Wheeler 2016

Biological Control of the Invasive Weed Schinus terebinthifolia
(Brazilian Peppertree): A Review of the Project with an Update

on the Proposed Agents
Author(s): Gregory S. Wheeler, Fernando Mc Kay, Marcelo D. Vitorino,
Veronica Manrique , Rodrigo Diaz , and William A. Overholt
Source: Southeastern Naturalist, 15(sp8):15-34.
Published By: Eagle Hill Institute
DOI: http://dx.doi.org/10.1656/058.015.sp802
URL: http://www.bioone.org/doi/full/10.1656/058.015.sp802
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Everglades Invasive Species
2016 Southeastern Naturalist 15(Special Issue 8):15–34
Biological Control of the Invasive Weed Schinus

terebinthifolia (Brazilian Peppertree): A Review of the
Project with an Update on the Proposed Agents
Gregory S. Wheeler1,*, Fernando Mc Kay2, Marcelo D. Vitorino3,
Veronica Manrique4, 5, Rodrigo Diaz4, 5, and William A. Overholt4
Abstract - Schinus terebinthifolia (Brazilian Peppertree) is a South American plant that has
become invasive in many countries around the world. It was introduced into the US about
100 years ago as an ornamental. Escaping cultivation, it now occurs in Alabama, Florida,
Georgia, Texas, California, and Hawai’i. This species is one of the most invasive weeds
threatening agriculture and natural areas in the Southeast. Efforts to manage Brazilian Pep-
pertree populations with biological controls began in Hawai’i in the 1950s and resulted in
the release of 3 insect species. However, the control agents have had minimal impact, and
the weed continues to be a difficult problem. More recently, our international team of col-
laborators has discovered and tested numerous new species of potential biological control
agents. These species attack different plant tissues and include defoliators, sap-suckers,
stem borers, and leaf- and stem-gall formers. Despite difficulty finding an agent sufficiently
specific for field release in Florida, we have narrowed the field to 2 promising species, the
thrips Pseudophilothrips ichini (Hood) and the foliage-gall former Calophya latiforceps
Burckhardt. Results of no-choice and choice trials conducted overseas and in quarantine
indicate that both species will safely contribute to the control of this invasive weed. Her-
bivorous feeding by immature and adult individuals of both herbivore species stunt growth,
distort leaves, and should reduce reproductive output of Brazilian Peppertree.
Introduction
Schinus terebinthifolia Raddi (Brazilian Peppertree) (Anacardiaceae), native to
South America, is one of the most aggressive and widespread invasive species in
Florida and Hawai’i (Ewel 1986, Rodgers et al. 2014). Also known as Christmas
Berry in Hawai’i, this species constitutes a threat to natural areas, agriculture, and
cattle production (Ewel 1986, Morton 1978, Yoshioka and Markin 1991). Brazil-
ian Peppertree has successfully colonized most of the Florida peninsula, covering
more than 280,000 ha (700,000 acres) with thick monospecific stands that eliminate
understory-plant growth (Schmitz et al. 1997). In the Florida Everglades ecosys-
tem, Brazilian Peppertree is the most widely distributed and abundant invasive
1
Invasive Plant Research Laboratory, USDA-ARS, 3225 College Avenue, Ft. Lauderdale,
FL 33314. 2Fuedei, formerly USDA/ARS/SABCL, Buenos Aires, Argentina. 3Programa de
Pós-graduação, em Engenharia Florestal PPGEF, Universidade Regional de 10 Blumenau,
Blumenau, SC, Brazil 89012-900. 4Biological Control Research and Containment Labora-
tory, University of Florida, 2199 South Rock Road, Ft. Pierce, FL 34945. 5Department of
Entomology, Louisiana State University, Baton Rouge, LA 70803. *Corresponding author
- greg.wheeler@ars.usda.gov.
Manuscript Editor: Brett Serviss
15
2016 Southeastern Naturalist Vol. 15, Special Issue 8
G.S. Wheeler, F. Mc Kay, M.D. Vitorino, V. Manrique, R. Diaz, and W.A. Overholt
weed, occupying 30,379 ha—an area greater than the combined infestations of the
next 3 most-problematic plant species (Rodgers et al. 2014). In Hawai’i, surveys
conducted in the early 1990s estimated that 50,000 ha were moderately to heavily
infested, with another 200,000 ha infested with occasional to scattered plants (Yo-
shioka and Markin 1991). In its naturalized range, Brazilian Peppertree decreases
biodiversity in coastal and upland habitats (Gann et al. 2015, Mytinger and Wil-
liamson 1987). The South Florida Water Mangement District spent an estimated
$1.7 million to control Brazilian Peppertree in 2011, and the Florida Department of
Environmental Protection spent over $10.5 million for herbicide treatment between
1998 and 2006 (G. Jubinsky, Florida Fish and Wildlife Conservation Commission,
Tallahassee, FL, pers. comm.; Rodgers et al. 2012). The US Fish and Wildlife
Service (1998) identified Brazilian Peppertree as one of the most significant non-
indigenous species currently impacting federally listed threatened and endangered
native plants throughout the Hawaiian Islands. Brazilian Peppertree also disrupts
traditional Hawaiian archeological settlements because its roots erode protected
historic features, especially unfortified rock walls (Leary and Gross 2013). Brazil-
ian Peppertree produces allelopathic compounds that suppress the growth of other
plant species (Gogue et al. 1974, Morgan and Overholt 2005). Volatiles released by
the leaves, flowers, and fruits of this species cause allergic reactions and respiratory
illness in sensitive people (Morton 1978, Stahl et al. 1983), and ingestion of the
leaves and fruits can have narcotic and toxic effects in grazing animals and birds
(Campello and Marsaioli 1974, Morton 1978). Chemical- and mechanical-control
measures have been used with some short-term success; however, permanent cost-
effective maintenance programs are required to prevent regrowth, particularly in
remote wildlands where other control measures are logistically difficult (Doren
and Jones 1997). Classical biological control may provide an ecologically sound,
cost-effective, and sustainable component of management strategies to protect na-
tive plants in these habitats. Our purpose here is to briefly summarize the history of
biological control of Brazilian Peppertree and the current status of our project.
Surveys of Native Range

One of the initial steps in a biological control project is to delimit the native
range of the target weed in order to search for agents in a diverse assemblage of
habitats. Brazilian Peppertree is a species that covers a latitudinally broad native
range, extending from Natal, Brazil (5.8°S) to near Maldonado, Uruguay (34.8°S;
Mukherjee et al. 2012, JBRJ 2015, Tropicos.org 2015, G.S. Wheeler, unpubl. data).
The northern portion of this distribution remains within about 100 km of the Atlan-
tic coast until Minas Gerais and Sao Paulo states, Brazil where it extends west into
eastern Paraguay and adjacent northeastern Argentina (Fig. 1).
Initial surveys to search for potential biological control agents for Brazilian
Peppertree were conducted in northern Argentina and Brazil in the 1950s and early
1960s (Davis and Krauss 1962; Krauss 1962, 1963). The early surveys explored
mostly the Brazilian states Minas Gerais, Rio de Janeiro, Sao Paulo, and Paraná,
where numerous species of defoliating Lepidoptera, Coleoptera, and Hymenoptera
16
were found (Krauss 1962). Gall-forming Lepidoptera, Diptera, and seed-feeding

Bruchidae were also reported (Krauss 1962). Bennett et al. (1990) and Bennett and
Habeck (1991) conducted literature reviews and field surveys in the late 1980s.
From surveys near Curitiba in Paraná state and review of Brazilian catalogs (Silva
Figure 1. Map of area that encompasses the distribution of Brazilian Peppertree in its native
range in South America. Black dots designate Brazilian Peppertree sites surveyed by the
authors during biological control surveys (2005–2014).
17
et al. 1968), these authors estimated that 150 herbivore species may be associated
with Brazilian Peppertree in Brazil.
Beginning in 2005, we conducted South American surveys; the most recent of
these occurred during August 2014. We intensively studied Brazilian Peppertree in
the northeastern provinces of Argentina and details regarding surveys conducted
there are provided in Mc Kay et al. (2009). We undertook 20 surveys during this
9-y period to describe the geographic range of Brazilian Peppertree in Brazil, cata-
log the herbivores associated with the plant, and import under quarantine and test
promising agents for biological control. Surveys established over 900 sites (Fig. 1)
were typically 15-d long, and included 2–3 collectors. We collected insects by vi-
sual inspection, dissection of plant tissues, and by shaking the plants and recovering
specimens that fell to a sheet placed below. To determine the host range of potential
agents in their native range, we also searched adjacent plants at each site, especially
members of the Anacardiaceae. At the same time, the genetic variation of Brazil-
ian Peppertree was mapped in its native range by DNA analysis of collected leaf
samples (Mukherjee et al. 2012, Williams et al. 2005).
Potential agents discovered

The earliest surveys detected 30 species of potential agents (Krauss 1963).
These discoveries were followed in the late 1980s by an additional 31 species from
the Brazilian catalogs (Bennett and Habeck 1991, Bennett et al. 1990, Silva et al.
1968). Possibly the most detailed list of Brazilian Peppertree herbivores found in
South America was for Argentina (Mc Kay et al. 2009). This list included 36 phy-
tophagous insect species and 1 fungus (Mc Kay et al. 2009). A similar list is being
developed from surveys conducted in Brazil that included more than 120 herbivo-
rous species (G.S. Wheeler, unpubl. data). This herbivore list is beyond the scope
of this paper but comprises 70 species of Lepidoptera, 27 species of Coleoptera,
10 species of Hemiptera, 3 species of Thysanoptera, 2 species of Diptera, and 11
pathogenic fungi (de Macedo et al. 2013; G.S. Wheeler, unpubl. data). Of these, a
subset of more than 40 species may be suitable agents, and knowledge of their host
range could benefit decisions for their use as a biological control agent.
During our onsite inspections of Brazilian Peppertree in South America, we
considered many potential agents unacceptable and we eliminated them from fur-
ther evaluation under quarantine conditions. These rejected taxa included species
that were too broad in their host range (e.g., Apocnemidophorus blandus (Pascoe)
[Coleoptera: Curculionidae]), might pose an unacceptable risk to human and animal
health (e.g., Eacles imperialis (Drury), Lonomia achelous (Cramer), [Lepidoptera:
Saturniidae], Acharia [= Sabine] spp. [Lepidoptera: Limacodidae]), or were al-
ready present in the US (e.g., Protambulyx strigilis L. [Lepidoptera: Saturniidae],
Megastigmus transvaalensis (Hussey) [Hymenoptera: Torymidae]). Several species
of beetles (e.g., Lexiphanes guerini (Perbosc) [Chrysomelidae: Cryptocephaline])
found feeding on Brazilian Peppertree leaves were known in the larval stages to
be ant inquilines, whereas others were from genera of the Eumolpinae that need
extensive taxonomic revision (A. Konstantinov, USDA/ARS/SEL, Beltsville, MD,
pers. comm.).
18
Whether all the species associated with Brazilian Peppertree in its native range
are documented is uncertain and additional surveys may reveal new herbivore
species. To estimate whether more species might be discovered with increased
sampling effort, we calculated a species-accumulation curve by plotting the cu-
mulative number of new species discovered against each additional survey (Bell
et al. 2014, Heard and Pettit 2005). In this analysis, if an asymptote is reached in
the accumulation curve it may be assumed that most of the herbivore diversity has
been discovered and additional surveys are not justified. Our species accumulation
curve indicated that more than 120 species have been discovered and additional
new species have been added at a steady rate through the last survey in August 2014
(Fig. 2). These results suggest that additional herbivore species will be discovered
during future surveys. A second, lower line on the graph plots the number of new
species that might have sufficient specificity and should be tested in quarantine.
This line begins near zero because the first surveys discovered mostly previously
reported insects (Fig. 2). Consequently, we doubt if all the species associated with
Brazilian Peppertree in South America have been discovered and surveys to search
for additional agents are continuing. We will publish the full list of herbivores when
our analysis indicates that further survey effort would likely produce few new her-
bivore species.
Figure 2. Species-accumulation curves showing discovery of new herbivore species on

Brazilian Peppertree during surveys conducted in Brazil from 2005 to 2014. Two lines are
plotted showing, respectively all species and a subset of those with potential to serve as
biological control agents.
19
Potential agents tested

One of the most important steps in the development of a biological control agent
is conducting research to predict its host range. An initial step in the testing of host
range is to expose all feeding stages of the candidate agent to plants considered
to be the closest relatives of the target weed, especially those that grow sympatri-
cally. Non-target species in the same family that co-occur with Brazilian Peppertree
include Rhus copallina L. (Winged Sumac), R. sandwicensis A. Gray (Hawaiian
Sumac, Hawaiian endemic), Toxicodendron radicans (L.) Kuntze (Poison Ivy),
and T. vernix (L.) Kuntze (Poison Sumac) (USDA/NRCS 2016). The species most
closely related to the target plant are considered most vulnerable to damage by
candidate biological control agents. If the candidate insect does not feed and com-
plete development on these closest relatives, then more distantly related species are
tested (Wapshere 1989).
The myriad testing strategies available have been reviewed elsewhere (Schaffner
2001, Van Klinken 2000). The host range of a biological control agent is determined
by a series of tests beginning with the most conservative—a no-choice starvation
test. In this test, the candidate agent is presented with test plants in optimum con-
dition and stage-appropriate for the herbivore to feed, complete development, and
reproduce. These tests determine the physiological host range of a potential agent
and are frequently criticized for being too conservative because their results may
be used to exclude potentially useful insects (Cullen 1990, Schaffner 2001). To
complement the lab results, host range in the field can be obtained by surveying
close relatives growing sympatrically with the target in the native range (Goolsby
et al. 2006). For Brazilian Peppertree biological control, potential agents that dem-
onstrated a narrow host range following preliminary observations in South America
were imported into the US for quarantine testing.
Agents tested and rejected

Following quarantine testing of a prospective agent in the US, researchers
submit a formal petition to the US Department of Agriculture Animal and Plant
Health Inspection Service (USDA/APHIS). This petition summarizes background
information describing the agent, the testing protocol, results, and interpretation
of the results by the researcher. The petition is presented for review to a technical
advisory group (TAG) composed of representatives from various federal and state
government agencies and managers of public lands. The ultimate goal of the TAG
review is to ensure that only safe biological control agents are introduced (Cofran-
cesco and Shearer 2004). Petitions approved by TAG are then passed to USDA/
APHIS for final decision (Van Driesche et al. 2008). For the recent (2005–2014)
Brazilian Peppertree project, we evaluated a total of 13 herbivore species but none
have been approved for release (Table 1). For most species, we chose to withhold
petitions from TAG review due to a lack of confidence in the agent’s safety toward
native or agricultural plants. These quarantine tests included mostly Lepidopteran
defoliators, stem borers, and leaf miners; 2 species of Coleoptera; and 1 species of
Hymenoptera.
20
Pergidae (sawflies). The first published account of a Brazilian Peppertree insect

rejected for biological control following testing was for the sawfly Heteroperreyia
hubrichi Malaise (Hymenoptera: Pergidae) (Hight et al. 2003). Host-range studies
conducted in Brazil by Vitorino et al. (2000) indicated that the sawfly would only
develop on Brazilian Peppertree and Anacardium occidentale L. (Cashew). Ship-
ments of the insect were received in Hawai’i in 1999. Subsequent quarantine testing
indicated that this species could oviposit and complete development, though poorly,
on the only Hawaiian native species of Anacardiaceae, Hawaiian Sumac. Even
though only 1% of the neonates survived on this non-target species in no-choice
starvation tests, subsequent testing in Hawai’i was discontinued (Table 1; Hight et
al. 2003). In Florida, this species was tested in quarantine against 36 plant species,
and the results confirmed those from Brazil in that neonates completed development
only on Brazilian Peppertree and Cashew. Oviposition was restricted to the target
weed and a petition submitted to TAG was approved (Medal et al. 1999). However,
like other members of the Pergidae sawfly family, this species was known to pro-
duce cytotoxic peptides (Oelrichs et al. 1999). Possibly due to concerns about its
toxicity in herbivorous vertebrates such as cattle, this species was never released in
Florida (cf. Dittrich et al. 2004).
Gracillariidae (leaf blotchers). Examination of leaf blotchers that mine leaves
of Brazilian Peppertree in its native range revealed a complex of at least 4 spe-
cies—Leurocephala schinusae Davis and Mc Kay, Eucosmophora schinusivora
Davis and Wheeler, Caloptilia schinusifolia Davis and Wheeler, and Marmara sp.
Table 1. Insects species that were evaluated and rejected following host testing for biological control
of Brazillian Peppertree.
Genus Species Order Family Source

Apocnemidophorus pipitzi Coleoptera Curculionidae TAG decisionA
Omolabus piceus Coleoptera Curculionidae Wheeler et al. (2013)
Plectrophoroides lutra Coleoptera Curculionidae Wheeler et al. (2011)
Paectes longiformis Lepidoptera Euteliidae Manrique et al. (2014a)
Crasimorpha infuscata Lepidoptera Gelechiidae F. Mc Kay, unpubl. data
Hymenomima memor Lepidoptera Geometridae E. Broggi and G.S. Wheeler,
unpubl. data
Oospila pallidaria Lepidoptera Geometridae M. Chaw ner and G.S.
Wheeler, unpubl. data
Oxydia vesulia Lepidoptera Geometridae Fung and Wheeler (2016)
Prochoerodes onustaria Lepidoptera Geometridae E. Jones and G.S. Wheeler,
unpubl. data
Eucosmophora schinusivora Lepidoptera Gracillariidae Rendon et al. (2012)
Leurocephala schinusae Lepidoptera Gracillariidae Mc Kay et al. (2012)
Tolype medialis Lepidoptera Lasiocampidae G.S. Wheeler, unpubl. data
Nystalea ebalea Lepidoptera Notodontidae Wheeler et al. (2014)
Tecmessa elegans Lepidoptera Notodontidae Oleiro et al. (2011)
Episimus unguiculus Lepidoptera Tortricidae TAG decision A
Heteroperreyia hubrichi Hymenoptera Pergidae Hight et al. (2003), TAG
decisionA
A
Technical Advisory Group web site (http://www.aphis.usda.gov/).
21
(Lepidoptera: Gracillariidae) (Davis et al. 2011). Field specificity of L. schinusae

in Argentina and Brazil indicated this species was not strictly monophagous on
Brazilian Peppertree. Its larvae completed development on several Schinus species
and on another member of the Anacardiaceae, Astronium balansae Engl. (Urun-
day) (Mc Kay et al. 2012). Of greatest concern were the quarantine results that
indicated larvae could complete development on several Florida natives, including
Rhus aromatica Aiton (Fragrant Sumac) and Winged Sumac. A second species of
Gracillariidae, E. schinusivora, was also colonized and tested under quarantine.
Although the larvae created more mines and seemed to complete development
best on Brazilian Peppertree, larvae also completed development almost as well on
Winged Sumac (Rendon et al. 2012). Neither species showed sufficient specificity;
thus, they were not petitioned for release. The third leaf blotcher (C. schinusifolia)
and a stem blotcher (Marmara sp.) were not tested. Additional tests, such as choice
tests or multigenerational tests, could have been conducted (Schaffner 2001, Van
Klinken 2000), but due to the broad host range indicated by the no-choice tests,
neither of these species received further testing (Table 1).
Notodontidae defoliators. Two species of Notodontidae defoliators were tested:
Tecmessa elegans Schaus and Nystalea ebalea Stoll (Lepidoptera: Notodontidae).
The first, T. elegans, was found from northern Argentina, north to Minas Gerais,
Brazil, on both Brazilian Peppertree and Lithraea brasiliensis L. Marchand
(Aroeira de Bugre) (Oleiro et al. 2011). No-choice starvation tests indicated this
species could feed and mature to the adult stage when fed Pistacia vera L. (Com-
mon Pistachio), and on several Florida natives, including Metopium toxiferum (L.)
Drug and Urb. (Poisonwood) and Winged Sumac. The second species, N. ebalea
was also tested under quarantine; larvae fed and matured on several Florida native
species (Wheeler et al. 2014). This same species, N. ebalea was later found feeding
on Brazilian Peppertree in Florida (Wheeler 2013). Neither of these species was
petitioned for release (Table 1).
Geometridae defoliators. Numerous species of Geometridae have been found
feeding on Brazilian Peppertree in Brazil (G.S. Wheeler, unpubl. data), a subset
of which have been colonized and tested under quarantine to determine their
specificity for the tree species. We colonized and tested 4 Geometridae defoliators:
Hymenomima memor (Warr.), Oospila pallidaria Schaus, Oxydia vesulia (Cramer),
and Prochoerodes onustaria (Hübner) (Lepidoptera: Geometridae). We examined
the host range of these species by no-choice starvation tests. All were found to feed
and develop on US native species and economically important plants. H. memor lar-
vae fed and completed development on nearly all species tested, including Winged
Sumac and Cashew (E. Broggi and G.S. Wheeler, USDA/ARS, Ft. Lauderdale,
FL, unpubl. data). O. pallidaria and O. vesulia larvae fed and completed develop-
ment on several Florida native species, including Winged Sumac and Poisonwood
(Fung and Wheeler 2016; G.S. Wheeler et al., USDA/ARS, Ft. Lauderdale, FL,
unpubl. data). Testing of P. onustaria indicated that this species fed and completed
development on several members of the Anacardiaceae, including the economic
species Mangifera indica L. (Mango) (E. Jones and G.S. Wheeler, USDA/ARS, Ft.
22
Lauderdale, FL, unpubl. data). When we obtained these findings, we eliminated the
geometrids from further testing and destroyed the quarantine colonies (Table 1).
Gelechiidae borer. Larvae of Crasimorpha infuscata Hodges (Lepidoptera:
Gelechiidae) produce stem galls near the tips of Brazilian Peppertree plants. This
species was previously released in Hawai’i in 1961 but it did not become estab-
lished on the islands (Krauss 1963, Yoshioka and Markin 1991). During field
surveys that we conducted in South America, we observed C. infuscata only on
Brazilian Peppertree and Schinus weinmannifolia Engl. (Arue’i) (F. Mc Kay, un-
publ. data). We also collected a few galls from stems of the congener Schinus molle
L. (Peruvian Peppertree) that resembled those caused by C. infuscata; however,
when we introduced these galls under quarantine, adult moths failed to emerge (F.
Mc Kay et al., unpubl. data). In quarantine no-choice testing, this species produced
stem galls on Common Pistachio and Winged Sumac; however, adults failed to
emerge from these non-target species (F. Mc Kay et al., unpubl. data). Given the
insect’s ≥5-month life cycle and the consequent slow pace of testing this species,
the difficulty encountered in Hawai’i with establishment, and the potential threat
to important North American plants, we discontinued further development of this
insect as a biological control agent (Table 1).
Tortricidae leaf binders. Episimus unguiculus (= E. utilis) Clarke (Lepidoptera:
Tortricidae) was first released in Hawai’i in 1951 and has established broadly
on the islands (Krauss 1963, Yoshioka and Markin 1991). Early larval instars of
E. unguiculus act as a leaf binder of Brazilian Peppertree, and during the last instars
the larvae roll and seal a single leaflet into a tubular retreat from which they feed
and pupate (Martin et al. 2004). We examined the host range of E. unguiculus for
releases in Florida; however, petitions to the TAG were rejected and no releases
were made (Table 1).
Lasiocampidae defoliators. We collected Tolype medialis (Jones) (Lepidoptera:
Lasiocampidae) larvae in Brazil that we observed feeding on Brazilian Peppertree
leaves. Under quarantine, when presented with leaves of the closest relatives grown
in Florida, the larvae fed and completed development on several species, including
Poisonwood, Winged Sumac, Comocladia dodonea (L.) Britton (Poison Ash), Co-
tinus obovatus Raf. (American Smoketree), Cashew, Mango, Pistacia terebinthus
L. (Terebinth) (Cyprus Turpentine), and Spondias purpurea L. (Jocote), but not
Poison Ivy (G.S. Wheeler et al., unpubl. data). Due to this broad host range, we
eliminated the species from further testing (Table 1).
Euteliidae defoliators. Manrique et al. (2012) collected the defoliator Paectes
longiformis Pogue (Lepidoptera: Euteliidae) in Bahia, Brazil, and tested the species
under quarantine. Results indicated that larvae survived to the adult when fed Com-
mon Pistachio and Malosma laurina Nutt. ex Abrams (Laurel Sumac) (Manrique et
al. 2014a). Following additional multiple-generation tests that showed P. longiformis
posed a risk to several non-target species, the authors concluded this species should
not be considered for release as a biological control agent (Table 1). Additional mem-
bers of this genus are known from Brazilian Peppertree in Brazil; however, their
suitability for biological control has yet to be determined (Pogue 2013).
23
Curculionidae defoliators. Members of this beetle family are some of the most
common and successful biological control agents used against invasive plants
(Clewey et al. 2012, Julien and Griffiths 1998). We tested 2 weevil species for
biological control of Brazilian Peppertree: Plectrophoroides lutra (Schoenher) (a
broad-nosed weevil) and Omolabus piceus (Germar) (Coleoptera: Curculionidae)
(a leaf-rolling weevil). We collected several broad-nosed weevil species in Bahia
state, Brazil. Of these, P. lutra was the most common and caused considerable
damage to the leaves of the target. We imported this species under quarantine and
evaluated the host range of the adults for biological control (Wheeler et al. 2011).
Results of no-choice tests indicated that the adults not only ate Brazilian Peppertree
leaves, but also leaves of Poison Ivy and Mango. Field observations of the leaf-
rolling weevil, O. piceus, indicated that the realized host range of this insect was
restricted to the target, Lithraea spp., and Cashew (Wheeler et al. 2013). However,
quarantine no-choice tests with O. piceus on North American native and agricul-
tural species indicated that the adults ate and reproduced on nearly all species
presented (Wheeler et al. 2013). Neither species was pursued further for biological
control (Table 1).
An additional Curculionidae species, Apocnemidophorus pipitzi (Faust) (Cole-
optera: Curculionidae) was tested and recently rejected. This insect feeds on leaves
as adults and bores in stems as larvae (Cuda et al. 2011, Mc Kay et al. 2009). How-
ever, recent results indicate that this species was not approved for field release due
to a broad host range (Table 1).
Recent agents tested and petitioned for release

Leaf-feeding thrips. We discovered the thrips Pseudophilothrips ichini (Hood)
(Thysanoptera: Phlaeothripidae) feeding on and causing significant damage to Bra-
zilian Peppertree leaf tips in Brazil. This species occurs over a large geographic range
from northern Bahia state, south to southern Santa Catarina, Brazil, and is seasonably
abundant from sea level to 1300 m asl (Wheeler et al. 2016). In visual inspections of
sympatric members of the Anacardiaceae in Brazil, we observed P. ichini only feed-
ing on Brazilian Peppertree. Temperature-based physiological models indicated that
this thrips could establish throughout the invaded range in the US (Manrique et al.
2014b). Two haplotypes of Brazilian Peppertree occur in the invaded range (Williams
et al. 2005), and P. ichini had similar survival when fed leaves of both haplotypes and
their intraspecific hybrids (Manrique et al. 2008). We selected P. ichini as a potential
biological control agent of Brazilian Peppertree because it appears to have a high
level of specificity for the target weed and a wide environmental tolerance, and field
observations and laboratory research indicate feeding damage dramatically reduces
growth and reproduction of the host.
Previously, the correct identity of this thrips species was called into question
(Manrique et al. 2008), and it was determined that earlier publications (Cuda et al.
2008, 2009; Garcia 1977; Hight et al. 2002) incorrectly applied the name P. ichini
to a different species (P. gandolfoi Mound, Wheeler, and Williams). Molecular
and morphological research indicated that more-recent testing correctly identified
P. ichini (Mound et al. 2010). Molecular methods were used to characterize this
24
thrips, and the resulting sequences are posted in National Center for Biotechnol-
ogy Information (NCBI, accessions GU942812- GU942818). Detailed methods are
provided in Mound et al. (2010).
We conducted a series of no-choice and choice tests with P. ichini on 127 plant
taxa, from 45 plant families (Wheeler et al., in press). Testing included 5 Mango va-
rieties, 3 Common Pistachio cultivars, and a hybrid Pistacia rootstock—taxa with
economic importance in the US. These host-range tests will be published separately;
however, we provide a brief summary here. In no-choice starvation tests, the thrips
fed and produced offspring on Brazilian Peppertree, and we observed no or few
adults or young on non-target species, except for the invasive ornamental Peruvian
Peppertree. This congener is a native of South America, a widely planted ornamen-
tal plant, and an invasive weed of natural areas in California (Howard and Minnich
1989, Nilsen and Muller 1980). The number of F1 P. ichini offspring produced on Pe-
ruvian Peppertree was, on average, 16% lower than on the controls. When thrips were
given a choice between Brazilian Peppertree and Peruvian Peppertree, they most
frequently selected Brazilian Peppertree, but in a single case (1 of 6 plants tested)
they chose Peruvian Peppertree. In this one replicate, the thrips produced 12 F1 adults
on the Peruvian Peppertree plant or 83% less than the controls. The choice tests
of the other test plants indicated that no or few—generally less than 2 F1 offspring
per plant—were produced on these non-target species. We conducted multiple-
generation tests and successfully obtained subsequent generations only on Brazilian
Peppertree and the non-target Peruvian Peppertree. We did not observe P. ichini
thrips on Peruvian Peppertree during our field observations in Brazil (Wheeler et al.
2016). These field observations and the quarantine test results above led to the con-
clusion that this thrips species is highly specific and safe for release against Brazilian
Peppertree. We presented a formal petition to the TAG in August 2014 requesting
permission for field release (Table 1).
Calophya latiforceps leaf gallers. A leaf-galling psyllid, Calophya latiforceps
Burckhardt (Hemiptera: Calophyidae), was discovered attacking Brazilian Pep-
pertree in Salvador, Bahia state in Brazil in 2010 (Burckhardt et al. 2011). A study
in 2012–2013 revealed that average gall density ranged from 0.3 to 37.5 galls/leaf,
and galls were observed in November and March, suggesting that the insect may
be present in the native range throughout the year (Diaz et al. 2014a). Additional
surveys found the same psyllid at several locations in Bahia and Espírito Santo
states (Diaz et al. 2015a). In an effort to predict whether the psyllid could establish
in Florida, one of the authors conducted a laboratory-based cold-tolerance study.
Survival of eggs and adults for several days at 0 oC suggested that the psyllid could
establish in all areas of Florida where Brazilian Peppertree is present (R. Diaz,
unpubl. data).
Based on collection records, the Calophya spp. associated with Schinus spp. in
South America are thought to be highly host-specific, with most species collected
from only 1 or 2 related hosts (Burckhardt and Basset 2000). Calophya latiforceps
has only been found associated with Brazilian Peppertree (Burckhardt et al. 2011).
We evaluated the laboratory host range of C. latiforceps by exposing psyllids to
25
89 plant species from 43 families, including 2 congeners of Brazilian Peppertree

and 5 cultivars of Common Pistachio and a hybrid Pistacia rootstock. These bioas-
says conclusively demonstrated that the psyllid is a highly specialized herbivore of
Brazilian Peppertree and is not able to survive on any other species. Minimal ovi-
position occurred on a few non-target plants, but all first instars died within 3 days
with no evidence of gall formation. In addition to testing non-targets, we examined
the ability of the psyllid to develop on the 2 Brazilian Peppertree haplotypes and
their hybrids that occur in Florida, and found that the insects were able to success-
fully develop on these different genetic lineages (Diaz et al. 2015b).
Prade et al. (2016) measured the impact of psyllids on Brazilian Peppertree per-
formance in several ways, including comparative measurements of photosynthesis
and chlorophyll content of infested and un-infested leaves, and quantification of
the effect of a 3-month infestation on plant performance. Photosynthesis was 63%
lower on galled leaves compared to leaves without galls, and chlorophyll content
was 10% lower on galled leaves versus those without galls. The 3-month study re-
vealed that plant height was reduced by 30%, leaf abscission was 4.5 times greater,
and the growth rate of trees was reduced 11% by psyllid infestation. A study in
the native range found that the closely related Calophya terebinthifolii Burckhardt
and Basset reduced biomass accumulation of Brazilian Peppertrees by 40% after 3
months (Vitorino et al. 2011). Although it is not possible to predict with certainty
the impact C. latiforceps will have on Brazilian Peppertree in Florida, some insight
may be offered by Calophya schini Tuthill (Hemiptera: Calophyidae), a special-
ized herbivore of Peruvian Peppertree, accidentally introduced into California in
the 1980s. The psyllid reached extremely high gall-densities and resulted in severe
defoliation of trees (Downer et al. 1988). Because of the severity of the problem,
a classical biological control program was initiated with the release of a parasitoid
from Chile (Zuparko et al. 2015), which reportedly provided satisfactory control
(Kabashima et al. 2014). Ironically, the California Invasive Plant Council now con-
siders the Peruvian Peppertree an invasive species (Cal-IPC 2014).
The psyllid (Psylloidea) families Psyllidae and Triozidae include several mem-
bers that transmit plant pathogenic bacteria (Hodkinson 2009), including taxa of
Candidatus Phytoplasma and Candidatus Liberibacter (Weintraub and Beanland
2006). The recent introduction into Florida of citrus-greening disease transmitted
by the Diaphorina citri Kuwayama (Psyllidae) (Manjunath et al. 2008) greatly
heightened the awareness of psyllid-vectored plant pathogens in the state. Although
there are no records of plant pathogen transmission by members of the family Calo-
phyidae, we assayed C. latiforceps for plant pathogenic bacteria and viruses. First,
Diaz et al. (2014a) used specific primers to detect the presence of 4 members of Ca.
Liberibacter: Ca. L. solanacearum (Lso), Ca. L. asiaticus (Las), Ca. L. america-
nus (Lam), and Ca. L. africanus (Laf). All tests were negative (Diaz et al. 2014a).
However, the authors went further and sequenced the 16S ribosomal RNA gene to
more broadly examine bacteria associated with C. latiforceps and 2 other Calophya
spp. This assay detected many bacteria that are not pathogenic to plants, but no Ca.
Liberibacter or Ca. Phytoplasma (Overholt et al. 2015). In addition, C. latiforceps
26
was tested for viruses using specific primers and by inoculating 2 highly susceptible
indicator species with psyllid homogenate, and all tests were negative (Diaz et al.
2014a). Based on the monophagy of C. latiforceps and the absence of plant patho-
genic bacteria and viruses, in April 2015, we submitted for review a formal TAG
petition for field release (http://www.aphis.usda.gov/).
Agents released
Three biological control agents were released in Hawai’i: the seed feeder
Lithraeus atronotatus Pic (Coleoptera: Bruchidae), the leaf folder Episimus
unguiculus Clarke (Lepidoptera: Tortricidae), and the defoliator Crasimorpha in-
fuscata Hodges (Lepidoptera: Gelechiidae) (Davis and Krauss 1962; Krauss 1962,
1963; Yoshioka and Markin 1991). Following the establishment of the first 2 spe-
cies in Hawai’i, damage has rarely reached levels that reduced the weed’s density
(Hight et al. 2002, Julien and Griffiths 1998, Yoshioka and Markin 1991).
Discussion
Biological control of invasive weeds in the southeastern US has had a number
of notable successes (Center et al. 2012, Rayamajhi et al. 2014). Most recently,
biological control of Solanum viarum Dunal (Tropical Soda Apple) with the beetle
(Gratiana boliviana Spaeth, Coleoptera: Chrysomelidae) reduced management
costs of this weed by 50% in Florida (Diaz et al. 2014b). Success of a biologi-
cal control program can be defined in many ways, using biological, ecological,
or economic contexts (Delfosse 2004). One of the most widely cited definitions
is divided into 3 categories: (a) complete—no other control method is required
or used, at least in areas where the agent is established; (b) substantial—other
methods are needed but the effort required is reduced; and (c) negligible—despite
damage inflicted by agents, control of the weed is still dependent on other control
methods (Hoffmann 1995). Some researchers consider as an important component
of success the discovery of a new agent and the completion of the host testing of
that agent; however, discovery and testing do not measure program success. For
our present example, biological control of Brazilian Peppertree, a degree of success
has been achieved by discovering and completing the testing of 2 agent species,
P. ichini and C. latiforceps. Our results demonstrated narrow specificity, safety, and
the potential to inflict damage on the target weed. If released, field studies will be
conducted that examine agent impacts on the weed and non-target populations.
Biological-control research of Brazilian Peppertree in Florida has been a long,
protracted process with little evidence of success. The most obvious limitation
has been the difficulty finding specialized herbivores in the native range that re-
strict their feeding to the target weed, while leaving native and economic species
unharmed (Table 1; Hight et al. 2003; Manrique et al. 2014a; Mc Kay et al. 2012;
Oleiro et al. 2011; Rendon et al. 2012; Wheeler et al. 2011, 2013, 2014). A further
setback resulted from the incorrect identification of the thrips P. ichini (Cuda et
al. 2008, 2009; Garcia 1977; Hight et al. 2002) that delayed colonization and test-
ing (Mound et al. 2010). Finally, a potentially host-specific sawfly species (e.g.,
27
H. hubrichi) may be non-toxic to cattle and wildlife, but regulators and the scien-
tific community need further evidence before they are convinced of its safety prior
to consideration for release (Dittrich et al. 2004).
We should acknowledge that the process of finding, selecting, and testing the
safety of potential agents is unpredictable and prone to numerous and lengthy de-
lays. The control method involves the introduction of exotic organisms into natural
areas, and strict procedures must be followed to ensure the safety and efficacy of the
proposed actions. Not surprisingly, the development of new agents can take many
years and require considerable investment in resources. Future efforts of this proj-
ect should focus on the 2 potential agents, P. ichini and C. latiforceps. Both species
have shown a high degree of specificity and effectiveness that should reduce the
competitiveness of Brazilian Peppertree in the southeastern US and Hawai’i. Once
approved, the mass production, redistribution, and impact of these agents on the
weed population and non-targets should be determined.
Acknowledgments
We thank E. Broggi, K. Dyer, and A. Sanchez (USDA-ARS-IPRL); M. Roddick, J. Ren-
don, M. Chawner, K. Hernandez, N. Silverson, J. Fung, and E. Jones (SCA-AmeriCorps); M.
Oleiro (Universidad de Buenos Aires); and Davi de Macedo and R. Barreto (Universidade
Federal Viҫosa, MG, Brazil) for assistance. Insect identifications were generously provided
by J. Brown, D. Davis, R. Gagné, A. Konstantinov, M. Pogue, and F.C. Thompson (USDA-
ARS-SEL, Beltsville, MD); S. Halbert (Florida Department of Agriculture and Consumer
Services, Gainesville, FL); C. Covell (McGuire Center, Gainesville, FL); C. O’Brien (Green
Valley, AZ); L. Mound and J. La Salle (CSIRO, Canberra, Australia); and A. Hausmann
(Zoologische Staatssammlung München, Munich, Germany). Molecular analysis of plant
and insect samples was conducted by D. Williams (TCU, Ft. Worth, TX). We also thank the
organizers for the invitation to participate in this Greater Everglades Ecosystem Restora-
tion symposium. This project was partially funded by Florida Fish and Wildlife Federation,
South Florida Water Management District, and USDA/ARS. We appreciate the efforts of 2
anonymous reviewers for their helpful comments and suggestions regarding this paper.
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Biological Control of the Invasive Weed Schinus terebinthifolia

(Brazilian Peppertree): A Review of the Project with an Update

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the

Biological Control of the Invasive Weed Schinus

Surveys of Native Range

were found (Krauss 1962). Gall-forming Lepidoptera, Diptera, and seed-feeding

Potential agents discovered

Figure 2. Species-accumulation curves showing discovery of new herbivore species on

Potential agents tested

Agents tested and rejected

Pergidae (sawflies). The first published account of a Brazilian Peppertree insect

Genus Species Order Family Source

(Lepidoptera: Gracillariidae) (Davis et al. 2011). Field specificity of L. schinusae

Recent agents tested and petitioned for release

89 plant species from 43 families, including 2 congeners of Brazilian Peppertree

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