wide. The pupae are initially whitish, but
gradually darken over time and eventually exhibit
tints of the adult coloration before the adults
emerge. They can be identified readily by their dis-
tinct locomotion; essentially, they scurry along on
their backs, upside-down.
Green June beetle grubs primarily feed on
decomposing organic matter, including compost,
thatch, and grass clippings. There are indications
that poorly managed turfgrass with excessive
thatch may be at greater risk, and that the use of
organic fertilizers just prior to the adult flights
may make a turfgrass area more attractive for egg-
laying. Green June beetle grubs do not feed on the
roots like many other scarabs, however, they do
cause considerable damage by their burrowing
and tunneling behavior. The grubs make distinct,
open vertical burrows with a surface hole approxi-
mately the size of a human’s thumb. The burrow-
ing and tunneling action of green June beetle
larvae causes loose soil to be excavated out at the
mouth of the burrow at night, forming a small
mound approximately 50–75  mm across. The
aforementioned mounds are frequently mistaken
for ant mounds except that the soil particles are
considerably coarser. This action disrupts the roots
system, dislodging the turfgrass, and loosens the
surface topsoil, permitting the turf to desiccate. As
T 3977
a result, the turf typically wilts and thins, allowing
the invasion of broadleaf and grassy weeds. Adult
green June beetles occasionally damage tree leaves,
though they mostly feed on ripening fruits, tree
sap and other sugary food sources. Similar to the
grubs, the adults create little piles of soil as they
burrow into and out of the turf canopy for egg-
laying and resting.
Like many other scarabs, the green June beetle
has a 1-year life cycle. Adults typically emerge in
late June with peak activity occurring over a
2–3 week period, usually in mid-July in Kentucky;
this event may be 2–3 weeks earlier in the south
and 1–2 weeks later in areas further north. Green
June beetle adults are active during the daytime,
and rest on vegetation as well as under the thatch
during the night. After mating, green June beetle
female adults seek out turf areas with moist soils
containing high levels of organic matter. The
females burrow down into the turf approximately
5–13 cm, excavating a small cavity where she lays
a cluster of 10–30 eggs. The cluster of eggs is
enclosed in a small-sized sphere of soil held
together by a sticky secretion. Each green June
beetle female makes numerous egg chambers, lay-
ing as many as 60–75 eggs over a 2-week period
of time. Eggs hatch in approximately 2 weeks. Sub-
sequently, the young larvae begin feeding at the
soil/thatch interface by early August. After con-
tinuing to feed and grow for several weeks, green
June beetle larvae attain the third instar in late
October or early November in the northern
regions of their distribution. Third instars can be
seen as early as the end of August in some Mid-
Atlantic states, but also will remain active until
November. As the soil temperatures continue to
decline, the grubs will continue to burrow deeper
into the soil profile, ultimately overwintering
approximately 20–76  cm below the turf surface
in  a semi-dormant, non-feeding state. In some
of  the southern states, where soil temperatures
do not drop significantly, green June beetle grubs
can remain active throughout the winter on warm
nights. Sometime in mid- to late April, the grubs
will move slowly back up to the soil/thatch
3978
T Turfgrass Insects of the United States: Biology and Management
i­ nterface to feed until late May. Thereafter, mature
grubs will begin preparing earthen cells or cavi-
ties, 20–40 cm below the turf surface, where they
will pupate. Pupation occurs mainly in early June,
and typically lasts for approximately 10–20  days.
After about 3  weeks, adult green June beetles
­burrow upward and emerge from the soil to feed,
mate, and lay eggs in susceptible areas of turf.
Japanese Beetle, Popillia japonica
Newman
The Japanese beetle is a native to the main islands
of Japan, where it is not considered a pest. How-
ever, in the eastern U.S. it is considered by many to
be the worst insect pest of turfgrasses and orna-
mental landscapes. As a result, countless dollars
and resources are aimed at controlling Japanese
beetle adults and larvae. Japanese beetle larvae are
white grubs that cause typical root-feeding dam-
age. As for the adults, unlike most scarab adults,
Japanese beetles attack and cause serious damage
to over 300 ornamental plant species.
Japanese beetle adults are attractive, broadly
oval insects that are approximately 8–11 mm long
and 5–7 mm wide. The head, thorax, and abdomen
are shiny, metallic green. With the exception of the
head, much of the dorsal side of the body is cov-
ered with hard, coppery-brown elytra that do not
fully extend to the tip of the abdomen. Another
distinguishing character is the presence of five
patches of white hairs that are located on each side
of the abdomen, as well as another pair of white
tufts on the dorsal side of the terminal abdominal
segment posterior to the elytra. These tufts of hairs
differentiate Japanese beetles from all other beetles
that they closely resemble. Like many other insect
species, the females are typically slightly larger
than their male counterparts. Newly laid eggs are
pearly white and oblong, approximately 1.5  mm
long. Upon absorption of water from soil mois-
ture, the eggs become spherical, almost doubling
in size within a few days. The larvae are typical
white grubs with three pairs of distinct, jointed
legs, and a yellowish-brown head capsule; they too
assume the C-shaped position in the soil and when
handled. Newly hatched grubs are translucent
white, becoming darker once they have fed. Like
all white grub species, there are three larval instars.
First instars are approximately 1.5 mm long, and
fully mature third instars are 25–30  mm long.
When compared to European chafers, masked
chafers, and May beetles, they are considerably
smaller. Japanese beetle larvae can be identified
easily by their distinctive raster pattern that exhib-
its two rows of short spines that are arranged in
the shape of a truncated V pattern. Pupae are typi-
cally scarab-like, and are cream colored initially,
but gradually become tan to light brown. They
measure about 14 mm long and 7 mm wide. Within
a few days of adult emergence, the pupa appears
metallic green.
Japanese beetle adults feed on over 300 spe-
cies of herbaceous and woody ornamental plant
species, including numerous popular shade trees.
Initial feeding damage usually occurs in the upper
canopy of preferred trees, on the upper leaf sur-
face, leaving only a lace-like skeleton of the leaf
veins. The grubs feed on the roots of equally as
many plants, including all cool-season turfgrasses,
weed species and ornamental plants. Damage to
turfgrass by grubs results in thinning, wilting, and
subsequent irregular patches of turf that can be
readily pulled back or rolled up from the soil like a
roll of carpet. Feeding damage by larvae to orna-
mental plant material frequently results in poor
plant health and in some cases eventual death of
the plant material.
Much like many other scarab species, the Jap-
anese beetle has a 1-year life cycle throughout
most of its range in the U.S. Depending on geo-
graphic location, adult emergence is most com-
mon in mid- to late June with peak activity
occurring in early July. Emergence may occur
about 2  weeks earlier in the Carolinas and
2–3 weeks later in the more northern states. Within
days of emergence, mating and egg-laying occurs.
Virgin female adults call males with a chemical sex
attractant (pheromone). As many as 20–100 males
 Turfgrass Insects of the United States: Biology and Management
may aggregate around a single female attempting
to mate with her. After mating, the female will seek
out suitable turfgrass sites in which to lay eggs.
Such sites include areas with moist, loamy soil
covered with well-maintained, lush, closely cut
turf. Throughout this mating and egg-laying pro-
cess, both male and female adults continue to feed
gregariously on ornamental plants, usually begin-
ning in the upper canopy of the tree. Females re-
mate after each egg-laying episode, laying eggs in
clutches of 1–4 eggs in the upper 7.5  cm of soil.
This process is repeated every few days during the
normal lifespan of a female, 30–45  days, during
which she may lay as many as 40–60 eggs. After
about a 2-week incubation period, the first instar
grubs begin feeding on fine, succulent roots and
organic matter, usually sometime in late July or
early August. In approximately 2–3  weeks, the
grubs will molt, becoming second instars, and
eventually reaching mature grubs (third instars)
after another 3–4 weeks. Throughout this time, as
periods of dry soil moisture or drought exist, the
grubs may burrow deeper in the soil profile. As
cooler temperatures prevail in the late fall, and the
first measurable frost occurs, the grubs will begin
to burrow deeper into the soil to depths of about
5–20  cm below the soil surface where they will
overwinter in a semi-dormant, non-feeding state.
As soil temperatures warm to above 10°C in the
spring (late March or early April), the grubs will
begin to move back up into the root zone to resume
vigorously feeding for approximately 4–6  weeks
before going back down into the soil profile to
form an earthen cell in which to pupate, normally
in late May or early June. Pupation typically
requires approximately 2–3 weeks; thereafter, adult
Japanese beetles emerge. At a latitude of Kentucky,
Virginia and Maryland, adults and eggs will be
present in July, first and second instars present by
mid-August, and third instars from late September,
and overwintering until May. Prepupae and pupae
are seen at this latitude in May and early June.
Timing of these developmental stages will be
2–3  weeks later in northern regions and about
1–2 weeks earlier in southern regions.
T 3979
May Beetles, Phyllophaga spp.
There are approximately 25 species of May beetles
that may infest and feed on the roots of turfgrasses
in North America. They are rather destructive as a
result of their large size, and because they destroy
the roots relatively close to the soil surface. Com-
pared to most other white grub species, May bee-
tles typically occur at considerably lower densities
than other turf-infesting grub species.
May beetle adults are brownish, reddish-brown
to almost black, medium- to large-sized, heavy-
bodied beetles ranging in size from 11 to 24  cm
long. Depending on species, body pubescence var-
ies greatly; some species are almost hairless, while
other are quite fuzzy. It is very difficulty to differen-
tiate among the various species. Egg are pearly white
and oval when first laid, but become more spherical
after absorbing water from the soil. When fully
mature and hydrated, eggs are nearly 2.5–3  mm
wide. In most species, fully mature or third instar
grubs are approximately 25–38 mm long. May bee-
tle grubs have a V- or Y-shaped anal slit with the
stem of the Y shorter than the arms. The most dis-
tinguishing characteristic is the raster pattern that
exhibits two parallel rows of short spines, and
resembles a zipper. The pupa is about 7–10  mm
long, and appears white initially but turns tan as it
matures. The pupa is initially enclosed in the final
larval instar skin, which soon splits and is pushed
back over the terminal portion of the abdomen.
Thus, it lies exposed in an earthen cell created by
the larva. This characteristic is common with the
Asiatic garden beetle and European chafer.
May beetle grubs attack the roots of nearly all
common turfgrasses. They cause extensive dam-
age to turfgrass much like many of the other turf-
infesting scarab species. The adults feed on tree
leaves, chewing on the tissue between the veins,
similar to Japanese beetles. Preferred hosts include
birch, elm, hickory, oak, persimmon, poplar and
walnut. In extreme situations, whole trees are
sometimes defoliated in the spring.
Depending on the species, May beetles have
1- to 4-year life cycles. Nearly all the May beetle
3980
T Turfgrass Insects of the United States: Biology and Management
species that occur in the temperate U.S. have
a 3-year life cycle, however, certain species have a
2-year life cycle in the transition zone and father
south where warm-season turfgrasses are grown.
There are a select few species that have only 1-year
cycles. All Phyllophaga species have a life cycle that
includes the developmental stages of an egg, three
larval instars, a pupa, and an adult. The adults of
most species are active from April to June depend-
ing on geographic location. In some southern
regions, though, flight activity may be seen during
any month of the year. May beetle adults emerge
and are active just after sunset, when they fly to the
tops of trees to feed and mate before returning to
the turf before sunrise. Subsequently, they are
highly attracted to lights, and often are observed
bouncing off screen doors. After mating, females
fly to the turf to burrow down approximately
8–10 cm to lay eggs singly in moist soil. An indi-
vidual female typically lays approximately 20–50
eggs in her lifespan. After an incubation period of
about 3–4  weeks, the eggs hatch and first instar
grubs begin feeding on the succulent roots of turf-
grass and organic matter. The larvae then quickly
develop, growing and molting into fully developed
second instars by early fall (September). Thereaf-
ter, they continue feeding into the late fall before
the first measurable frost occurs, when they
migrate downward to lower depths for overwin-
tering. In the early spring, the following April, the
second instars migrate upward to resume feeding
on the roots of turfgrass, eventually molting into
third instars by mid-June. The third instars con-
tinue to feed and grow, causing most of their dam-
age in July and August. For May beetle species with
a 2-year life cycle, they will reach their full size and
pupate by the end of the second summer. Most of
these 2-year species reach full maturity as adults
by late fall of the second year, but remain in the
soil throughout the winter, emerging the following
spring. For species with a 3-year life cycle, as cooler
temperatures prevail during the fall of the second
year, the nearly fully mature larvae slowly migrate
downward again in late September and early
­October to overwinter. Finally, in the third year of
the life cycle, in the early spring during late March
and early April, the third instars again migrate
upward to feed throughout April and May before
they complete their larval development. In June,
the larvae migrate slightly downward to a depth of
approximately 15–25  cm where they form an
earthen cell in which to pupate. By late June, the
third instars become prepupae, transform into
pupae in July and August, becoming adults some-
time in late August or early September. The young
adults remain in the aforementioned earthen cell
until the following spring, when they emerge in
May or June. Regardless of whether the species has
a 2- or 3-year life cycle, most of the damage is
occurs during the second year.
Northern and Southern Masked
Chafers, Cyclocephala borealis
(Arrow) and Cyclocephala lurida
(Bland)
Both northern and southern masked chafers are
native to North America, and are widely distrib-
uted from the Atlantic seaboard westward to the
Rocky Mountains and into the southwestern U.S.,
and from southern New York to as far south as
South Carolina. Northern and southern masked
chafers are among the most destructive insect
pests of turfgrass in the Midwest and Central U.S.,
causing typical white grub damage. In addition,
there is often significant indirect injury due to the
feeding of vertebrate predators on these grubs.
Distribution of both species overlaps throughout
much of the Midwest. However, southern masked
chafers are more common in the southern extent
of their range.
Northern and southern masked chafers are
quite similar in appearance and size in all life stages.
Northern masked chafer adults are dull yellow-
brown beetles, approximately 11–12  mm long
and 6–7 mm wide. The only distinction from the
southern masked chafer is that southern masked
chafer is more shiny, and reddish-brown. Males
and females of both species have distinguishable
 Turfgrass Insects of the United States: Biology and Management
darker, chocolate brown color across the head
and eyes that enables one to differentiate them
from most other scarab species that are similar
in size and color. Other important morphologi-
cal characteristics that help to identify northern
masked chafer beetles are the dense hair on the
ventral side of the thorax, and the scattered
arrangement of erect hairs on the wing covers.
The adults of southern masked chafer lack such
hairs. Newly laid eggs of both the northern and
southern masked chafers are pearly white, oval,
approximately 1.3–1.7 long, that like other white
grub species, become considerably larger and
more spherical after absorbing water from the
soil. The larvae of northern and southern masked
chafers are typical white grubs with a C-shaped
body and six jointed legs. It is practically impos-
sible to differentiate the two species. Newly
hatched grubs are translucent white, becoming
grayish after feeding, and they are about 4–5 mm
long. Fully mature northern and southern
masked chafer grubs are considerably larger and
more robust than Japanese beetle larvae, ranging
in size from 23 to 25 mm in length. They also
have a reddish-brown head capsule compared
to  a more yellowish-brown head capsule in
­Japanese beetles. Their raster pattern exhibits
an  evenly spaced, non-uniform arrangement of
approximately 20–30 stout hairs. Pupae are
approximately 17 mm long and are creamy
­initially, later becoming reddish-brown as they
mature.
Although northern and southern masked
chafer grubs eat the roots of all turfgrasses, includ-
ing endophytic cool-season species, they also feed
on decaying organic matter and frequently are
found in mulched plant beds, heavier organic soils
and compost heaps. When damage does occur to
turf, typical white grub feeding damage is com-
mon. The adults do not feed or cause damage to
turf or other plant material.
The northern and southern masked chafers
both have a 1-year life cycle like many other scarab
species. The adults are active in June and July, with
peak activity occurring in late June through early
T 3981
July in areas such as southern Ohio. They may be
observed up to a month earlier in more southern
locations. There is a distinct difference in adult
behavior between northern and southern masked
chafers. Southern masked chafer is predominantly
active from just after sunset until around 11:00 p.m.,
whereas northern masked chafer is mostly active
after midnight. Otherwise, their behavior is quite
similar in that they swarm over the turf surface on
warm, humid nights, especially after a heavy rain,
in search of mates. As soon as mating occurs, the
female will burrow into the turf canopy to lay her
eggs in the soil. The eggs are laid singly or in small
clusters in the upper 2.5–5 cm of the soil. The incu-
bation period is approximately 14–18 days depend-
ing on temperature, and most eggs hatch by late
July to mid-August. When soil moisture is ade-
quate, the larvae will grow and develop relatively
quickly, molting into second instars in approxi-
mately 3  weeks. By early September, the grubs
develop into third instars, continuing to feed and
grow until about mid- to late October when cooler
soil temperatures force them to go deeper into the
soil profile to overwinter. Similar to other white
grub species, they overwinter in a earthen cell just
below the frost line. In the spring, when tempera-
tures become conducive, they migrate back up into
the root zone to resume feeding until fully mature
in mid- to late May. Thereafter, the fully mature lar-
vae begin moving down into the soil profile to form
earthen cells to pupate. The prepupal life stage pro-
ceeds, requiring approximately 4–6 days, while the
pupal stage typically takes about 14–20 days to
complete. Thereafter, adult beetles begin emerging
in mid- to late June.
Oriental Beetle, Exomala orientalis
(Waterhouse)
The Oriental beetle is native to the Philippines,
but  was accidentally introduced into the U.S. in
Connecticut sometime before 1920. It was initially
called the “Asiatic beetle” when it was first discov-
ered in the U.S. The Oriental beetle is primarily
3982
T Turfgrass Insects of the United States: Biology and Management
a pest of regional importance in the northeastern
temperate U.S. However, in recent years it has
caused extensive damage to turfgrass (both warm-
and cool-season turfgrass) as far south as north-
ern Georgia. It is present throughout the
Appalachian mountains and even the foothills in
North Carolina. Like most turf-infesting scarabs,
it causes typical grub damage.
Adult Oriental beetles are broadly rounded
beetles approximately 9–10 mm long with rela-
tively spiny legs. The adult beetles range in color
from predominantly straw-colored to nearly
entirely brownish-black. Their head is typically
solid dark brown and the elytra have distinct
­longitudinal grooves. The eggs are somewhat
milky-white, oblong, approximately 1.5 mm long,
becoming slightly larger and more spherical after
absorption of water. Oriental beetle larvae closely
resemble Japanese beetle grubs. Both species have
a transverse anal slit, though they can be differen-
tiated easily by their raster patterns. Oriental
­beetle grubs have two parallel rows of 10–16 short,
stout inward-pointing spines. Fully mature (third
instar) Oriental beetle grubs are approximately
20–25 cm long. The prepupa resembles that of the
Japanese beetle. Pupae are approximately 10  cm
long, cream colored at first, but eventually become
light brown as they age. The pupa also has as dis-
tinct thick fringe of hairs at the terminal segment
of the abdomen.
Oriental larvae feed and destroy the roots of
all cool-season turfgrasses as well as nursery stock
and strawberry. The resulting damage is typical of
most turf-infesting white grub species. The adults
cause very little damage to plant material.
Like most scarab species that infest turf, the
Oriental beetle has a 1-year life cycle. Its life cycle
is similar to that of the Asiatic garden beetle and
the Japanese beetle, with adults emerging in late
June to early July. In many areas, the adults emerge
a week or two earlier than the Japanese beetles.
Because they are relatively weak fliers as compared
to the Japanese beetle, they often are found crawl-
ing around, especially on flowers. Adult females
lay their eggs singly 2.5–23 cm deep in moist soils.
Each female lays about 25 eggs in her lifetime,
throughout July and into early August. The eggs
typically hatch after an incubation period of about
3 weeks. The larvae immediately begin feeding on
the succulent roots of turfgrass, growing and
developing into second instars by early September,
and third instars by early October. Grub damage is
most apparent in early September, especially when
the turf is experiencing heat and drought stress. As
cooler soil temperatures prevail, the nearly mature
grubs burrow down into the soil to hibernate in
earthen cells. In the spring, when soil temperatures
are conducive in April and early May, they migrate
back to the root zone to feed until early June.
Thereafter, the grubs again burrow down slightly
into the soil profile to pupate in earthen cells. The
prepupal and pupal periods last for approximately
1–2  weeks, respectively. Nearly all of the grubs
pupate by mid- to late June, and the adult beetles
subsequently begin emerging in late June. Timing
of these developmental changes may be approxi-
mately 1–2 week earlier in the southern region of
its distribution (North Carolina) than in the more
northern states.
Mole Crickets (Scapteriscus spp.)
(Orthoptera: Gryllotalpidae)
Mole crickets are undeniably some of the most
destructive insect pests of turfgrass in the south-
eastern United States. Four species of mole crick-
ets can be found in the U.S., although only two of
the four cause considerable damage to golf courses,
lawns and sod farms. The tawny mole cricket,
Scapteriscus vicinus Scudder, and the southern
mole cricket, Scapteriscus borellii Giglio-Tos (for-
merly S. acletus Rehn and Hebard) are believed to
have been introduced through ports in the early
1900s from South America, and are the two most
prominent pest species. Both tawny and southern
mole crickets can be found in the coastal region of
the Southeast, from the southern portion of North
Carolina over to eastern Texas. Two other species
of mole crickets, the short-winged mole cricket
 Turfgrass Insects of the United States: Biology and Management
(S.  abbreviatus Scudder) and the northern mole
cricket (Neocurtilla hexadactyla Perty) can be
found in the U.S. as well. The northern mole cricket
is a native species that rarely, if ever, reaches pest
status. It can be found from southern New England
south to Florida and west to the Central Plains.
The short-winged mole cricket is incapable of dis-
persing through flight due to its shortened wings,
and thus, is typically found in coastal areas near
ports of entry. When present in abundant num-
bers, the short-winged mole cricket can cause sig-
nificant damage to turfgrass. At this time, its
distribution is limited to Georgia, Florida, and
some areas of the Caribbean, including Haiti,
­Nassau, Puerto Rico, Cuba and the Virgin Islands.
Tawny mole crickets are a more significant
pest than southern mole crickets due to the fact
that their diet consists mostly of plant material,
including both the above-ground and below-
ground parts of the turfgrass, while the southern
mole crickets are primarily predaceous. The tun-
neling nature of both species makes them very
damaging to turfgrass. As the crickets tunnel in
their underground burrows, mechanical damage
of the root system occurs, resulting in desiccation
and susceptibility to other types of damage from
foot traffic or golf carts.
Mole crickets are difficult to mistake for
other turfgrass pests due to their unique appear-
ance. Adults are relatively large, ranging from
3.2 to 3.5  cm long, and have characteristic
shovel-like front legs. The pronotum of mole
crickets is heavily sclerotized and their bodies
are covered with a dense coat of fine hairs. The
nymphs resemble the adults, but are smaller in
size, and lack fully grown wings. At maturation,
the front wings of the southern mole crickets
and tawny mole crickets are folded back and
almost reach the tip of the abdomen. To differ-
entiate between the two species, one can look at
the coloration or the tibial dactyls. Tawny mole
crickets are typically golden brown with a mot-
tled coloration on the pronotum and more
robust, while southern mole crickets are grayish
with four pale-colored dots on the pronotum.
T 3983
The most reliable distinguishing characteristic
between the two pest species is the arrangement
of the tibial dactyls. Both species have two dac-
tyls, with the separation between the two for the
tawny mole crickets being V-shaped and nar-
rower than the width of one dactyl, while the
southern mole crickets have a larger U-shaped
space that is about the size of the width of one
dactyl.
There are three distinct developmental stages
of mole crickets: eggs, nymphs and adults. Both
species produce one generation in most areas of
their distribution, although southern mole crick-
ets may have two generations per year in south
Florida. Adults of both species have significant
dispersal flights in the spring and minor flights in
the fall. Tawny mole crickets typically fly from
February to May in Florida, while southern mole
crickets fly from March to June, and it is not
uncommon to have flights of both species occur-
ring on the same night. Flights for both species
generally occur up to a month later in their north-
ern range in the Carolinas. Tawny mole crickets
will complete most flight activity before oviposi-
tion, while southern mole crickets will fly between
clutches. The tendency of southern mole crickets
to fly between egg-layings may have contributed
to their quick spread after introduction into the
U.S. Flights begin soon after sunset and continue
for approximately 60–90 min in response to the
calls of the males. Although the majority of flying
mole crickets appear to be females, it is not uncom-
mon for males to comprise a percentage of the fly-
ing crickets. Some of the flights are performed in
an attempt to find a suitable mate, but many of the
females that fly have already mated and use the
intensity of the males’ calls to indicate good ovipo-
sition sites. The moisture levels present in the soil
influence the intensity of the calls, and because
desiccation is a major factor in egg mortality, it is
necessary for the females to find adequate soil
moisture for successful oviposition.
Once the female finds a suitable site, she will
spend about 2  weeks feeding and tunneling
before laying a clutch of 25–60 eggs. Once the
3984
T Turfgrass Insects of the United States: Biology and Management
eggs have been laid, the female seals the tunnel
and leaves the eggs to develop and hatch in
3–4  weeks, depending on the temperature.
Females of both species can lay as many as
10 clutches of eggs. Oviposition begins as early
as March for tawny mole crickets in northern
Florida, and may continue well into April and
June. Some southern mole crickets begin laying
eggs as early as April in northern Florida, with
peak egg-laying occurring in May and June.
Timing for egg-laying and hatch is usually
delayed by a month in the northern regions.
Typically all tawny eggs have been laid by the
beginning of July, while it is not unusual to see
newly hatched southern mole cricket nymphs
into September. After hatching, new nymphs will
tunnel closer to the surface and begin feeding.
As the nymphs continue to grow and go through
7–10 instars, damage will become more evident.
By December, approximately 85% of tawny mole
crickets have molted to adults, while only 25% of
the slower-developing southern mole crickets
reach maturity before winter. Those nymphs that
do not reach adulthood by winter will complete
development in the spring. Even though there
are adults of both species present by fall, no mat-
ing or egg-laying appears to occur after fall
flights. Crickets of both species overwinter as
large nymphs or adults and do not become active
again until the spring when temperatures rise.
Mole cricket activity is most significant at night
following heavy rains or irrigation when the
crickets come to the surface to forage for food.
Effective management of mole crickets
involves scouting, mapping, sampling and treat-
ment. In the spring when adults are present,
mating and flying, considerable damage may
appear. Due to the large size of the crickets,
unpredictable weather and large dispersal flights,
it is difficult to effectively control crickets in the
spring. At this time, spot treatment is advised for
sensitive or critical areas. It is also very impor-
tant to map those areas that appear to have sig-
nificant adult activity for treatment of nymphs
later. The time period after egg hatch when
nymphs are small and nearer the surface is the
best time to treat, usually in mid-June or early
July. It is best to concentrate on those areas where
adult activity was seen in the spring. Soapy water
flushes can be used to confirm the presence of
small nymphs in areas where adult activity was
seen earlier in the year. An important aspect of
control is to get the insecticide treatment to
come into contact with the crickets. Therefore,
areas of mole cricket activity should be allowed
to dry for several days and then pre-irrigated the
night before treatment, thus bringing the nymphs
closer to the surface and making control easier.
As crickets continue to grow and increase in
feeding, damage may reappear in the fall, but
effective control of small nymphs is the best way
to minimize their impact.
Ground Pearls (Margarodes spp.)
(Hemiptera: Coccidae)
Ground pearls are a common name for several
species of unique scale insects that spend most of
their life in the soil and feed on the roots of vari-
ous species of warm-season turfgrass. The two
most common species in turf are Margarodes
meridionalis Morrill and Eumargarodes laingi
Jakubski. These pests are present almost every-
where in the U.S. that warm season turfgrass is
most common, from North Carolina across to
California.
Ground pearls are subterranean, and the
female spends most of its life in the soil. The pinkish-
white eggs are laid in clusters in the soil and cov-
ered with a white waxy substance. The first instar
nymphs that hatch are only 0.2 mm long and this
crawler stage attaches itself to a root. Once attached
it covers itself with a waxy substance and begins
formation of the “pearl.” As the pearl grows it
may appear to have a purple to yellowish globular
covering. The pearls range in size from 0.5  mm
to 2 mm in size. Adult females may appear in the
late spring and throughout the summer. They are
pinkish sac-like creatures with well-developed
 Turfgrass Insects of the United States: Biology and Management
forelegs and are about 1.6 mm in length. The male
is rarely seen and has a gnat-like appearance.
Ground pearls attack a range of warm-season
turfgrasses, but appear to be most common on
bermudagrass, centipede, zoysiagrass, and St.
Augustinegrass. Centipede often appears to be the
most severely damaged. The distribution is spo-
radic, but where infestation does occur, the dam-
age can be quite serious. The nymphs (pearls) feed
on the roots by extracting plant juices (and possi-
bly injecting toxic substances), which results in an
initial appearance of unhealthy, yellow turfgrass.
This appearance usually worsens during hot, dry
summers and the plant often will turn brown and
then die. This rapid death would indicate toxin
may be involved. The damaged areas vary from a
few centimeters to several meters in diameter. The
turfgrass usually does not regrow in these areas
even the next summer. Weeds often grow in these
irregular, but somewhat circular areas. Through
time, the damaged areas may eventually coalesce
and a significant portion of the turf may die.
The life history of this pest is not well under-
stood across its range, but one generation per year
probably occurs throughout its range. Under
unfavorable conditions, the ground pearls may
take longer than a year to complete their life cycle.
The nymphs overwinter in the soil, and some
nymphs will mature in the spring and summer,
emerge from the cyst and move toward the soil
surface as adults. The adults may be seen moving
on the soil surface in late spring and all summer.
After moving for a short period of time, they
reenter the soil and move down only about
5–8  mm to secrete the waxy coat in which the
eggs will be laid a few days later. The females lay
eggs without mating, as they reproduce partheno-
genically. They lay about 100 eggs over a 2-week
period and the eggs hatch in about 10  days to
2  weeks. The new crawlers move to the roots,
attach and begin to encyst once feeding is initi-
ated. Ground pearls have been found as deep as
25–30 cm in the soil. A fungal disease of ground
pearls has been reported, and ants probably play a
significant role as predators.
T 3985
Red Imported Fire Ant (Solenopsis
invicta Buren) (Hymenoptera:
Formicidae)
The red imported fire ant has become a pest of
great significance throughout the warm season
turfgrass areas of the South, particularly the South-
east west to Texas. This introduced species of ant
was accidentally introduced from South America
into the Mobile, Alabama, area around 1930. This
ant has spread rapidly throughout the South in all
areas with mild winters and adequate moisture.
States as far north as Virginia and Tennessee now
battle this problem.
The mounds from fire ants are typically coni-
cal in shape and vary considerably in size, but large
mounds are usually 25–40  cm in diameter and
may be 20–30 cm in height. The mounds may pen-
etrate more than a meter into the soil. In very
sandy soils the mounds may be less well devel-
oped. They usually are found in open sunny areas
and often appear following a disturbance of the
soil (e.g., construction). Mounds commonly
appear at the base of trees, structures, near rotting
logs and stumps, power boxes, and along curbing
and sidewalks. A mound contains three forms
of adult ants as well as the brood (immature ants).
Adult ants can be black reproductive males, queens
or worker ants. The large egg-laying queens have
no wings while the unmated queens and males are
winged. The worker ants (which are the ants most
commonly seen foraging near the mound) are
wingless, sterile females and they vary in size from
1.5 to 4 mm in length. These workers have a shiny
black abdomen and reddish-brown head and
thorax.
Red imported fire ants forage and feed on a
variety of materials, often on insects and related
organisms, seeds, carrion and discarded food
items. These ants can both sting and bite, but the
venom from their sting is the biggest problem.
They can sting repeatedly and are quite aggressive
against anything that disturbs their mound. A rel-
atively small percentage of people are hypersensi-
tive to the venom in the imported fire ant sting
3986
T Turfgrass Insects of the United States: Biology and Management
and can become quite ill from even one sting. Fire
ants also cause problems by creating unsightly
mounds that may smother the turfgrass, create an
uneven surface, and damage mowing equipment.
They do not feed directly on the turfgrass, but they
can be found infesting any turfgrass species that
grows in a climate appropriate for fire ant
survival.
Mating flights can occur any time of year,
but are most common in the spring and early
summer. Mating flights often occur after a rainy
period. Reproductive males and unmated females
(both winged) fly in the spring and after comple-
tion of the mating flight, the newly mated queen
lays eggs in a small chamber in the soil. The males
die soon after the flight, while the queen sheds
her wings and begin the task of starting a new
colony. Approximately 10–15 eggs are laid and
once they hatch in a little over a week, the queen
takes care of them until they are adults in about
3  weeks. These adults then begin taking care of
the queen and egg production increases up to
200 eggs per day. These new fire ants mounds are
inconspicuous, and often are not noticed until
fall. During the summer, the colony increases in
size and by late in the year, the above-ground
portion of the mound may be quite prominent.
Mature colonies may contain anywhere from
100,000 to more than 500,000 ants. The workers
typically live 2 months, but a queen can survive
for 5 years. Some colonies may contain more than
one queen. Colonies with single queens are more
territorial and areas with such colonies usually
will have 40–150 mounds per acre. Multiple
queen colonies are less protective and workers
roam freely from one mound to another. There
may be more than 200 mounds per acre in these
situations.
Management of Turfgrass Insect Pests
Effective and environmentally responsible insect
pest management begins with a planned, well-
designed control strategy that considers a
­ ultitude of tactics including but not limited to
m
biological, chemical, cultural, and plant resis-
tance. This pest management strategy is referred
to frequently as Integrated Pest Management
(IPM). IPM relies on a combination of preventa-
tive and curative (i.e., corrective) measures to
keep pest densities below levels that would cause
unacceptable damage. The goal of IPM is to man-
age pests effectively, economically, and with
nominal risk to people, animals and the environ-
ment. IPM is not a rigid pest management pro-
gram that precludes the use of pesticides, nor is it
a biological or organic pest control program. IPM
is merely a decision making process that consid-
ers all control tactics that will provide acceptable
control of a respective pest. When successful,
IPM typically reduces dependence on pesticides.
The process of IPM involves the following
seven principal steps:
Sampling and Monitoring
Regularly inspecting areas of turf throughout the
growing season enables a turfgrass manager to
detect pests early, before they reach damaging lev-
els. Monitoring can aid in assessing the need for
action, provide an evaluation of the success of pre-
viously implemented control tactic(s), and develop
site history information that will provide invalu-
able insight for potential future problems.
Pest Identification
Accurate identification is essential. The biology of
a pest cannot be understood if the pest is not cor-
rectly identified.
Decision-Making
Management decisions are guided by action
thresholds (density of pests that will cause unac-
ceptable damage). As decisions are made, factors
 Turfgrass Insects of the United States: Biology and Management
such as likelihood of success, treatment cost and
environmental consequences are considered.
Appropriate Intervention
All appropriate management tactics, including
biological, chemical, cultural control and plant
resistance, must be considered. Turfgrass manag-
ers first must attempt to determine the cause of the
pest outbreak, and make the necessary cultural
management practice adjustments to reduce the
risk of future problems. Occasionally, insecticide
treatments may be warranted, however, always
consider less toxic products when practical.
Follow-up
Through consistent and disciplined sampling and
monitoring, turfgrass managers can effectively
evaluate the success of a control tactic as well as
determine the need for further action.
Record-Keeping
Accurate and detailed record-keeping enables a
turfgrass manager to recall when and where spe-
cific pest problems have occurred and to plan to
deal with them in the future. Such information can
help managers to evaluate previous management
practices and may provide insight in developing
and/or modifying future pest management pro-
grams. Record-keeping also provides managers
with a document that may circumvent potential
litigation.
Employee and Client Information
Another crucial component of a successful IPM
program is communication. This involves edu-
cating employees, clients and the public. Educa-
tion of employees can be accomplished by
T 3987
developing ongoing training programs that focus
on pest recognition, and biology and agronomic
factors that affect pest management decisions.
Other educational opportunities, such as field
days, workshops and short-courses, also provide
valuable training that helps induce employees
to  work more safely and effectively as well as
helping to increase professionalism and envi-
ronmental stewardship. As for effective client
communication, information vehicles such as
newsletters, fact sheets, bulletins, fliers, personal
communication, electronic mailings, etc., all pro-
vide excellent opportunities to convey valuable
information. Finally, communication to the pub-
lic sector can be accomplished through newspa-
per articles, bulletins, open houses, town meetings,
television promotions, etc.
IPM considers all appropriate management
options, including biological, chemical, cultural
and plant resistance.
Biological Control
Biological control is the use of predators, parasi-
toids, and disease-causing microbes or patho-
gens to suppress pest populations (Table  17).
Compared to chemical control research, to date
there has been very little research on the impact
and use of predators and parasitoids in the turf-
grass system. Most biological control research
efforts have been directed at microbial control
(i.e., bacterial, fungal, viral, and entomopatho-
genic nematodes). Moreover, of this work, much
has focused on entomopathogenic nematodes
(i.e., insect parasitic nematodes). Entomopatho-
genic nematodes are microscopic roundworms
that attack and kill insect larvae, and reproduce
within the dead host. They are beneficial organ-
isms that naturally occur in most soils, and they
are practically harmless to humans, plants and
animals. There are numerous species of insect
parasitic nematodes; different species and strains
of nematodes vary in their activity against dif-
ferent species of insects. As with many biological
3988
T Turfgrass Insects of the United States: Biology and Management

control agents, specific environmental condi- Chemical Control

tions must be met in order for nematodes to be
effective: they are sensitive to direct sunlight and
high temperatures, and they require thin films of
water that enable them to move over soil
particles.
Despite the potential that biological control
agents possess, only a limited number of compa-
nies currently market biological control agents. As
a result, product availability and cost often dis-
courage turfgrass managers from integrating them
into their integrated pest management program.
To further confound the reluctance of the use of
biological control agents, they are frequently
directly compared to conventional insecticides,
and because they do not consistently perform at
the same level, they are often discounted or not
considered as a viable control option. Nonetheless,
more consideration should be given to biological
control agents.
When used judiciously, selectively and responsi-
bly, insecticides are tremendously important tools
in an overall IPM program. To date, chemical con-
trol continues to be the most common control
strategy. This is likely due to numerous factors
such as convenience, economics, effectiveness,
familiarity and/or confidence of turfgrass manag-
ers with this strategy. Nonetheless, chemical con-
trol should not be the primary line of defense in
managing turfgrass insect pests. When effective,
alternative control strategies are available, always
consider tactic(s) that have the least risk to people
and the environment. Conversely, in some
instances alternative, non-chemical control strate-
gies may not be available. Thus, insecticide treat-
ments may be the only control option. Subsequently,
when selecting an insecticide, always consider
products that are least hazardous to people and

Turfgrass Insects of the United States: Biology and Management, Table 17  Beneficial invertebrates:
predators and parasitoids
Organism Taxonomy Type Host(s)
Ant Hymenoptera: Formicidae Predator Eggs and larvae of numerous
insects
Big-eyed bug Hemiptera: Geocoridae Predator Chinch bug, greenbug, mites,
eggs and larvae of small
arthropods
Entomopathogenic Secernentea: Rhabditida Predator/Pathogen Numerous insect larvae
nematodes
Green lacewings Neuroptera: Chrysopidae Predator Aphids, mealybugs, and other
soft-bodied arthropods
Ground beetles Coleoptera: Carabidae Predator Eggs and larvae of numerous
arthropods
Tiger beetles Coleoptera: Carabidae Predator Eggs and larvae of numerous
arthropods
Lady beetles Coleoptera: Coccinellidae Predator Aphids and mealybugs
Rove beetles Coleoptera: Staphylinidae Predator Eggs and larvae of arthropods
Scoliid wasps Hymenoptera: Scoliidae Parasitoid Green June beetle larvae and
other white grubs
Spiders Arachnida: Araneida Predator Most insects
Tiphiid wasps Hymenoptera: Tiphiidae Parasitoid Most white grub species
 Turfgrass Insects of the United States: Biology and Management
the environment, and that will provide the most
effective control in an economical manner.
As previously mentioned, turfgrass insects
can be categorized into three primary groups (i)
leaf and stem, (ii) thatch, and (iii) root zone/soil.
Subsequently, chemical control of insect pests in
respective groups require specific considerations
and application procedures.
Leaf and Stem Insect Pests
The turf area should be mowed and the clippings
removed prior to the insecticide application to
enhance the insecticide penetration into the turf
canopy. A thorough irrigation before an insecti-
cide application will help move insects out of the
turf canopy (i.e., thatch and soil) and bring them
to the surface. For night feeding insects such as
black cutworm or sod webworm larvae, insecti-
cide applications should be made in the late after-
noon or early evening to maximize potential for
exposure to the target pest and minimize the like-
lihood of photodegradation (i.e., sunlight decom-
position) and volatilization of the insecticide, as
well as reduce pesticide exposure to humans and
animals. When liquid (i.e., sprayable) insecticides
are used, avoid irrigation for at least 12 h to maxi-
mize contact and subsequent control. Regardless
of insecticide formulation, avoid mowing turf after
application for at least 24 h. When granular prod-
ucts are used, a moderate application (i.e., one-
quarter inch or 6 mm) of irrigation is recommended
to help dissolve and activate insecticide granules.
Liquid and granular applications have their respec-
tive advantages and disadvantages. Liquids typi-
cally provide greater mortality from initial contact
and they frequently leave a residue that results in
some residual control. In contrast, granules have
little initial contact activity, and because they have
a tendency to bounce off the foliage, they are not
effective against foliage dwelling insects such as
mites and greenbugs. However, they provide some-
what longer residual control of thatch dwelling
insect pests.
T 3989
Thatch Inhabiting Insect Pests
Turfgrass insects that inhabit thatch can be diffi-
cult pests to control depending on the quantity of
thatch accumulation, as well as the active ingredi-
ent and formulation of the insecticide. When
thatch accumulation is one-half inch (12 mm) or
greater, the effectiveness of insecticide applica-
tions is greatly impeded. Consequently, reducing
the thatch layer by de-thatching or aerification
prior to an insecticide application will increase
insecticide efficacy. Another important tactic for
effective management of thatch inhabiting insect
pests is to apply a moderate (i.e., one-quarter inch
or 6 mm) amount of irrigation prior to the insec-
ticide application to maximize the likelihood of
the treatment reaching the target pest. Overall,
granular insecticides tend to perform better than
liquid formulations, however, the active ingredient
of the product is the overriding factor that influ-
ences the effectiveness.
Root Zone/Soil Inhabiting Insect Pests
Soil dwelling or root feeding insect pests are often
the most difficult to control. Pests such as white
grubs and mole crickets can be controlled with
either liquid or granular insecticides. The two pri-
mary strategies for controlling soil inhabiting or
root feeding insects are (i) preventative and (ii)
curative (i.e., corrective) control.
Preventative control is a strategy in which an
insecticide is applied before a possible insect prob-
lem and subsequent damage develops. This approach
can be compared to an insurance policy; potential
damage is avoided or minimized. This approach to
insect pest management can be quite attractive
to  turfgrass managers since it is relatively easy to
implement and it requires dramatically less time
and effort in monitoring, sampling and decision-
making. Preventative control requires the use of
insecticides that have a relatively long residual
­activity (i.e., more than 100  days). Nonetheless,
turfgrass managers must still understand the
3990
T Turfgrass Insects of the United States: Biology and Management
­biology of  the pest in order to accurately time
the treatment to ensure maximum control of the
target pest.
Curative control is the complete opposite of
preventative control; this approach is essentially a
reactionary or corrective strategy. This approach
heavily relies on monitoring and sampling of turf
areas. When populations of a turfgrass insect pest
are determined to be above an unacceptable level
(i.e., threshold), an insecticide application is made
to control the pest. Curative control applications
typically are applied after damage is evident,
though ideally before severe damage results.
Regardless of the formulation or active ingredient
of the insecticide, the application must be watered
in thoroughly with a minimum of one-half to
three-quarters of an inch (12–18  mm) of post
treatment (i.e., after the application) irrigation to
move the residue through the thatch to the target
zone where the pest is located. If an irrigation sys-
tem is not available, simply rely on anticipated
rainfall. Another effective strategy for optimal
control of soil inhabiting and root feeding insects
is the application of pretreatment irrigation. The
application of one-half inch (12  mm) of water
24–48 h before insecticide treatment will encour-
age the target insects to move closer to the surface
and to decrease the absorbency of the thatch. This
approach is especially important if conditions
have been hot and dry and insects are deeper in
the soil.
When using any chemical control agent or
product, always read and follow the label direc-
tions. Be conscientious of the potential impact on
humans, animals and the environment. Consider
using products that are the least toxic and hazard-
ous. Ultimately, remember that there are no “silver
bullets” that will eliminate all pests.
Cultural Control
Cultural control is described as suppressing pest
populations or reducing their damage by normal
or slightly modified management practices. These
measures must be implemented before the insect
reaches pest status or damage occurs. Essentially,
cultural control is a proactive approach to pest
management. Such management practices include,
but are not limited to, (i) mowing, (ii) irrigation
and drainage, (iii) fertility, and (iv) thatch manage-
ment. Ultimately, healthy turfgrass is more toler-
ant to potentially damaging insect populations.
Mowing
Generally, proper mowing practices such as
sharp mower blades and removing no more that
one-third of the grass blade at each mowing
will  make the turf healthier and subsequently
more tolerant to insect damage. Excessively close
mowing and/or scalping greatly reduces plant
vigor, thus decreasing tolerance to environmen-
tal stresses. As a result, close-cut turf tends to
have greater susceptibility to damage from cer-
tain turfgrass insect pests. Close and consistent
mowing may remove the eggs of some insect
pests such as the black cutworm.
Irrigation and Drainage
Irrigation and drainage can have both a positive
and negative impact on the potential for insect
damage. Certain insect pests prefer hot and dry
conditions while other prefer irrigated turf where
soils have adequate moisture. For example, Japanese
beetle adults will seek out moist areas of turf to
lay  their eggs. This is likely due to the fact that
moist soils are required for egg and young larval
survival. Thus, withholding irrigation during adult
egg-laying may reduce the potential for survival of
eggs and subsequent grub damage. Unfortunately,
this cultural management strategy is not practical
for a golf course manager since adult activity
occurs in late June through August. Conversely,
turfgrass insect pests such as chinch bugs prefer
hot and dry conditions for survival and optimal
reproduction. Therefore, irrigating or watering
 Turfgrass Insects of the United States: Biology and Management
when chinch bugs are present will help to mini-
mize damage and subsequent survival and repro-
duction. Overall, sound irrigation contributes to
healthy, vigorous turf, thus, the turf is able to with-
stand higher pest populations and recover more
rapidly from insect damage.
Fertility
Similar to the effects of irrigation and drainage,
fertility also can have both a positive and negative
impact on the potential for insect damage. For
example, high levels of nitrogen fertility often
result in rapid, succulent growth, subsequently
increasing the likelihood of insect damage. Exces-
sive nitrogen fertilization coupled with improper
irrigation and mowing also can result in a thatch
accumulation which provides a hospitable envi-
ronment for insects such as billbugs, cutworms,
chinch bugs, and sod webworms. Additionally,
heavy fertilization of cool-season turfgrasses in
the spring stimulates rapid shoot growth at the
expense of a deep, healthy root system. These weak,
shallow-rooted turfgrass plants are less likely to
recover from insect damage. A proper, well bal-
anced fertility program can result in health, vigor-
ous turf that has a greater potential to recover
from insect damage. Moreover, in some instances,
fertilization coupled with appropriate irrigation
can aid in the ability of turf to recuperate from
insect injury such as white grub damage. For spe-
cific fertility and irrigation recommendations,
consult your local cooperative extension agent or
state specialist.
Thatch Management
Thatch is described as a tightly intermingled layer
of living and dead roots, crowns, rhizomes, stolons
and organic debris that accumulates between the
zone of green vegetation and the soil surface. Cer-
tain levels of thatch (i.e., less than one-half inch or
12 mm) accumulation are beneficial, however, this
T 3991
layer in the turf canopy also provides a prime hab-
itat for insect pests. In addition, thatch also acts as
a barrier to the penetration of soil insecticides tar-
geted at soil dwelling and root feeding insects. As
a result, turfgrass managers frequently spend valu-
able time and resources attempting to reduce
thatch to an acceptable level. Thatch accumulation
can be managed effectively through proper irriga-
tion, fertility, aerification and verticutting (i.e.,
vertical mowing or de-thatching).
Plant Resistance
Establishing insect-resistant turfgrasses is another
valuable IPM tool. Resistance to insects has been
discovered in numerous plants, though the degree
of resistance may vary considerably from one
plant species to another. Even within a species, one
cultivar or variety can have varying levels of resis-
tance to particular insect pests. When it comes to
plant genetics, there are often trade-offs associated
with plant resistance. While a plant may be devel-
oped for a characteristic such as color, other ben-
eficial traits may be sacrificed or lost to attain this
trait (e.g., insect resistance). Unfortunately, plant
resistance to insects is a relatively low priority of
both managers and plant breeders. There is higher
priority or value in developing a plant material
that exhibits improved color, texture, growth, cold-
hardiness, disease resistance, etc. Subsequently,
only a few insect resistant turfgrasses exist. None-
theless, of the insect resistant turfgrasses that are
available, most are quite effective in managing
pests. One mechanism by which plant resistance is
expressed is via endophyte-infected turfgrasses.
Endophytes are fungi that live within healthy grass
plants, but have no adverse effect on the turfgrass
plants. To date, they are known to occur only in
perennial ryegrass, and tall and fine-leaf fescues.
Endophytes produce alkaloids that are toxins that
do not harm the plant, but are either deterrents or
toxicants to the insects that feed on the above-
ground plant parts, including stems, leaf sheaths
and leaves. Only nominal levels of the alkaloids
3992
T Turnip Aphid, Lipaphis erysimi (Kaltenbach) (Hemiptera: Aphididae)
are present in root tissues, thus, endophyte-
infected turfgrasses do not provide meaningful
control of root feeding insects. In addition to the
insect resistance attributes that endophytes have,
they also may improve stress tolerance and
enhance resistance of turfgrass to some diseases.
Unfortunately, there are no endophytic cultivars of
Kentucky bluegrass or creeping bentgrass, nor do
they occur in warm-season turfgrasses.
References
Brandenburg RL, Villani MG (1995) Handbook of turfgrass
insect pests. Entomological Society of America, Lan-
ham, MD
Niemczyk HD, Shetlar DJ (2000) Destructive turf insects.
H.D.N. Books, Wooster, OH
Potter DA (1998) Destructive turfgrass insects. Ann Arbor,
Chelsea, MI
Vittum PJ, Villani MG, Tashiro H (1999) Turfgrass insects of
the United States and Canada. Cornell University Press,
Ithaca, NY
Watschke TL, Dernoeden PH, Shetlar DJ (1995) Managing
turfgrass pests. Lewis, Ann Arbor, MI, 361 pp
Turnip Aphid, Lipaphis erysimi
(Kaltenbach) (Hemiptera:
Aphididae)
John L. Capinera
University of Florida, Gainesville, FL, USA
Turnip aphid is found in both tropical and
­temperate areas throughout the world. It is often
confused with cabbage aphid, however, so distri-
butional records and economic impact of both
species are sometimes incorrectly reported.
Life History
The turnip aphid is very prolific. Under temperate
conditions, 11–25 generations are reported annu-
ally. Under the warmer conditions, up to 35 gen-
erations have been observed annually. Aphid
longevity is usually 20–40 days, and reproduction
begins about 6  days after aphids reach maturity.
Wingless parthenogenetic females typically pro-
duce 80–100 young, often at a rate of 4–6 per day.
Winged parthenogenetic females produce fewer
offspring.
An egg-producing (oviparous) female form
is known. Egg deposition rarely occurs, however,
with nymph-producing (viviparous) forms occur-
ring on crops and weeds throughout the year,
even in cold climates. Oviparous females have
been observed on several continents, however.
Therefore eggs, although rarely observed, may
occur on crops.
There are four instars. Nymphs are pale green-
ish yellow in color, and average about 0.6, 0.9, 1.0,
and 3.3 mm in length during the four instars,
respectively.
The wingless (apterous) adult females are
whitish green or green in color, and measure about
1.4–2.4  mm in length. The dorsal surface of the
thorax and abdomen of wingless adult females is
marked with two rows of dark bands, which
coalesce into a single band on the distal abdomi-
nal segments. The legs are pale with dusky joints.
The antennae are dark and the cornicles pale with
dusky tips. The entire body is lightly covered with
a white secretion (Fig. 116).
Turnip Aphid, Lipaphis erysimi (Kaltenbach)
(Hemiptera: Aphididae), Figure 116  Wingless
adult female of turnip aphid, Lipaphis erysimi
(Kaltenbach).
 Turnip Aphid, Lipaphis erysimi (Kaltenbach) (Hemiptera: Aphididae)
T 3993

The winged (alate) adult females are pale Rondani (Diptera: ­C ecidomyiidae) prey on the
green in color, with a black head and thorax. The aphids. Fungus epizootics sometimes occur
last three abdominal segments are marked dor- when aphid population densities are high, espe-
sally by narrow black bands. The sides of the cially during the autumn months.
abdomen also bear black patches. The legs are
brownish to blackish, and the antennae black.
The cornicles are dusky yellowish, with a small
Damage
black area around the base. The wings are trans-
parent, but marked with conspicuous black veins.
Turnip aphids feed principally on the undersides
Winged females measure about 1.4–2.2  mm in
of leaves, but under high aphid densities or during
length.
the winter months the aphids may move to the
Males have also been observed occasionally,
center of the plant and feed on both the upper and
but are too infrequent for their biology to be
lower surfaces of tender young foliage. They also
known. The wingless male is quite small, measur-
feed readily on the stem tissue of the flowers.
ing 1.2–1.3 mm in length. It is olive-green to
Heavy infestations will kill plants, and even light
brown in color.
infestations will cause the leaves to cup, with yel-
Turnip aphid generally can be differentiated
lowing of the foliage occurring where aphids are
from cabbage aphid by the very sparse occurrence
concentrated. Stunting of the plants is common,
of waxy exudate on the body, and by the slightly
but contamination of foliage with aphid bodies,
longer cornicles, 0.23 mm, of the former. In humid
cast skins, and honeydew is the principal type of
climates, however, there tends to be greater accu-
direct damage.
mulation of waxy secretions on the aphid body.
Turnip aphid may also serve as a vector of
Therefore, it is probably better to use the shape of
stylet-borne plant viruses. At least 10 viruses are
the cauda, a structure found at the tip of the abdo-
transmitted, including cabbage black ring spot,
men, to differentiate these two species. When
cauliflower mosaic, radish mosaic, and turnip
viewed from above, the cauda of cabbage aphid is
mosaic virus.
triangular, about as wide as long. In contrast, the
cauda of turnip aphid is slender, about twice as
long as wide.
This aphid has been found associated with all Management
Brassica crops, including such vegetables as broc-
coli, Brussels sprouts, cabbage, cauliflower, col- Aphid water pan or sticky traps capture winged
lards, kale, kohlrabi, mustard, radish, rape, turnip, turnip aphids, but trap catches do not correlate
and watercress. Cruciferous weeds also are known well with overall aphid populations on plants.
to be suitable hosts. However, these techniques are useful to detect
Turnip aphid is host to many parasitoids when winged aphids enter fields. This infor-
and predators. Diaeretiella rapae (MacIntosh) mation is critical for the prevention of popula-
(Hymenoptera: Braconidae) is frequently reported tion establishment and the transmission of
to be an important biological suppressant, but in viruses.
rapidly maturing crops such as radish apparently Although sanitation is perhaps the most
there is insufficient time for the parasitoids to important factor in turnip aphid management,
attain high levels of abundance. Various ladybird insecticides are used extensively. Systemic and
beetles (Coleoptera: Coccinellidae), flower flies nonsystemic insecticides are commonly applied in
(Diptera: Syrphidae), lacewings (Neuroptera: liquid or granular formulations, often at short
Chrysopidae), and the fly Aphidoletes aphidimyza intervals.
3994
T Turnip Root Maggot, Delia floralis (Fallen) (Diptera: Anthomyiidae)
References
Capinera JL (2001) Handbook of vegetable pests. Academic,
San Diego, 729 pp
Cottier W (1953) Aphids of New Zealand. New Zealand
Department of Scientific and Industrial Research
­Bulletin 106, 382 pp
Davis JJ, Satterthwait AF (1916) The false cabbage aphid
(Aphis pseudobrassicae Davis). Purdue University Agri-
cultural Experiment Station Bulletin 185:915–939
Paddock FB (1915) The turnip louse. Texas Agricultural
Experiment Station Bulletin 180, 77 pp
Turnip Root Maggot, Delia floralis
(Fallen) (Diptera: Anthomyiidae)
John L. Capinera
University of Florida, Gainesville, FL, USA
Turnip root maggot is found in northern regions
of Asia, Europe, and North America. Turnip root
maggot greatly resembles seedcorn maggot, Delia
platura (Meigen), and many records probably rep-
resent mixed populations.
Life History
Throughout its range, there is but one generation
per year. Turnip root maggots overwinter as pupae,
and flies from the overwintering population
emerge throughout the summer months. Late July
and early August are peak emergence times.
Eggs of turnip root maggot are white, elongate,
and one side is concave while the opposite side is
convex. Eggs are marked with longitudinal ridges,
and measure about 1.1–1.2  mm long and
0.28–0.38 mm wide. Eggs are laid in July and August,
and are usually deposited in clumps in the soil
around the base of plants. Females normally deposit
about 200 eggs during their adult life of about
40 days. Eggs hatch 8–9 days after being deposited.
Larvae also are whitish in color, undergo three
instars, and attain a length of 9–10  mm before
pupating. Duration of the larval stage is 5–8 weeks.
The anterior larval spiracles have 14–16 lobes, a
character that is useful for distinguishing this
maggot from most related species. Larvae are
found feeding on the host plant from August to
October. At maturity they move in the soil a short
distance from the feeding site and pupate.
The puparium is oval, and bluntly rounded at
each end, and brown in color. The average length is
about 6.5–7.5  mm. Pupae are the overwintering
stage, and therefore are present from August until
the following spring, a period of 8–10 months.
Flies generally resemble cabbage maggot
adults, but are slightly larger, measuring 7–9 mm
long. They also lack the tuft of bristles at the base
of the hind femora that is distinctive in cabbage
flies, and their color tends to be a lighter gray.
Adults live 1–2  months, and usually begin to
deposit eggs when they are about 9–10 days old.
The host range of turnip root maggot is quite
similar to that of cabbage maggot, Delia radicum
(Linneaus), but turnip maggot is more abundant in
northern latitudes and where soils are light. Turnip
maggot is known principally for its damage to
rutabaga and turnip, which explains the common
name. However, it damages most crucifers, includ-
ing weed species. It is generally considered to be a
truly phytophagous insect, like cabbage maggot,
rather than being attracted to stressed or plant
­disease-infected plants, like seedcorn maggot.
Biology of this insect is not well known, and the
natural enemies are particularly poorly studied. It
appears that predators and fungi that are associated
with other Delia spp. also affect turnip root maggot.
Studies in Norway showed that over 40% of turnip
root maggot eggs were consumed by predators in
only 2–3 days. Plots with greater numbers of carabids
and staphylinids (both Coleoptera) had greater egg
mortality, and insecticides interfered with predation.
Damage
Turnip root maggot can be quite damaging. In Can-
ada’s Prairie Provinces, up to 40% of ­commercial
turnips and 80–90% of rutabagas have been made
unsuitable for consumption due to feeding damage
by this insect. Larvae generally confine their feed-
ing to roots, but sometimes work their way up into
 Tussock Moths (Lepidoptera: Lymantriidae)
T 3995

petioles of the lower leaves. They normally scarify
the surface of the root, rarely penetrating very
deeply. For crops where the root is not harvested,
such as cauliflower, the damage is much less, due to
both the indirect nature of the injury and the fact
that ­larvae tend to occur so late in the season that
the plants are fairly mature.
Management
Capinera JL (2001) Handbook of vegetable pests. Academic,
San Diego, 729 pp
Finch S (1989) Ecological considerations in the management
of Delia pest species in vegetable crops. Annu Rev
­Entomol 34:117–137
Miles M (1952) Studies of British anthomyiid flies. III. Imma-
ture stages of Delia cilicrura (Rond.), D. trichodactyla
(Rond.), Erioischia brassicae (Bch.), E. floralis (Fall.) and
Pegohylemyia fugax (Mg.). Bull Entomol Res43:83–90
Miles M (1955) Studies of British anthomyiid flies. VI. The
annual cycle of generations in some anthomyiid root
flies. Bull Entomol Res 46:11–19

Yellow sticky traps can be used to monitor abun-

dance of adults. Flies are more likely to land on Turtle Beetles
horizontal surfaces than vertical surfaces, however,
so water pan traps might be more suitable. Allyl Members of the family Chelonariidae (order
isothiocyanate is an important element in host Coleoptera).
acceptance, functions as an oviposition stimulant,  Beetles
and may be useful in monitoring. Management of
turnip root maggot often depends on use of insec-
ticides, usually applied as a granular formulation
at planting, to protect against larval injury. Tussock Moths (Lepidoptera:
In general, fast maturing varieties seem espe- Lymantriidae)
cially prone to damage. Chinese cabbage, mustard,
and some cauliflower cultivars were especially sus- John B. Heppner
ceptible to injury, whereas kale and radish were Florida State Collection of Arthropods,
quite resistant, and broccoli was intermediate. In an ­Gainesville, FL, USA
evaluation of 22 cauliflower selections, significant
differences in susceptibility to injury were identi- Tussock moths, family Lymantriidae, total 2,490
fied. There was a positive correlation between plant species worldwide; actual fauna likely exceeds
damage and number of eggs deposited by flies. 3,000 species. Most of the fauna is Old World
Weather and soil conditions affect damage
potential. As is the case with seedcorn maggot,
damage is worse in cool, wet years. Also, in the
Prairie Provinces of Canada, damage by turnip
root maggot occurs principally on farms that are
irrigated. In Norway, turnip root maggot is the
principal crucifer pest on light soils, whereas cab-
bage maggot is the major pest on heavy soils.
 Vegetable Pests and their Management

References
Tussock Moths (Lepidoptera: L­ ymantriidae),
Brooks AR (1951) Identification of the root maggots (Dip-
­Figure 117  Example of tussock moths
tera: Anthomyiidae) attacking cruciferous garden crops
in Canada, with notes on biology and control. Can ­(Lymantriidae), Lymantria dispar (Linnaeus) from
­Entomol 83:109–120 Germany.
3996
T Twig Borer
tropical (ca. 2,090 sp.). Two subfamilies are used,
Orgyiinae and Lymantriinae, but this classifica-
tion is uncertain. The family is in the superfamily
Noctuoidea, in the section Cossina, subsection
Bombycina, of the division Ditrysia. Adults small
to very large (16–135 mm wingspan); some with
brachypterous females (some are apterous). Mac-
ulation mostly somber browns and grays, but
some mostly yellow or white, or more colorful; a
few species even with hyaline wings. Adults mostly
nocturnal but some are diurnal or crepuscular.
Larvae are leaf feeders, sometimes gregariously.
Host plants include many different plant families.
Many species are serious defoliators of forest trees
(Fig. 117).
References
Bryk F (1934) Lymantriidae. Lepidopterorum catalogus
62:1–441. W. Junk, The Hague
Bryner R (2000) Lymantriidae – Trägspinner. In: Schmetter-
linge und ihre Lebens räume: Arten – Gefährdung –
Schutz. Schweiz und angrenzenden Gebiete, 3: 529–580,
pl. 24–25. Pro Natura-Schweizerische Bund fuer
Naturschutz, Basel
Ferguson DC (1978) Noctuoidea. Lymantriidae. In: Dominick RB
et al (eds) The moths of America north of Mexico
including Greenland. Fasc. 22.2. E. W. Classey, London,
110 pp, 9 pl
Griveaud P (1977) Insectes Lépidoptéres. Lymantriidae.
Faune Madagascar 43:1–588
Holloway JD (1999) Family Lymantriidae. In: The moths of
Borneo, 5: 1–188, 63 + 12 pl. Malayan Nature Society:
Kuala Lumpur (Malayan Nat J 53)
Seitz A (ed) (1910–34) Familie: Lymantriidae. Die Gross-
Schmetterlinge der Erde, 2: 109–141, pl. 19–22 (1910);
2(suppl.): 95–106, 283–284, pl. 8 (1932–34); 6:
535–564, pl. 72–74 (1927); 10: 291–387, pl. 38–47
(1915–25); 14: 127–205, pl. 20–28 (1926). A. Kernen,
Stuttgart
Twig Borer
An insect that enters the shoot tip of a growing
woody plant, causing the twig to wilt and die.
Twirler Moths (Lepidoptera:
Gelechiidae)
John B. Heppner
Florida State Collection of Arthropods,
­Gainesville, FL, USA
Twirler moths, family Gelechiidae, are a very
large family, with over 4,830 species described,
however, possibly with a fauna exceeding 10,000
species worldwide. Subfamily arrangements
have varied but now include four subfamilies,
plus many tribes: Physoptilinae, Gelechiinae,
Pexicopiinae, and Dichomeridinae. The family
is part of the superfamily Gelechioidea in the
section Tineina, subsection Tineina, of the divi-
sion Ditrysia. Adults small (4–35  mm wing-
span), with head smooth-scaled and labial palpi
recurved; haustellum scaled; maxillary palpi
4-segmented. Hindwings usually with distinc-
tive falcate apical point and with long fringes
(Fig.  118). Maculation varied, but mostly som-
ber colors, but some can be colorful and with
metallic-iridescent markings. Adults mostly
nocturnal but some are diurnal or crepuscular.
Many adults tend to twirl in circles on leaves
when disturbed. Larvae have a range of feeding
habits but most are leaf skeletonizers, using a
Twirler Moths (Lepidoptera: G ­ elechiidae),
­Figure 118  Example of twirler moths
­(Gelechiidae), Filatima albilorella (Zeller) from
Florida, USA.
 Twospotted Spider Mite, Tetranychus urticae Koch (Acari: Tetranychidae)
leaf fold or leaf tie as protection. A large variety
of plants are used as hosts. Some species are
economically important.
References
Clarke JFG (1969) Gelechiidae. In Clarke JFG, Catalogue of the
type specimens of Microlepidoptera in the British Museum
(Natural History) described by Edward ­Meyrick,6:219–537;
7:1–531. British Museum (Natural History), London
Elsner G, Huemer P, Tokár Z (1999) Die Palpenmotten (Lepi-
doptera, Gelechiidae) Mitteleuropas: Bestimmung –
Verbreitung – Flugstandort – Lebensweise der Raupen.
F. Slamka, Bratislava. 208 pp (85 + 28 pl.)
Gaede M (1937) Gelechiidae. Lepidopterorum Catalogus,
79:1–630. W. Junk, The Hague
Hodges RW (1986) Gelechioidea. Gelechiidae (part). In: The
moths of America north of Mexico including Greenland.
Fasc. 7.1: 1–195, 4 pl. (1986); 7.6: 1–339, 5 pl. (1999).
Wedge Entomological Foundation, Washington
Huemer P, Karsholt O (1999) Microlepidoptera of Europe,
vol 3. Gelechiidae I (Gelechiinae: Teleiodini, Gelechiini.
Apollo Books, Stenstrup, 356 pp, 14 pl
Janse AJT (1949–54) Gelechiadae [sic]. In: Janse AJT, The
moths of South Africa, 5: 1–464, 202 pl. Pretoria
Li H-H (2002) The Gelechiidae of China (I) (Lepidoptera: Gele-
chioidea). Nankai University Press: Tianjin, 538 pp (32 pl.)
Piskunov VI (1981) Gelechiidae. In: Identification keys to the
insects of European Russia. 4. (Lepidoptera), 2: 659–748.
Academie Nauk, St Petersburg (in Russian)
Twisted-Wing Parasites
Members of the order Strepsiptera.
 Stylopids
Twospotted Spider Mite,
Tetranychus urticae Koch (Acari:
Tetranychidae)
John L. Capinera
University of Florida, Gainesville, FL, USA
The most widespread and important of the spider
mites is twospotted spider mite, Tetranychus urticae
T 3997
Koch, which is found throughout the world in
temperate and subtropical locations. Though most
damaging in warmer regions, twospotted spider
mite survives temperate climates better than most
other species of spider mites. Also, this species
can  become very troublesome in greenhouses
everywhere.
Life History
With a life cycle of only 8–12 days at 30°C and
about 17 days at 20°C, over 20 generations may
develop annually, though conditions rarely allow
this rate of population cycling. Overwintering
may occur on many hosts in warm-winter cli-
mates, and in cold winter areas forage legumes
and greenhouses often shelter these pests, but
adult twospotted spider mite females also pass
the winter under leaves or other organic debris
in a state of diapause. The development time
of  the immature stages is 4–5  days at 30–32°C,
but is extended to about 16–17  days when the
temperature is 15°C at night and 28°C during
the day.
The eggs are whitish and spherical. They mea-
sure about 0.10–0.15  mm in diameter. Eggs are
often deposited singly on the lower surface of foli-
age, but sometimes on the upper surface, usually
under dense strands of silk. Females oviposit at a
rate of 5–6 eggs per day, for a total of 60–120 eggs.
Duration of the egg stage is about 3 days at 30°C
and 6–7 days at 20°C.
The first instar is called the larva, and is color-
less initially but yellowish or pinkish in color after
feeding. The body is nearly spherical in shape, and
bears three pairs of legs. The terminal portion of
the larval stage is a nonfeeding period called the
nymphochrysalis or protochrysalis. Duration of
the first instar is 1–2  days at 30°C and 2–3  days
at 20°C.
There are two nymphal instars, the proto-
nymph and the deutonymph. These stages are eas-
ily separated from the larva because they bear four
pairs of legs. They tend to be green or red in color.
3998
T Twospotted Spider Mite, Tetranychus urticae Koch (Acari: Tetranychidae)

As in the larval stage, the terminal portion of each

nymphal period is a nonfeeding period called
the deutochrysalis and teliochrysalis, respectively.
Duration of each instar is 1–2  days at 30°C and
about 3 days at 20°C.
Adults are 0.4–0.5  mm long. Males are
slightly smaller than females, and are usually
less abundant than females. Like the nymphs,
adults bear four pairs of relatively long legs.
They also have numerous long hairs on their
legs, and long but sparse hairs on their body.
Females tend to be oval in body shape, males
elongate-oval or diamond-shaped. The actively
feeding female is usually greenish, with dorso-
lateral dark spots. Overwintering females of
twospotted spider mite become orangeish red.
Color is not a very reliable character with tet-
ranychid mites; accurate determination depends
on examination of tarsal characteristics and
Twospotted Spider Mite, Tetranychus urticae Koch
genitalia of males.
(Acari: Tetranychidae), Figure 119  Adult female
Males are attracted to immature females by a
twospotted spider mite, Tetranychus urticae Koch.
sex pheromone, perform extensive mating rituals
and may mate repeatedly. The preoviposition
period of females is 1–2  days. Fertilized females
produce both male and female offspring; unfertil- ­ articularly Scolothrips sexmaculatus (Pergande)
p
ized females produce only males. Duration of the (Thysanoptera: Thripidae). Also, fungi sometimes
adult stage is normally about 30 days except when cause epizootics.
overwintering. The preoviposition period of adults
is less than a day at 30°C, and 1–2  days at 20°C.
Adults disperse by crawling and by wind-borne
dispersal (Fig. 119). Damage
These mites affect a large number of vegetable
crops, though tomato, bean, and cucurbit crops are Twospotted spider mites generally feed on the
affected most often. They also damage cotton, soy- lower leaf surface. They pierce individual cells with
bean, strawberry, tree fruit crops and many orna- their stylets, withdrawing the cell contents.
mental plants. Twospotted spider mite can feed on 18–22 cells/
The natural enemies of spider mites are min, resulting in many dead cells, and often a
numerous and diverse. Among the most impor- speckled appearance. Leaf transpiration is acceler-
tant are predatory mites, particularly Phytoseiulus ated, and affected leaves may dry and drop from
persimilis Athias-Henriot (Acari: Phytoseiidae); the plant. Yellowing and speckling are the most
ladybird beetles, particularly Stethorus spp. common early plant responses to feeding, though
(Coleoptera: Coccinellidae); dusty-wings (Neu- reddening may also occur. Injection of plant
roptera: Coniopterygidae); pirate bugs, particu- growth regulators or interference with growth reg-
larly Orius spp. (Hemiptera: Anthocoridae); some ulators during feeding is also reported. Wilting,
plant bugs (Hemiptera: Miridae); and thrips, tissue death, and leaf deformity and abcission are
 Twospotted Spider Mite, Tetranychus urticae Koch (Acari: Tetranychidae)
characteristics of prolonged and high density
infestations. Disruption of photosynthesis results
in stunting of plant growth and reduced fruit
yields. Mite products such as webbing, eggs, cast
skins, and fecal material also detract from the cos-
metic quality of plants.
Prior to the 1940s spider mites were infre-
quently considered to be serious pests, but since
then they have assumed major pest status in some
crops. Apparently mite problems are induced by
crop management practices, particularly the use
of broad-spectrum insecticides. Also, the suitabil-
ity of crops for mites is greatly enhanced when
mites develop on plants that receive excessive
nitrogen fertilization, grow in a dusty environ-
ment, or are stressed by inadequate moisture and
high temperatures. These environmental factors
can convert plants that might be only poor hosts
into very good hosts, resulting in mite population
increase and crop damage.
Management
Visual examination of foliage for leaf stippling on
the upper surface, and mites and webbing on the
lower surface, is the usual method of sampling.
Older, or lower, leaves are usually examined. Infes-
tations tend to be clumped initially, with clumping
decreasing as the crop matures and females dis-
perse to younger foliage.
Chemical insecticides (acaricides) are com-
monly used in greenhouses to prevent injury by
mites, though natural enemies usually are capa-
ble of maintaining spider mite densities at low
levels on crops grown under field conditions. In
the field, insecticides directed at other pests can
induce mortality among natural enemies of
mites, causing spider mite population increases.
Therefore, considerable effort is now directed at
managing pests without disrupting natural con-
trol of mites, often by use of selective insecti-
cides. Avoidance of early-season applications of
insecticides is also recommended. Certain classes
T 3999
of insecticides, particularly pyrethroids, are
especially disruptive. If chemicals must be
applied for mite suppression, thorough coverage
of the plants is essential. Frequent application of
insecticides has led to many cases of resistance
among spider mites. Resistance has not devel-
oped to oils, but oils are effective mostly against
eggs, and frequent application leads to phytotox-
icity among vegetable crops. Insecticidal soaps
are similarly useful, though eggs are not entirely
susceptible. Neither oil nor soap should be used
at temperatures above 32°C. Sulfur is applied to
some crops, but not to cucurbits, and not if tem-
peratures exceed 32°C.
Cultural practices can have considerable
influence on mite damage. Water stress disrupts
the physiology of the host plant, making it more
suitable for mite survival and population increase.
Dry, dusty conditions also favor mite survival
because blowing dust interferes with the predators
of mites more than it does the mites; the latter are
partially protected beneath their silk webbing.
Thus, overhead sprinkler irrigation may alleviate
mite problems. Excessive nitrogen fertilization of
crops also favors mite population increase. Weeds
and senescent crops can be important sources of
mites, as can winter legume forage crops. Plant
cultivars vary considerably in resistance to mites,
and in some crops this offers excellent opportu-
nity to manage mites whereas in others there
seems to be little inherent resistance.
Biological suppression of mites through sup-
plemental release of predators has been well
developed for greenhouse crops. This approach is
not often implemented for annual crops grown
outdoors, though the successful use of the preda-
tory mite Phytoseilus persimilis Athia-Henriot
(Acari: Phytoseiidae) for twospotted spider mite
suppression in strawberry fields shows that the
approach is applicable if allowed by crop eco-
nomics. This predatory mite is commonly used to
suppress twospotted spider mite in greenhouses.
Effective use of P. persimilis involves maintenance
of a low level of pest mites so that the predators
do not starve, and the distribution of pests (prey)
4000
T Twostriped Grasshopper, Melanoplus bivittatus (Say), (Orthoptera: Acrididae)
uniformly in the greenhouse so that the preda-
tory mites also will become widely distributed.
Supplemental release of predatory mites may be
needed to maintain a favorable ratio of preda-
tors to prey, often between 1:6 and 1:25. The
maintenance of stable predator–prey–host plant
relations is not a simple task, and even seemingly
benign environmental changes such as variation
in light intensity within the greenhouse affect
stability.
 Citrus Pests and their Management
 Small Fruit Pests and their Management
 Potato Pests and their Management
References
Capinera JL (2001) Handbook of vegetable pests. Academic,
San Diego, 729 pp
Carey JR, Bradley JW (1982) Developmental rates, vital
schedules, sex ratios, and life tables for Tetranychus urti­
cae, T. turkestani and T. pacificus (Acarina: Tetranychi-
dae) on cotton. Acarologia 23:333–345
Huffaker CB, van de Vrie M, McMurtry JA (1969) The ecology
of tetranychid mites and their natural control. Annu
Rev Entomol 14:125–174
van de Vrie M, McMurtry JA, Huffaker CB (1972) Biology,
ecology, and pest status, and host-plant relations of
­tetranychids. Hilgardia 41:343–432
Twostriped Grasshopper,
Melanoplus bivittatus (Say),
(Orthoptera: Acrididae)
This grasshopper is widely distributed in northern
North America. In the United States it extends
from the Atlantic to the Pacific Ocean, and is
absent only from the Gulf Coast region. In south-
ern Canada it occurs from Nova Scotia to British
Columbia.
Life History
Over most of its range, twostriped grasshopper
displays one generation annually, with the egg
stage overwintering. In Colorado, eggs begin to
hatch in June, though hatching can occur over a
4–6  week period. Nymphs may be present until
September, but adults appear beginning in July.
Oviposition commences in August and continues
until adults are killed by cold weather. At higher
elevations in British Columbia, a 2-year life cycle
is reported.
The egg is elongate-cylindrical, with the
ends tapering to blunt points. The eggs are olive
in color and measure about 5.0  mm in length
and 1.2 mm in diameter. The reported values of
number of eggs per pod and total fecundity vary
considerably among studies. One study reported
69.7 eggs per pod and a mean total of 129 eggs
per female, whereas another reported 43.3 eggs
per pod and a total of 355 eggs. The number of
pods produced per female ranges from 4 to 15,
with a mean interval between oviposition of
4 days, but this assumes good weather. Eggs are
arranged in columns of four within a frothy
secretion; the egg structure is called an egg pod.
The pods are curved, measure 30–38  mm in
length and 6–7 mm in diameter. They are inserted
into the soil at a depth of 2–5  cm, and topped
with a frothy plug. Favorite oviposition sites
are  along fence rows, ditch banks, and pastures
with compact, undisturbed soil. Pods are often
inserted among the roots of plants, and a soil
moisture content of 10–20% is preferred. The act
of oviposition requires about 2 h. The egg is the
overwintering stage, and typically persists in the
soil for 7–8  months. Embryonic development
begins in the summer and autumn after oviposi-
tion, and is 60–80% complete before embryos
enter diapause for the winter. However, they can
be induced to hatch if exposed to about 5°C for
90 days.
Nymphal development normally requires
30–50 days. Most nymphs display 5–6 instars, but
7 instars occurs occasionally. Nymphal develop-
ment time when fed lettuce or alfalfa and cultured
at 21°C is about 10, 8.5, 10, 11, and 14 days, respec-
tively for, instars 1–5. The young nymphs initially
are dark brown or greenish, but gain a distinct
 Twostriped Grasshopper, Melanoplus bivittatus (Say), (Orthoptera: Acrididae)
dark stripe along the pronotum behind each eye at
the third instar. The wing development is poor
until instar 3, and the developing wings point
downward. At instar 4, the wing orientation is
reversed, with the wings oriented upward, but also
pointing posteriorly. In the fifth instar, the wings
are quite evident and extend out to at least the sec-
ond abdominal segment. The number of antennal
segments is 12–13, 17–18, 19–22, 23–25, and 24–26
for instars 1–5, respectively. Corresponding body
lengths are 5–6.6, 7.4–10.4, 9–14, 15–21, and
20–17  mm. Nymphs are on the soil and seeking
food each morning, but may ascend plants to
escape the heat of the soil by noon. Like the adult
stage, nymphs will perch on elevated roosts at
night, and will sun themselves in the morning
and  in cool weather to attain optimal body
temperature.
This is a fairly large and robust species. Males
measure 23–29 mm in length, females 29–40 mm.
The general body coloration is olive or brownish
green dorsally and yellowish or yellowish green
ventrally. The head and pronotum tend to be
darker, usually olive green. A narrow but distinct
yellow stripe passes from behind each eye along
the pronotum and forewings, extending nearly to
the wing tips. The stripes are often bordered
below with black, especially on the anterior por-
tions of the body. The stripes come together pos-
teriorly in the forewings, forming a “V.” It is this
pair of yellow stripes that is the basis for the com-
mon name of this grasshopper. The forewings are
usually uniform in color except for the stripes,
and the hind wings colorless. The hind femora
are yellow with a dark stripe along the outer face.
The hind tibiae are variable, usually reddish but
also greenish, yellowish, and purplish, and
equipped with black spines. The male cerci are
short, broad, and boot-shaped.
Adults seek crop borders and roadsides for
reproduction. Mated females have a 7- to 14-day
preoviposition period, after which they oviposit
within the roots of grasses and weeds. Duration of
oviposition is about 30  days (range 15–55  days)
(Fig. 120).
T 4001
Twostriped Grasshopper, Melanoplus bivittatus
(Say), (Orthoptera: Acrididae), Figure 120  Adult
female twostriped grasshopper, Melanoplus
­bivittatus (Say), depositing eggs in the soil.
Damage
This species is adaptable, and is found in a variety
of habitats. However, it is most abundant in moist
meadows, dense vegetation along water courses,
and in disturbed, weedy areas. In the Great Plains
region it is abundant in moist tallgrass regions,
but  uncommon in the drier shortgrass prairie.
Twostriped grasshopper feeds on both grasses and
broadleaf plants, but prefers the latter and fares
poorly in habitats lacking broadleaf plants. Plants
in the families Compositae and Cruciferae seem to
be preferred. Among the uncultivated vegetation
consumed is arrowleaved colt’s foot, Petasites sagit­
tatus; burdock, Arctium lappa; dandelion, Tarax­
acum officinale; dog mustard, Eruscastrum gallicum;
flixweed, Descurainia sophia; needleleaf sedge,
Carex eleocharis; leadplant, Amorpha canescens;
oxeye daisy, Chrysanthemum leucanthemum; pep-
perweed, Lepidium densiflorum; plantain, Plantago
major; redtop, Agrostis alba; sand dropseed,
Sporobolus cryptandrus; Canada thistle, Cirsium
arvense; sunflower, Helianthus spp.; wavyleaf this-
tle, Cirsium undulatum; mustard, Brassica spp.; and
others. In North Dakota alfalfa fields, the plants
most often consumed, after alfalfa, were kochia,
Kochia scoparia; wild oat, Avena fatua; awnless
­bromegrass, Bromus inermis; tansymustard,
4002
T Twostriped Grasshopper, Melanoplus bivittatus (Say), (Orthoptera: Acrididae)
­Descurainia sophia; marsh elder, Iva xanthifolia;
and quackgrass, Agropyron repens. On prairie, how-
ever, the plants most often consumed were Ken-
tucky bluegrass, Poa pratensis; leadplant, Amorpha
canescens; and western ragweed, Ambrosia psilos­
tachya. Survival rates and body weights are higher,
and development times shorter, on mixed diets
than on single hosts.
Twostriped grasshopper commonly infests
vegetable and field crops, though most injury is
limited to field margins. Among vegetable crops
injured are beet, cabbage, chicory, corn, lettuce,
onion, potato and likely others. Field crops such as
alfalfa, birdsfoot trefoil, clover, young barley and
oat, timothy, vetch and the immature seedheads of
wheat also are fed upon. Flowers and ornamental
plants are not immune to attack.
The natural enemies of the crop-feeding Mel­
anoplus spp. are quite similar. For information on
natural enemies of twostriped grasshopper, see the
section on natural enemies of migratory grasshop-
per, Melanoplus sanguinipes (Fabricius).
Survival and population increase in grasshop-
pers are favored by hot weather. High numbers
tend to occur after a period of years with abnor-
mally hot and dry weather during the spring and
summer months. This is especially true in north-
ern areas, where it tends to be cooler. Enough pre-
cipitation is required to provide adequate food for
grasshoppers, of course, but protracted periods of
rainfall during egg hatch, especially if accompa-
nied by cool weather, disrupt feeding by young
grasshoppers and induce high mortality. The late
onset of winter can favor grasshopper population
increase because it allows adults additional time to
produce eggs.
Twostriped grasshopper consumes the leaves
of numerous plants. Damage is greatest in areas
adjacent to weeds, and along fence rows, irriga-
tion ditches, roadsides, and fallow fields. Damage
is exacerbated by drought, which apparently
increases nymphal survival rates and decreases
the amount of weed vegetation available to the
grasshoppers. Although the grasshoppers will
feed at night if it is sufficiently warm, where
nights are cool these grasshoppers tend to perch
on elevated objects at night. This behavior allows
them to be warmed by the light from the setting
and rising sun, maximizing their period of activ-
ity. This also results in nibbling on the resting
substrate by the grasshoppers; these grasshop-
pers will feed on the bark of bushes and young
trees, and even damage shingles on buildings and
eat holes in vinyl window screens while perching.
The nymphs and adults are fairly dispersive,
walking tens or even hundreds of meters in the
search for food. At high densities they show pro-
pensity to swarm, which is expressed by band
formation in the nymphal stage and flight by
adults. The temperature threshold for flight is
30–32°C. Ascending to heights of 200–500  m,
and flying with the wind, swarming adults can
disperse long distances.
Management
Grasshopper populations are usually assessed by
visual observation. A sweepnet is a useful tool to
aid in collection, and its use a prerequisite to iden-
tification of the species complex. It is important
to determine if grasshoppers collected from non-
crop areas are crop-feeding species because there
are many nonpest grasshoppers that restrict their
feeding to grasses or weeds. It is advisable to
monitor nearby uncultivated land, particularly
weedy areas, in addition to crop plants, due to the
tendency of the pest species to invade crops later
in the season.
Liquid formulations of insecticides are com-
monly applied to foliage to protect against dam-
age. Because grasshoppers rarely develop in crops,
but instead invade from weedy areas, it is often
the edges of crop fields that are most injured.
Therefore, application of insecticide to the bor-
ders of crop fields is often adequate to protect an
entire field. It is even better to apply insecticides
to the developing grasshopper populations in
weedy areas before they move to crops. This not
only minimizes damage to crop plants, but often
 Twostriped Grasshopper, Melanoplus bivittatus (Say), (Orthoptera: Acrididae)
results in younger grasshoppers being targeted
for elimination. Younger grasshoppers are more
susceptible to insecticides, with large nymphs and
adults sometimes difficult to kill.
Application of insecticide-treated bait is an
effective alternative to foliar treatments for Mel­
anoplus spp. because these grasshoppers spend
considerable time on the soil where they come
into contact with baits. Bait formulations are
bulky and more difficult to apply than liquid
products, so they are less often used, but have the
advantage of limiting exposure of crops to insec-
ticide residue and of minimizing mortality of
beneficial insects such as predators and parasi-
toids due to insecticide exposure. Also, the total
amount of insecticide active ingredient necessary
to obtain control is usually considerably less when
applied by bait because the grasshoppers actively
seek out and ingest the toxin. Finally, for relatively
expensive products that must be ingested to be
effective, such as microbial insecticides, baits are
the most effective delivery system.
The attractant used most commonly for
grasshopper bait is flaky wheat bran, though
other products such as rolled oats are sometimes
suggested. No additives, other than insecticide
(usually 5% active ingredient), are necessary
because the wheat bran is quite attractive to Mel­
anoplus grasshoppers. Other additives such as
sawdust, water, vegetable or mineral oil, molas-
ses, amyl acetate, salt, or sugar have been sug-
gested, but provide little or no additional benefit
over dry bran. The bait should be broadcast
widely to maximize the likelihood of grasshop-
per contact, and should be applied while grass-
hoppers are in the late instars because adults
ingest less bait.
Elimination of weeds within, and adjacent to,
crops is the most important cultural practice, and
can have material benefit in preventing damage to
crop borders. However, during periods of weather
when grasshoppers become numerous they may
move long distances and invade crops.
Tillage is an effective practice for destruction
of eggs. Deep tillage and burial are required, ­shallow
T 4003
tillage having little effect. All the crop-feeding Mel­
anoplus species deposit some eggs in crop fields,
especially during periods of abundance, but it is
fence row, irrigation ditch, field edge, and roadside
areas that tend to be the favorite oviposition sites, so
tillage is not entirely satisfactory unless other steps
are taken to eliminate grasshopper egg pods from
these areas that cannot be tilled. Though providing
suppressive effects, deep tillage is not consistent
with the soil and water management practices in
many areas, so may not be a good option.
Row covers, netting, and similar physical bar-
riers can provide protection against grasshoppers.
This approach obviously is limited to small plant-
ings, and can interfere with pollination. Also,
grasshoppers are capable of chewing through all
except metal screening, so this approach does not
guarantee complete protection.
The opportunities for biological control are
limited. Historically, poultry were found to con-
sume large numbers of grasshoppers and could
provide considerable relief if the grasshopper-
infested garden was small or moderate in size and
the birds were plentiful. This remains a viable
option for some people, and turkeys are usually
considered most suitable among poultry. The birds
may also inflict some direct damage to plants,
however, so introduction of poultry is probably
most viable when grasshoppers are plentiful and
threatening.
The microsporidian pathogen Nosema locus­
tae is well studied as a microbial control agent of
Melanoplus spp. and is available commercially. It is
fairly stable, and easily disseminated to grasshop-
pers on bait. However, its usefulness is severely
limited by the long period of time that is required
to induce mortality and reduction in feeding and
fecundity. Also, the level of mortality induced by
consumption of Nosema is quite low, often imper-
ceptible. It is best used over very large areas, not
just on individual farms, and should be applied at
least one year in advance of the development of
potentially damaging populations.
Fungi have also been investigated for grass-
hopper suppression. A grasshopper strain of
4004
T Two-Spotted Stink Bug, Perillus bioculatus (Fabricius) (Hemiptera: Pentatomidae, Asopinae)
­ eauveria bassiana has been effective in some trials,
B believed to have originated somewhere from the
and Metarhizium anisopliae var. acridum has
worked well for grasshopper and locust suppression
in Africa and Australia, so it may prove useful for
Melanoplus spp. Behavioral thermoregulation by
grasshoppers, wherein they bask in the sun and
raise their body temperatures, is potentially a limit-
ing factor for use of fungi. Basking grasshoppers
easily attain temperatures in excess of 35°C; such
high temperatures decrease or even prevent disease
development in infected grasshoppers. Inconsistent
quality control in production of fungi also limits
use of these organisms for grasshopper control.
 Grasshopper Pests in North America
 Grasshoppers and Locusts as Agricultural Pests
 Grasshoppers, Katydids and Crickets
(Orthoptera)
References
Capinera JL, Scott RD, Walker TJ (2004) Field guide to the
grasshoppers, katydids, and crickets of the United States.
Cornell University Press, Ithaca, NY, 249 pp
Church NS, Salt RW (1952) Some effects of temperature
on  development and diapause in eggs of Malanoplus
bivittatus (Say) (Orthoptera: Acrididae). Can J Zool
30:173–184
Parker JR (1939) Grasshoppers and their control. USDA
Farmers’ Bulletin 1828. 37 pp
Pfadt RE (2002) Field guide to common western grasshop-
pers. Wyoming Agricultural Experiment Station Bulle-
tin 912. 288 pp
Smith DS (1966) Fecundity and oviposition in the grasshop-
pers Melanoplus sanguinipes (F.) and Melanoplus bivit­
tatus (Say). Can Entomol 98:617–621
Two-Spotted Stink Bug, Perillus
bioculatus (Fabricius) (Hemiptera:
Pentatomidae, Asopinae)
Patrick De Clercq
Ghent University, Ghent, Belgium
The two-spotted stink bug or double-eyed soldier
bug, Perillus bioculatus, is a predatory bug belong-
ing to the pentatomid subfamily Asopinae. It is
southeastern Rocky Mountains to the Plains
region and to have followed the eastward migra-
tion of the Colorado potato beetle, which appears
to be its primary prey, at least in agricultural set-
tings. The insect is presently found from Mexico
into Canada.
Like those of other asopines, adults of Perillus
bioculatus are broadly oval and more or less shield-
shaped. Adult males are 8.5–10 mm long and the
females are 10.5–11.5 mm long. Basically, there are
three color forms: in the white form, the back-
ground is white with black and brown markings;
in the yellow form, there are less pale areas, which
are yellow rather than white, and all markings are
black; in the red form, the background is red, and
markings are black. The adults (Fig.  121) may
gradually change from white or yellow to red, but
not vice versa. The adults live for 1–2 months and
are capable of laying 100–300 eggs. The bug has
two to three generations per year and overwinters
as an adult from September to October to April to
May; adults usually hibernate in litter, but have
also been found to enter buildings.
The eggs are blackish and barrel-shaped
to somewhat elongate; the operculum is encircled
by a row of about 15 micropylar processes, which
are much smaller than in the spined soldier
bug, Podisus maculiventris. The egg is on average
1.2 mm long and is 0.9 mm at its widest diameter.
The eggs are laid in clutches consisting of 10–25
eggs, often arranged in a double row. There is no
embryonic development below 15°C. At temper-
atures between 20°C and 25°C, eggs hatch within
5–8 days.
The nymphs are round to oval in shape. There
are five nymphal instars. The body length of the
five instars averages 1.5, 3, 4–5, 6–7, and 7–9 mm,
respectively. First and second instars have a black
head and thorax and a tomato red abdomen with
dark patches. In third and fourth instars, the red
background color may vary from tomato red to
orange red or reddish yellow; the black color of
the thorax often shows a greenish luster. In the
fifth instar, there are two distinct forms; the dark
 Two-Spotted Stink Bug, Perillus bioculatus (Fabricius) (Hemiptera: Pentatomidae, Asopinae)
on. The nymphs and adults have a thickened
­rostrum or beak which they use to kill their prey
Two-Spotted Stink Bug, Perillus bioculatus
­(Fabricius) (Hemiptera: Pentatomidae, Asopinae),
Figure 121  Adult of two-spotted stink bug, Perillus
bioculatus.
form is greenish black and red, whereas in the
pale form, the thorax and abdomen are mainly
white to yellowish with dark markings. In the
fifth instar, distinct wing pads are developed.
During the last three instars, the red color may
gradually change to yellow and white; on the
other hand, nymphs with a yellowish background
color may also become red. The carotinoid pig-
ment responsible for the red coloration in the
nymphs and the adults is believed to originate
from their food. At high temperatures, the red
pigment of the nymphs is quickly oxidized, yield-
ing paler individuals.
The first instars hardly move about and form
close groups. The gregariousness of the nymphs is
more pronounced than in Podisus maculiventris,
and even in later instars, the nymphs tend to form
clusters, especially when they are preparing for the
next molt and when temperatures are low. The first
instars usually do not feed on prey and only require
moisture, mainly in the form of plant juices. The
nymphs start to attack prey from the second instar
T 4005
and to suck up the liquefied prey tissues. Smaller
nymphs in particular are often observed to attack
prey collectively; on the other hand, gregarious-
ness can also enhance the development of smaller
nymphs by their opportunistic feeding on prey
killed by larger, conspecific nymphs. Like other
asopines, all predatory stages regularly feed on
plant sap. Development of the nymphal stage
requires about 3 weeks at 20–25°C, partly depend-
ing on food availability and quality.
Perillus bioculatus appears to be more of a
specialist pentatomid predator compared to the
spined soldier bug, Podisus maculiventris. In the
field, the predator is usually found in association
with the eggs and larvae of coleopterans, mainly
from the Chrysomelidae family. It has been
reported to feed on other insects, including the
larvae of several lepidopterans. The bug appears
to be, however, a rather timid predator with a dis-
like for highly mobile or aggressive prey. The two-
spotted stink bug is best known for its predation
on the Colorado potato beetle, Leptinotarsa
decemlineata. The predator attacks all life stages
of the beetle, but some scientists found that it has
a preference for the eggs. Interestingly, the bugs
usually suck out every egg in a mass, unlike some
of the pest’s predators with chewing mouthparts.
It has been estimated that Perillus bioculatus can
consume over 300 eggs during its nymphal period.
This suggests a great potential for eliminating
Colorado potato beetle populations provided that
the pentatomid is present early enough in the sea-
son. Because natural populations of the predator
in potato fields are usually too low early in the
season, augmentative releases of laboratory-
reared individuals may help in suppressing out-
breaks of the pest in early spring. However, some
workers have questioned the predator’s dispersal
and predation capacities, particularly under cool
climates. Nonetheless, in small scale field plots,
significant reductions of high density populations
of Colorado potato beetle larvae have been
achieved by releasing one to three second- or
4006
T Tympanum
third-instars per plant. Like the spined soldier
bug, Perillus bioculatus has been introduced in
different parts of Europe for biological control of
the Colorado potato beetle, but none of these
introductions were successful. However, there are
reports of established populations in the European
part of Turkey since 2003, probably as a result of
an accidental introduction.
High numbers of predators needed for
­augmentative field releases necessitate an econom-
ically viable mass production. The two-­spotted
stink bug can be reared on larvae of several noctu-
ids (including Trichoplusia and Spodoptera spp.), a
method that is cheaper than rearing it on the Colo-
rado potato beetle, because the noctuids are easily
mass-reared on artificial diets. The availability of
an artificial diet for the predator itself may further
reduce costs of mass propagation. Artificial diets
have been developed that can support consecutive
generations of the predator, but development and
survival rates are reduced and fecundity is only one
tenth of that raised on live prey.
 Stink Bugs (Hemiptera: Pentatomidae)
Emphasizing Economic Importance
 Predatory Stink Bugs (Hemiptera:
Pentatomidae, Asopinae)
 Bugs (Hemiptera)
References
De Clercq P (2000) Predaceous stinkbugs (Pentatomidae:
Asopinae). In: Schaefer CW, Panizzi AR (eds) Het-
eroptera of economic importance. CRC, Boca Raton,
737–789 pp
Hough-Goldstein JA (1998) Use of predatory pentatomids in
integrated management of the Colorado potato beetle
(Coleoptera: Chrysomelidae). In: Coll M, Ruberson JR
(eds) Predatory Heteroptera: their ecology and use in
biological control. Proceedings, Thomas Say Publica-
tions in Entomology. Entomological Society of America,
Lanham, 209–223 pp
Knight HH (1923) Studies on the life history and biology of
Perillus bioculatus Fabricius, including observations on
the nature of the color pattern. In: 19th Report, State
Entomologist of Minnesota: 50–96
Rojas MG, Morales-Ramos JA, King EG (2000) Two meridic
diets for Perillus bioculatus (Heteroptera: Pentatomidae),
a predator of Leptinotarsa decemlineata (Coleoptera:
Chrysomelidae). Biol Control 17:92–99
Tamaki G, Butt BA (1978) Impact of Perillus bioculatus on the
Colorado potato beetle and plant damage. USDA Tech-
nical Bulletin 1581
Tympanum
A membrane-covered cavity on the thorax, abdo-
men, leg or other part of the body that functions
like an ear to perceive sound. These chordotonal
organs are optimized to perceive high frequency
sound (Fig. 122).
Typhus
There are several types of typhus, all of which are
associated with arthropods. The most common
are epidemic and endemic typhus. Epidemic typhus
(also known as Brill disease) is associated with
poor hygiene, and often is associated with cold
temperatures. It is spread by lice. Historically, it is
associated with periods of warfare and human
disaster. Endemic typhus (also known as murine
typhus) is associated with rat fleas and rat feces. It
is most common during the warm weather when
rats and fleas are most abundant. These forms of
typhus are caused by rickettsia, either Rickettsia
prowazekii (epidemic tphus) or Rickettsia typhi
(endemic typhus).
Symptoms include high fever, severe head-
ache, nausea and vomiting, abdominal pain and a
transient rash. It is a severe illness, and may result
in death if it is not treated, particually in the case
of epidemic typhus. Symptoms occur within
14  days of exposure, and the disease is treated
with antibiotics. Sanitation and avoidance of flea-
infested rats and rat feces is recommended.
Other forms of typhus include tick typhus
and scrub typhus. Tick typhus, transmitted by
ticks, is a form of spotted fever and is found in
Africa and the Indian subcontinent. Scrub typhus
is transmitted by mites, and is found in Southeast
Asia and the Pacific islands. Avoidance of wild
 Type Specimen
T 4007

Mesothoracic wing

Mesotergum Mesothoracic wing

1st abdominal tergum

Conjuctiva
Metatergum
Protergum
Metapleural wing process
Metapleural suture

Tympanum
1st abdominal spiracle
Mesopleural wing process
Mesothoracic spiracle Metathoracic spiracle
Mesepisternum
Metathoracic leg process
Mesopleural suture
Mesepimeron Metepisternum

Mesothoracic leg process

Coxa of mesothoracic leg

Tympanum, Figure 122  Head and thorax of a grasshopper (Orthoptera).

a­ nimals and animal habitats is recommended for Type Specimen

avoidance of these diseases.
 Mites The original specimen (“type”) from which a new
 Ticks species description is created. The holotype.
 History and Insects
 Lice
 Fleas