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Biological Control of Plant-parasitic

Nematodes, 2nd Edition


Soil Ecosystem Management in Sustainable Agriculture

Graham R. Stirling
Biological Crop Protection Pty Ltd, Brisbane, Australia
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Library of Congress Cataloging-in-Publication Data

Stirling, Graham R.
Biological control of plant-parasitic nematodes : soil ecosystem manage-
ment in sustainable agriculture I by Graham R. Stirling. -- 2nd ed.
p.cm.
Includes bibliographical references and index.
ISBN 978-1-78064-415-8 (alk. paper)
1. Plant nematodes--Biological control. 2. Soil management. I. Title.

SB998.N4S85 2014
632' .6257--dc23
2013040394

ISBN-13: 978 1 78064 415 8

Commissioning editor: Rachel Cutts


Editorial assistant: Alexandra Lainsbury
Production editor: Laura Tsitlidze

Typeset by SPi, Pondicherry, India


Printed and bound in the UK by CPI Group (UK) Ltd, Croydon, CRO 4YY.
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6
Nematodes, Mites and Collembola
as Predators of Nematodes, and the
Role of Generalist Predators

_Nematodes have a diverse range of natural in the soil food web and provide a back-
enemies, but the literature on biological control ground level of nematode suppression in
has been dominated by research on microbial all soils. Consequently, they are vitally import-
antagonists for a number of reasons. First, most ant when soils are being managed to conserve
microorganisms are readily cultured on defined natural enemies of nematodes. The roles of
media, and so they are amenable to study in nematodes, Collembola and mites as top-
the laboratory. Second, commercial mass pro- down regulators of nematodes and other
duction techniques are available for bacteria members of the soil fauna are discussed here,
and fungi, and so they tend to be the first together with the soil and crop management
organisms selected for research programmes tactics that can be employed to enhance their
on inoculative or inundative biological con- activity within agroecosystems. The relative
trol. Third, organisms that exhibit a degree of merits of specialists and generalists as bio-
specificity towards the target nematode have logical control agents are also considered,
generally been considered more effective bio- and it is suggested that polyphagous preda-
control agents than generalists, and this has tors are an important but underestimated
meant that research has focused on bacteria component of the soil biological community,
such as Pasteuria, and relatively specialized and must play a role in ecologically sound
fungi capable of parasitizing the females and nematode management programmes. The
eggs of sedentary endoparasitic nematodes. chapter concludes with a discussion of best-
This chapter focuses on another group practice farming systems and their capacity
of soil organisms that are best described to provide the regulatory services needed to
under umbrella terms such as 'generalist', suppress nematode pests.
'polyphagous' or 'omnivorous', and considers
their role in suppressing nematode popula-
tions. It covers all the predatory micro-, meso-
and macro-fauna discussed in a review by Small Predatory Nematodes
(1988), but focuses particularly on nematodes,
Collembola and mites, the most widely stud- In the soil environment, nematodes that prey
ied predators of nematodes. Often neglected on other nematodes are found mainly in five
by those interested in finding 'silver bullet' taxonomic groups within the Nematoda:
solutions to nematode problems, these gener- Mononchida, Dorylaimida, Diplogasteridae,
alist predators dominate higher trophic levels Seinuridae and Tripylidae. Since these orders

© G.R. Stirling 2014. Biological Control of Plant-parasitic Nematodes,


2nd Edition (G.R. Stirling) 157
158 Chapter 6

and families are not only phylogenetically


different (van Megen et al., 2009) but also eco-
logically diverse, predatory nematodes can-
not be considered as a single entity. The m ain
characteristics of each group of n em atodes
are, therefore, outlined next. Addition al gen-
eral information can be obtained from Khan
and Kim (2007).

Characteristics of the five major


groups of predatory nematodes

The Mononchida, commonly referred to as


mononchs or mononchids, are unique among
the predatory n em atodes in that all species are
predacious. Most species are rela tively large
(usually greater than 1 mm in length) and are
considered K strategists by ecologists due to
their lon g life cycles and relatively low fecund-
ity. In the successional or colonizer-persis ter
classification often u sed to den ote the eco-
logical role of n ematodes, they occupy level 4 Fig. 6.1. A typical mononchid (Parahadronchus
(see Table 3.1 in Chapter 3). Equipped with a shakih). (a) Male; (b) female; and (c) a magnified view
distinct and well-armed m outh cavity that is of the buccal cavi ty. (From Ahmad and Jairajp uri,
2010, with permi ssion.)
instantly recognizable (Fig. 6.1), mon onchids
either completely swallow their prey or use
one or more puncturing or grasping teeth to feeders (Yeates et al., 1993a). Predatory species
tear the victim apart. A recent monograph by are often 1-4 mm in length, and they either
Ahmad and Jairajpuri (2010) provides an excel- suck body fluids from their prey through an
lent coverage of the morphology and phyl- opening in their n arrow stylet, or use a mural
ogeny of this group of nematodes, and is also tooth and associated sheath to ingest liquid
an indispensable guide to the taxonomy of the food. A book by Jairajpuri and Ahmad (1992)
Order Mononchida, w hich contains eight fam- covers the m orph ology and systematics of
ilies, 49 genera and hundreds of species. this group of nematodes, w hile a review by
The order Dorylairnida, which also con- McSorley (2012) provides a good summary of
tains large-bodied K strategists, is p h ylogenet- the ecology of three of the most common
ically related to the mononchids, with both dorylaimid genera, Aporcelaimellus, Eudorylaimus
orders residing in a single major clade within and Mesodorylaimus.
the Nematoda (Holterman et al., 2006). How- Since diplogasterids are close relatives
ever, members of the Mononchida form a rela- of the bacterial-feeding rhabditids, they share
tively tigh t taxonomic unit, whereas the order with them characteristics such as a short life
Dorylaimida is much more diverse, w ith its cycle and a capacity to feed on bacteria.
members displaying a mosaic of m orphological However, the buccal cavity of mos t diplogas-
characters that make them notoriously diffi- terids is a~med with teeth, and although this
cult to identify (Holterman et al., 2008). These enables these species to prey on nematodes,
taxonomic and diversity issues mean that it is they are often selective in their feeding habits
almost impossible to make general statem ents (Grootaert et al., 1977). Little is kn own about
about the feeding h abits of dorylaimids. Most their ecology in natural environments, but
gen era are considered omnivorous, but some the fac t tha t they are readily cultured on
are pred ators and others are plant or fungal bacteria has meant that there h as been some
Generalist Predators of Nematodes 159

interest in using them as inundative bio- (Prado Vera et al., 2010). Tripylids have a rela-
logical control agents against plant-parasitic tively narrow stoma armed with teeth, and
nematodes. their intestinal contents indicate that they
The genus Seinura is unusual in that it is ingest small microfauna, including nematodes.
one of very few predatory nematodes in the However, their impact as predators in agricul-
Aphelenchoididae, a family that predomin- tural soils has never been determined.
antly feeds on fungi. Predation on nematodes
is a three-stage process involving penetration
of the cuticle by the stylet; injection of digest-
ive enzymes to immobilize the victim and The prey of predatory soil nematodes
disintegrate its tissues; and bulb pulsation to
withdraw the body contents of the prey and Nematodes likely to be predacious are nor-
suck them into the intestine (Linford and mally distinguished from other nematodes
Oliveira, 1937; Hechler, 1963; Wood, 1974; on the basis of their oesophageal structure
Esser, 1987). However, predatory activity has and the type of armature used to capture and
only been observed on agar, and little is consume their prey (Fig. 6.2). However, as
known about the role of Seinura as a predator Small (1987) pointed out, the structure of the
in natural environments. buccal cavity provides no more than an indi-
The fifth group of predatory nematodes cation that a nematode may consume other
belong to the family Tripylidae, a group of pre- nematodes, as most predatory nematodes are
dominantly aquatic nematodes that also occurs to some extent omnivorous, and nematodes
in soil. There are seven genera in the Tripylidae, with similar mouth parts can have widely dif-
but a recent molecular study suggests that the ferent feeding habits. Thus, to fully understand
family should be reorganized into two clades the ecological role of a purported predator, its

Fig. 6.2. The mouth parts and anterior region of common predatory nematodes. From left to right:
mononchids have a wide buccal cavity armed with teeth and/or denticles; dorylaimids are equipped with
an odontostyle; Seinura has a stylet similar to plant- and fungal-feeding aphelenchids; diplogasterids have a
slender or spacious stoma that may be armed with moveable teeth; while the stoma of the Tripylidae is a
simple tube with one or more teeth on the dorsal and ventral walls.
160 Chapter 6

primary food sources must be determined in the number of predators aggregating


an environment where a full range of poten- at feeding sites (Bilgrami and Gaugler,
tial prey is available. 2005).
Much of our current knowledge of the • Mesodorylaimus is a widely distributed
biology, life history and feeding habits of genus that is usually considered omnivor-
predatory nematodes has been obtail;led by ous. In a laboratory study that is some-
observing their behaviour on agar plates. times cited as evidence ofomnivory, a species
However, from the perspective of feeding closely related toM. lissus was observed to
habits, prey availability on agar does not feed predaciously on other nematodes and
reflect the natural situation. Also, there is lit- encysted amoebae; parasitically on fungal
tle evidence that the behaviour of the predator hyphae, algae, root hairs and epidermal
and prey in such a highly contrived environ- cells of wheat; and microphagously in
ment bears any resemblance to activity in soil. colonies of bacteria and actinomycetes
Thus, only a limited number of studies in (Russell, 1986). However, further work is
Petri dishes will be mentioned here, simply to required to confirm these observations, as
indicate the type of information that has been in some of these cases, it is not clear
obtained from this type of research. Further whether the nematode was stylet-probing
examples can be found in Khan and Kim (2007). a potential food source, or feeding, grow-
ing and reproducing on that food source.
• Studies in New Zealand and India pro- • Mononchids are usually categorized as
vide examples of the many different relatively long-lived nematodes, but
feeding habits that are possible within observations on agar have shown that
aporcelaimids. In the former study, an Mononchus aquaticus can multiply rapidly
unidentified species of Aporcelaimellus on a diet of Panagrellus redivivus, with a
took at least 12 weeks to complete its life generation time of only 14 days being
cycle, but was only able to multiply on recorded at 28°C. Prey were only detected
two of nine algal species (Wood, 1973a). when they touched the lips of the
The studies in India looked at the preda- predator, ~d rhabditids were preferred
tory activity of A. nivalis in the presence as a food source over other nematodes
of nematodes, and showed that when (Grootaert and Mertens, 1976). However,
this species was offered various plant- in another study in which rhabditids
parasitic nematodes as prey, Meloidogyne were not included as prey, the least active
and Heterodera juveniles were preferred, nematodes were found to be the most
but predation was determined by factors vulnerable to attack (Bilgrami et al., 1983).
such as prey number, temperature, agar • Prey preference studies with three diplo-
concentration and starvation of the preda- gasterid predators (Butlerius sp., Monon-
tor (Khan et al., 1991). However, when choides longicaudatus and M. fortidens)
encounters with 31 potential prey species showed that all three species were cap-
from five feeding groups were assessed, able of feeding on bacterial-feeding and
the attack rate and strike rate was great- plant-parasitic species (Grootaert et al.,
est, and the number of prey remaining 1977; Bilgrami and Jairajpuri, 1989).
was lowest, for bacterial-feeding nema- Thus, claims by Bilgrami et al. (2005)
todes (Bilgrami, 1993). that juveniles of Meloidogyne incognita,
• Observations on the feeding behaviour Heterodera avenae and Anguina tritici were
of two dorylaimids on rice root nema- the 'highly preferred' prey of Monon-
tode, Hirschmanniella oryzae, showed that choides gaugleri must be treated with cau-
Discolaimus major killed more prey, and tion, as the only prey tested. were plant
fed and aggregated longer than Laimydorus parasites. Prey search duration was depend-
baldus. Prey search and killing abilities ent on temperature and prey density, and
were governed by temperature, prey dens- was briefest (10-20 minutes) at a tempera-
ity, starvation and prey incubation, ture of 20-30°C when 150-225 prey were
and depended on feeding duration and present on a 5.5 em-diameter Petri dish.
Generalist Predators of Nematodes 161

Another common method of determin- and Eudorylaimus) were considerably more


ing the feeding habits of predatory nema- common in its gut than in the soil nematode
todes is to measure the response of prey when community (see Small, 1987, for details of an
predators are added to pots. However, such unpublished study by P. Grootaert).
experiments have the same failings as obser- In the first serious attempt to define the
vations on agar, as a full range of food sources prey of predatory nematodes, Small (1987)
will not be available to the predator when collated information derived from gut content
sterilized soil or potting mix is used as a sub- analyses, direct observation, observations of
strate. When natural soil is added to pots, nematodes in culture, feeding experiments
evidence that 'prey' numbers are reduced by and pot experiments, and used it to draw
the 'predator' is only circumstantial, as other conclusions about the diet of various preda-
predators are also likely to be contributing. tory nematodes. Although it was recognized
Therefore, observations of gut contents pro- that the methods used to assess feeding habits
vide the only direct evidence of predation in were not entirely satisfactory, the detailed
the soil environment. However, as indigest- tables included in that review provide a good
ible or undigested remains of the prey must be summary of published information on the
seen (e.g. enchytraeid setae, nematode stylets), prey of various species of predatory nema-
such analyses cannot be used for fluid feeders todes. One of the summary tables (presented
or for predators with difficult-to-identify prey in modified form as Table 6.1) is particularly
in the gut. useful, because it indicates the prey organ-
One of the best examples of the system- isms that have been reported for each of the
atic use of gut content analysis to characterize five main groups of predatory nematodes.
the feeding habits of a predatory nematode in When the information presented in Small
a natural environment was a study in which (1987) is considered in its entirety, a number
the nematodes found in the gut of a monon- of conclusions can be drawn:
chid (Anatonchus tridentatus) were compared
with the community of nematodes present • Predatory nematodes may have preferred
in the soil from which the predator was food sources, but most are polyphagous
obtained. Twenty-three nematode species to some extent.
were found in soil from the sampling site, and • Seinura is the only known monophagous
18 of those species were represented in the predator.
gut contents, indicating that this predator • Nematodes are the most frequently
was polyphagous with respect to its nema- recorded prey of predatory nematodes.
tode diet. However, A. tridentatus seemed to However, it is not clear whether this
prefer some nematodes over others, as certain represents a genuine preference by the
dorylaim.ids (e.g. Pungentus, Aporcelaimellus predators, or merely reflects the greater

Table 6.1. An indication of the diet of five groups of predatory nematodes based on the percentage of
records published prior to 1987 that referred to common soil organisms as prey.
0
/o of records referring to various organisms as prey
No. of
Predator records Nematodes 01 igochaetes Rotifers Tardigrades Protozoa Othersa

Mononchids 143 75 7 7 5 6
Dorylaimids 91 47 24 4 1 4 19
Aphelench idsb 15 100 0 0 0 0 0
Diplogasterids 39 59 5 0 3 21 13
Othersc 32 25 6 31 6 13 19

~Includes bacteria, fungal hyphae and spores, moss, algae, diatoms, mites, mite eggs and insect eggs
bMainly Seinura
clncludes Tripyla and Tobrilus (Tripylidae); lronus (lronidae); Synonchium (Cyatholaimidae); and Eurystomina (Oncholaimidae)
(Modified from Small, 1987, with permission.)
162 Chapter 6

interest of nematologists in studying the designation of mononchids as predators


nematodes as prey. is usually interpreted to mean that their prey
• Plant-parasitic nematodes are rarely, if is nematodes, when the authors clearly state that
ever, the primary prey of predatory they 'feed on invertebrates such as protozoa,
nematodes. Most members of the nema- nematodes, rotifers, and enchytraeids'. Also,
tode community are potential prey, and the comments about the possible role of
whether a parii.cular species is successfully bacteria in the nutrition of mononchids are
attacked depends on its proximity to the usually ignored. Mononchus propapillatus and
predator (in space and time), and factors M. tunbridgensis have been cultured on bac-
such as body size, cuticle thickness, reten- teria (Yeates,1987a;Allen-Morley and Coleman,
tion of cuticles from previous moults, and 1989), while first and second stages of
a capacity to elude attack by moving rap- M. aquaticus did not prey on nematodes but
idly. Since nematode body size varies with survived on bacteria (Bilgrami et al., 1984),
life stage, juvenile and adult predators raising questions about the role of bacteria in
may have different food sources, and prey the nutrition of mononchids. Yeates (1987b)
may be differentially susceptible to preda- argued that mononchids would have difficulty
tion at different stages in their life cycles. competing with rhabditids for bacteria as their
• Oligochaetes (mainly enchytraeids) often large size would limit their scavenging range,
feature as prey, particularly for some of while the energy requirements of later stages
the larger nematodes. could probably only be met by predation.
• Dorylaimids that are often considered However, this does not preclude the possibil-
predatory (e.g. Eudorylaimus, Labronema, ity that bacteria are an important food source
Aporcelaimellus and Aporcelaimus) are for small mononchids and the juvenile stages
really polyphagous and may need to of large species.
ingest algae or moss to reproduce (Wood, Three other issues raised by Yeates et al.
1973b). (1993a) must also be kept in mind when con-
• Mononchids, diplogasterids and Seinura sidering the feeding habits of predatory nema-
are commonly reported as cannibalistic, todes. First, in a habitat such as soil, predators
whereas this phenomenon is rarely seen with broad mouths are likely to coincidently
in dorylaimids. However, it is not clear ingest foods other than their invertebrate
whether cannibalism is an artefact of cul- prey during the feeding process. Substrate
ture conditions in which preferred prey ingestion, for example, has been reported for
are absent. diplogasterids. Second, predatory nematodes
may feed on diatoms and other algae, fungal
Small's (1987) review concludes with a spores, yeast cells and protozoa, but this is
comment that our knowledge of the natural difficult to confirm because these organisms
prey of predatory nematodes is slight, and lack marker structures and cannot be seen in
that much of the available information stems the opaque gut of a nematode. Third, feeding
from chance observations. That conclusion is habits should ideally be determined at a spe-
supported by Yeates et al. (1993a), who noted cies level, as food preferences are likely to
that the feeding habits of many nematodes vary within genera or families.
have been inferred, and have not been con- The difficulties involved in verifying the
firmed by maintenance in biologically defined diet of soil organisms in an environment
conditions for many generations. where many potential food sources are avail-
The most common source of information able raises questions about whether it is pos-
on the feeding habits of nematodes is a paper sible to better define the feeding habits of
by Yeates et al. (1993a) that lists the presumed predatory nematodes. Small (1987) mentioned
feeding types of most nematode families and that faecal analysis, serological techniques
genera. Although this reference is a vital and marking of potential prey were possibil-
source of information for nematologists and ities that had not yet been used, but with the
is commonly cited in ecological studies, the technologies available today, the best option
detail in the paper is often overlooked. Thus, is molecular analysis of gut contents. PCR-based
Generalist Predators of Nematodes 163

techniques are widely used to analyse preda- Predatory nematodes as regulatory


tion by invertebrates in terrestrial ecosys- forces in the soil food web
tems, and although it is not always easy to
detect degrad~d, semi-digested DNA- and Specialist and generalist predator nematodes
issues such as short-post-ingestion detection occupy upper trophic levels within the soil
periods, cross amplification and the risk of food web, and one of their functions (along
false positives inevitably cause difficulties- with many other organisms discussed else-
these problems have been overcome to some where in this book) is to act as top-down regu-
extent for insects and mites (King et al., 2008). lators of herbivorous, bacterivorous and
A recent study in Hawaii indicates that such fungivorous nematodes occupying lower
techniques are also useful for nematodes. trophic levels. There is experimental evidence
When the gut contents of five omnivorous to show that mononchids can markedly
and predatory nematodes were examined reduce populations of bacterivores and fun-
using species-specific PCR primers, Monon- givores in microcosms (see Chapter 3 for a dis-
choides, Mononchus, Neoactinolaimus, Meso- cussion of experiments by Allen-Morley and
dorylaimus and Aporcelaimellus tested positive Coleman, 1989, and Mikola and Setala, 1998),
for DNA of Rotylenchulus reniformis, one of the but given the biological complexity of soil
most common plant-parasitic nematodes in and the polyphagous feeding habits of preda-
Hawaiian soils (Cabos et al., 2013). Since that tory nematodes, the critical question from
study was done in soils where many poten- a biological control perspective is whether
tial prey were available, simple assays of this they play a role in regulating or suppressing
nature can be used to determine whether plant-parasitic nematodes. Yeates and Wardle
certain prey are utilized by predatory nema- (1996) argued that they were likely to play no
todes in natural environments. In future, more than a minor role for the following rea-
next-generation sequencing technologies sons: (i) mononchids and dorylaimids are
offer opportunities for much more powerful K strategists with generation times of weeks
dietary analyses, as they provide precise or months, and so they do not have the repro-
taxonomic identification of the food items ductive capacity to respond to rapid increases
actually utilized when a diet is highly in populations of plant parasites; (ii) predators
diverse (Pompanon et al., 2012). Since DNA may have multiple food sources; (iii) bacterial-
metabarcoding has the potential to reveal feeding nematodes often make a greater
many prey species simultaneously, it may contribution to the diet than plant-feeding
eventually provide information on the diet- nematodes; and (iv) large predators may
ary range of predatory nematodes that is be unable to access nematodes located in
vital to understanding their function within small soil pores. Nevertheless, the authors
an ecosystem. did conclude that plant growth could pos-
In concluding this discussion, it is clear sibly be improved by increasing populations
that most predatory nematodes are polypha- of predatory nematodes. However, this effect
gous to some extent. Individual species will was most likely to be achieved through indir-
vary in where they lie on a continuum from ect mechanisms (i.e. predatory nematodes
stenophagous specialist to ultra-generalist, enhancing nutrient cycling and thereby
but few species will be totally reliant on improving the plant's capacity to cope with
nematodes as a food source. Furthermore, it stresses associated with a high nematode
is unlikely that a predatory nematode will burden), rather than through a reduction in
feed only on plant-parasitic nematodes, and populations of plant-feeding nematodes.
this must be kept in mind when their poten- It would be unreasonable to expect pol-
tial as biocontrol agents is being considered. yphagous predators to regulate populations of
Predatory nematodes are generalists rather plant-parasitic nematodes to the same extent
than specialists, but this does not mean that as some of the more specialized parasites dis-
they cannot play a role in suppressing popu- cussed elsewhere in this book, but a study by
lations of economically important nematode Sanchez-Moreno and Ferris (2007) indicates
pests. that they do have a suppressive function. Soil
164 Chapter 6

was collected from woodland and an adja- Impacts of agricultural management


cent vineyard, and analyses of the nematode on omnivorous nematodes and
assemblage indicated that taxa richness, the generalist predators
Structure Index and the abundance of omni-
vores and predators (e.g. Discolaimus, Eudory- Short- and long-term effects
laimus, Qudsianematidae and Prionchulus) of soil fumigation
were significantly higher in the woodland.
Suppressiveness, as determined in a bioassay One way to start looking at the impact of
with Meloidogyne incognita juveniles, was agricultural management on the nematode
greater in the woodland soil and was posi- coDrrnnunity is to consider the short- and
tively related to the Structure Index, relative medium-term effects of perhaps the most bio-
abundance of omnivores and predators, and logically disruptive practice used in agricul-
organic matter content, whereas it was nega- ture: fumigation of soil with a broad-spectrum
tively correlated with the abundance of biocide such as methyl bromide. A study by
bacterial and fungal-feeding nematodes. Yeates et al. (1991) is useful in this respect, as it
However, this does not mean that omnivor- followed the recovery in biological activity in
ous and predatory nematodes were totally w1disturbed soil cores after they were fumi-
responsible for suppressing the plant para- gated with methyl bromide and then returned
site. The prevalence of omnivores and preda- to their original pasture or forests sites. Micro-
tors indicated that long and complex food bial biomass and bacterial numbers recovered
webs were present in the natural soil, and rapidly following fumigation, but after about
that organisms in similar functional guilds 24 weeks, fungal hypha! lengths were 25°/o
would also have been contributing to a sup- lower in the fumigated soils. Nematodes were
pressive service that is ultimately provided eliminated by the fumigant, and although
by many different members of the soil bio- recolonization was detected by day 26, nema-
logicalcoDrrnnunity. tode abundance and the number of species
Analyses of soil nematode communities present was still much lower in fumigated
by many authors in many different environ- than untreated soils after 24 weeks (10 versus
ments have consistently shown that monon- 62 nematodes/g soil; and 10 versus 31 nema-
chiefs and dorylaimids are more common in tode species, respectively). The cumulative
natural and relatively undisturbed ecosys- number of nematode genera detected to
tems than in agroecosystems, and are favoured 24 weeks (Table 6.2) is particularly interesting
by perennial rather than annual cropping because it indicates the capacity of different
(Freckman and Ettema, 1993; Wasilewska, nematode groups to respond to a major disturb-
1994; Neher, 1999b, 2001). Given that these ance event. The predominant nematodes
nematodes have a regulatory role, and that found in the fumigated soils were bacterial-
their presence is an indicator of a structured feeding species (e.g. Rhabditus, Cephalobus and
food web in which nematode predation and Plectus), as few aphelenchids and tylenchids
multitrophic interactions are occurring (Ferris had returned. With regard to the omnivorous
et al., 2001), it has been hypothesized that the and predatory component of the nematode
relatively low abundance of these nema- community, some mononchids were observed
todes in agroecosystems is one of the reasons in fumigated soil after 24 weeks whereas the
that their potential prey (bacterivorous, fungiv- dorylaimids were almost completely absent.
orous and herbivorous nematodes) exhibit However, samples taken more than 4 years
unregulated population increase in many after the soil was fQmigated showed that both
agricultural fields. The following two sections groups of nematodes had returned, as popula-
briefly summarize the research that has been tions of predators at the high-ralnfall pasture
undertaken to understand the factors respon- and forest sites were higher in fumigated soil
sible for the decline in populations of omnivores than the control (Yeates and van der Meulen,
and generalist predators under agriculture, 1996). However, there were differences in the
and the continuing research effort to find recolonization capacity of genera, as Iotonchus
management practices that can be used to failed to colonize either pasture or forest soil,
restore the condition of soil food webs. whereas Clarkus recolonized well.
Generalist Predators of Nematodes 165

Table 6.2. Mean nematode population densities from day 0 to day 166 in untreated (U) and methyl
bromide-fumigated (F) soil cores located at pasture and forest sites in moderate and high-rainfall
environments; and the number of nematode genera (grouped by higher taxa) accumulated in soil
collected 54,110, and 166 days after cores were fumigated and transferred to each site.

Moderate rainfall sites High-rainfall sites

Pasture Forest Pasture Forest

u F u F u F u F

Nematodes/g soil 42.3 2.4 8.2 1.2 304.5 5.0 10.8 0.3
No. of genera
Enoplida 2 1 2 4
Mononchida 1 1 2 3
Dory/aim ida 9 9 1 8 10
Chromadorida 4 2 7 2 6 3 7 1
Rhabditida 5 4 5 4 5 5 4 3
Diplogasterida 1 1
Aphelenchida 1 2 2 7
Tylenchida 9 2 6 1 4
TOTAL 29 13 33 10 31 11 33 6

(From Yeates eta/., 1991, with kind permission from Springer Science+ Business Media B.V.)

A study in the Netherlands carried out in (bacterivorous nematodes and protozoa) the
the field at about the same time as the previ- first to recolonize, and organisms in upper
ous study showed similar effects of soil fumi- trophic levels in the food web the last to
gation. Nematodes were first detected 3 weeks recover. Interestingly, however, mononchids,
after plots were fumigated with metham which are usually considered K strategists,
sodium, with bacterivorous and fungivorous were observed more frequently in fumigated
nematodes in c-p 1 and c-p 2 guilds being soil at 24 weeks than r-strategist diplogas-
observed. Nematode populations in fumi- terids (Table 6.2), raising questions about the
gated plots then remained low for another factors that govern the colonizing ability of
30 weeks, and even after 1 year, persisters these generalist predators. The value of the
(c-p 3--5) were still rare or below detection results obtained more than 4 years after soil
levels. The addition of cow manure (20 t/ha) was fumigated (Yeates and van der Meulen,
to plots 4 weeks after the fumigation was 1996) is that the data showed recolonization
completed did not markedly increase num- was both nematode-specific and site-specific.
bers of omnivorous or predatory nematodes Some mononchid species recolonized well
(Ettema and Bongers, 1993). Another study in and others did not, while the structure of the
strawberry-growing soils with a long history re-formed nematode community was influ-
of soil fumigation showed that fumigants enced as much by site (i.e. vegetation and
being used as alternatives to methyl bromide rainfall) as by previous fumigation. This sug-
reduced populations of omnivores and preda- gests that it is difficult to generalize with
tors to almost undetectable levels, and that regard to how a nematode community will
recovery did not occur during the time respond to a disturbance event.
between annual fumigation events (Sanchez-
Moreno et al., 2010). Negative effects of other agricultural
These observations are consistent with management practices
the notion that the soil biological community
is radically changed by a major disturbance Although no other agricultural practice is
event such as fumigation. The community likely to affect the nematode community to
then undergoes a series of successional the same extent as soil fumigation, there is
responses, with bacteria and their predators a large body of evidence to indicate that
166 Chapter 6

practices commonly used in agriculture have some weeds, was similar to fields that had
subtle and sometimes major effects on nema- grown a legume crop or had been planted to
todes, particularly those at higher levels in sugarcane (Stirling et al., 2007).
the soil food web. Evidence for the negative
impacts of some of those practices is summar- TILLAGE. A review of 106 published studies
ized next. However, care is needed in inter- indicated that tillage is more likely to be det-
preting the results of some studies, as rimental to large than small soil organisms
nematodes are often only identified to family (Wardle, 1995). Omnivore-predator nematodes,
level and indices are used to characterize the which are smaller than many other members
nematode community. For example, a review of the soil fauna, showed a variable response
of the literature by Neher (2001) showed that to tillage, probably because a variety of tillage
the Maturity Index was reduced by cultiva- implements would have been used in the
tion, nitrogen fertilization, liming, soil fumi- studies included in the analysis, and the fre-
gants and herbicides, indicating that these quency and depth of tillage would also have
practices are likely to have had negative varied markedly. Results of some later stud-
effects on some cp-4 and c-p 5 nematodes. In ies (e.g. Yeates et al., 1999; Sanchez-Moreno
such situations, the original publications et al., 2006) suggest there may be few adverse
must be consulted to determine whether par- effects from tillage, possibly because the
ticular nematodes were negatively affected. omnivores and predators now present in
agricultural fields are taxa that are relatively
soLARIZATION. Heat at temperatures above tolerant of tillage. However, tillage more com-
60°C is commonly used for experimental pur- monly has a negative effect on these nema-
poses to eliminate predatory nematodes and todes, as shown by the following studies:
other antagonists of nematodes (e.g. McSorley (i) cultivating land that had been under shrub
et al., 2006). However, the much lower tem- vegetation for many years reduced the abun-
peratures achieved when soil is solarized dance of predatory nematodes and quickly
may also affect omnivores and predators. For changed the nematode community structure
example, Wang et al. (2006) found that Seinura to that of a continuously cultivated soil
was tolerant of the heat generated by solar- (Villenave et al., 2001); (ii) omnivores were
ization, whereas Mylodiscus, the dominant more abundant in no-till than conventional
predator at the site where the work was con- till soils in North Carolina, but contrary to what
ducted, did not survive in solarized plots. In might be anticipated based on their c-p value
another study, the number of omnivore + of 4, three mononchid genera (Anatonchus,
predator genera was reduced by solarization, Clarkus and Mylonchulus) were relatively tol-
with only one genus (Eudorylaimus) surviving erant of cultivation (Fiscus and Neher,
the treatment (McSorley, 2011c). 2002); (iii) in a field experiment in California,
differences in the second and third trophic
FALLOWING. A long-term bare ground fallow levels of the nematode community were
(5 years of regular cultivation and occasional achieved through differential management,
applications of glyphosate) markedly reduced but these differences disappeared after a
numbers of omnivores + predators and the single oat crop was planted and the soil
number of genera in that trophic group was ploughed (Berkelmans et al., 2003); and
(McSorley, 2011c). However, the less severe (iv) after 6 years of no-till, omnivores were
fallowing practices commonly used in agri- more abundant, and structure and maturity
culture are likely to have far less impact. For indices were higher than in soil that had
example, a survey of 49 fields in Australia been tilled conventionally (Okada and
that were due to be replanted with sugarcane Harada, 2007).
showed that the number of omnivores and
predators (and the proportion of that group
of nematodes within the nematode community) NITROGEN. Experiments in which a range of
following a 5-12 month fallow maintained different nematodes were exposed to assay
with herbicides or cultivation but supporting solutions containing various nitrogen sources
Generalist Predators of Nematodes 167

showed that nematodes in c-p groups 4 and 5 anhydrobiosis in overcoming the toxic
were more sensitive to nitrogen than lower stress of nitrogenous compounds?
c-p groups (Tenuta and Ferris, 2004). Since
levels of nitrogen salts high enough to reduce
OTHER CHEMICAL STRESSORS. Numerous studies
the survival of c-p 4 and c-p 5 nematodes are
(reviewed by Nagy, 2009) have shown that
likely to occur at microsites around fertilizer
omnivorous and predatory nematodes are
granules, and in some parts of the soil profile
especially vulnerable to heavy metal pollutants.
when nutrients are applied as a single annual
For example, this group of nematodes was
dose in a band, the authors suggested that
particularly sensitive to zinc, copper and
nitrogen fertilization may contribute to the
nickel in soil (Korthals et al., 1996), while
low abundance of these nematodes in many
experiments in water, dune sand and soil
agricultural soils. However, it is not clear
showed that sensitivity to CuS04 increased
whether the detrimental effects of nitrogen are
with c-p class (Bongers et al., 2001). These
confined to situations where it is used inap-
detrimental effects on the nematode commu-
propriately or excessively. Results from a ferti-
nity can continue long after soil is contami-
lizer trial in New Zealand indicated that
nated with heavy metals, as omnivorous and
nitrogen applied at 200 kg/ha/ annum had lit-
predacious nematodes were either reduced
tle impact on populations of omnivorous nema-
or eliminated by zinc and copper treatments
todes, whereas the extremely high application
that h~d been applied 12 years previously
rate of 400 kg/ha/ annum reduced popula-
(Georg~eva et al., 2002). However, when zinc
tions of Aporcelaimus (Sarathchandra et al.,
and copper are used as microelements in
2001). Since enhancement of fertilizer use effi-
agriculture, they can have positive rather
ciency is currently a major focus of agricultural
than negative effects on c-p 4 and c-p 5 nema-
research, the critical question from an agroeco-
todes (Nagy, 1999), suggesting that it is the
logical perspective is whether the omnivorous
concentration rather than the presence of
and predatory nematode community is detri-
these elements that is important from a bio-
mentally affected when fertilization practices
logical perspective.
are optimized to the point where soil nitrogen
availability is relatively well synchronized
CONCLUSION. It is clear that omnivorous and
~th crop demand. Some of the critical ques-
tions to be answered with regard to the effects predatory nematodes are sensitive to a range
of nitrogen on these nematodes are: of physical and chemical disturbances, and
this is the reason they are often considered
• When nitrogen is concentrated in bands 'stress-sensitive' species. Since they have
due to the application methods commonly long generation times (months rather than
used in row crops, what is the short- and days or weeks), and produce relatively low
long-term impact on the nematode com- numbers of eggs, recolonization occurs slowly
munity within and between the bands? following a disturbance event. Thus, when
• Can the detrimental effects of nitrogen be populations of omnivorous and predatory
minimized by reducing the volume of soil nematodes are depleted by mismanagement,
in direct contact with the fertilizer (i.e. by it will take time to restore the regulatory
increasing the distance between fertilizer balance in the soil food web.
bands, with a consequent increase in the
nitrogen concentration within the band)?
• Are any observed changes in nematode Management to maintain a
n~bers and diversity due to the toxic well-structured soil food web
effects of nitrogen, or to changes in the
availability of the nematodes' food sources? Based on the observations discussed, a food
• Since toxicity to nematodes is most web with some capacity to regulate nema-
likely to occur as the soil dries and tode populations through the activities of
nitrogen concentrations increase within a biological community that includes omniv-
soil water films, what is the role of orous and predatory nematodes is only
168 Chapter 6

likely to be achievable in agricultural soils by rather than granules; or to apply a controlled-


enhancing the food sources that sustain these release product. We also need to address the
nematodes, and by minimizing the disturb- issue of low fertilizer use efficiency in modem
ance events that affect them. Thus, the first industrialized cropping systems. Commonly,
steps commonly taken to improve food web more than 50°/o of applied nitrogen is not used
structure are to (i) increase organic inputs by the crop, and this excess nitrogen is not
with cover crops, and (ii) reduce disturbance only detrimental to the off-farm environment,
through conservation tillage practices such as but may also have negative consequences
no-till, minimum-till or strip till. Although it is for omnivorous and predatory nematodes.
too early to draw conclusions on the types of Improving nitrogen use efficiency by synchro-
cover crops that should be included in the nizing soil nitrogen availability with plant
rotation sequence, the choice of crop appears nitrogen demand remains a major challenge
to be important, as the crop grown in a long- in agriculture (Grandy et al., 2013), but impro-
term fanning systems trial in California had vements in this area could have major spin-
significant effects on the nematode commu- offs in terms of enhancing the structure of soil
nity in most years (Berkelmans et al., 2003). food webs.
A capacity to produce biomass is likely to be Producing biomass in situ by growing
another important attribute of the crop, but legumes and a diverse range of other crops in
there is some evidence to suggest that legumes a minimum-till farming system is the most
are beneficial. Bean, safflower, tomato and sustainable way of arresting the decline in
maize were included in the California trial levels of soil organic matter that has occurred
mentioned above, and although differences in under modern agriculture. However, an alter-
the Structure Index, which is primarily deter- native that is economically feasible in some
mined by omnivorous and predatory nema- situations is to use locally available organic
todes, were not consistent between crops, this wastes as soil amendments. From the per-
index was generally higher following beans. spective of creating a more structured nema-
Amending soil with sunn hemp, a leguminous tode community, there is some evidence that
amendment, increased the abundance of this approach can produce the desired effect.
omnivorous and predatory nematodes in pots For example, when cow manure was applied
(Wang et al., 2003b), while the Structure Index at 20 t/ha to a coarse sandy soil in the
was significantly greater following sunn Netherlands, predatory mononchids (genus
hemp than bare ground in a strip-tilled living Clarkus) increased from negligible levels to
mulch system in Hawaii (Wang et al., 2011). 3-So/o of the nematode community after 44-60
One advantage of including legumes in weeks. Three dorylaimid genera also increased
the rotation sequence is the additional benefit markedly from about 16 weeks, largely due
of building soil nitrogen pools. However, the to an increase of Microdorylaimus, which
biological problems associated with nitrogen appeared to be feeding on algae (Ettema and
usage will not be overcome by simply intro- Bongers, 1993). In another experiment with
ducing a legume into the farming system. rice straw compost in Japan, pre<iatory nema-
Given the detrimental effects of excessive todes increased in abundance in comparison
nitrogen on c-p 4 and c-5 nematodes, overall with chemical and no fertilizer treatments
nitrogen management must be improved, and (Okada and Harada, 2007). However, exces-
to do this we need to know much more about sive amounts of nitrogenous amendments
the effects of application rate, placement, for- can also have negative impacts. For example,
mulation method and nitrogen source, on mononchids were almost eliminated by the
these organisms. Applying nitrogen fertilizer 10 t/ha poultry manure typically applied to
in bands or as granular formulations creates ginger fields in Fiji (Turaganivalu et al., 2013).
high-nitrogen pockets that may impact nega- Most organic amendments are usually
tively on omnivorous and predatory nema- incorporated into soil with tillage imple-
todes, so we need to know whether it is better ments, but applying them to the soil surface
from a biological perspective to spread the as mulch may be a better option, as the soil is
fertilizer evenly or to band it; to use powders not physically disrupted. The main benefits
Generalist Predators of Nematodes 169

from mulching are greater moisture reten- Although the impact of organic amend-
tion and a more stable temperature and ments and mulches on omnivorous and preda-
moisture environment, and this leads to tory nematodes has often been studied, many
increased soil microbial activity and bio- of the observations made are not as useful as
mass. Thus, when asparagus and maize crops they could be for a number of reasons: experi-
were mulched with sawdust in New Zealand, ments are often done in soils where nema-
populations of omnivorous nematodes todes at higher trophic levels have been
and two groups of predatory nematodes depleted by years of inappropriate manage-
(Mononchidae and Nygolaimus) were enhanced ment; the soil is cultivated aggressively when
to the point where their predatory activities the experiment is established, or when the
were thought to have been suppressing amendment or mulch is applied; and the soil
populations of bacterial and fungal-feeding nematode community is assessed before it
nematodes (Yeates et al., 1993b ). Further has had time to respond fully to a treatment.
observations after the mulch had been in The following are some of the many examples
place for 7 years indicated that populations of such studies that could be mentioned: (i) in
of top predatory nematodes were consist- an experiment in which composted cotton gin
ently greater in mulched plots than other trash, swine manure and a rye-vetch green
treatments in each of the last 6 years of manure were applied as amendments to a
the experiment (Fig. 6.3). Since an increase tomato field in North Carolina, the fact that
in microbial biomass was not matched by a the plots were tilled twice during each grow-
corresponding increase in bacterial-feeding ing season probably explained why the already
nematodes, it was presumed that the top low populations of omnivorous nematodes
predators were keeping these nematodes did not recover sufficiently to affect maturity
in check (Yeates et al., 1999). indices (Bulluck et al., 2002); (ii) plots in a

Annual crop (Q-5 em) Perennial crop (Q-5 em)

300
I I I I 600 I I I I
-
-~ 200 400
E
0
lO
~ 100 200
ci
.s
en
CD
"'C

~ Annual crop (5-10 em) Perennial crop (5-10 em)


E
Q)
c 150 I
~
~
"'C
~
c. 100
c.
~
50

1991199219931994199519961997 1991199219931994199519961997

Fig. 6.3. Total populations of top predatory nematodes in an annual crop (maize) and a perennial crop
(asparagus) when weeds were managed with sawdust mulch (x) or by four treatments that involved repeated
cultivation (o), hand weeding (6) or herbicide application (• and o). Vertical bars represent least significant
differences at P = 0.005. (From Yeates eta/., 1999, with permission.)
170 Chapter 6

Florida experiment were rototilled before levels in the soil food web are no longer present
cover crop and mulch treatments were estab- following decades of cultivation.
lished, and this may have been one of the
reasons that treatments had little impact on
omnivores and predators (Wang et al., 2008);
and (iii) when maize litter was added to an Maintaining the suppressive services
arable soil in Germany, the micro-food web provided by predatory nematodes
was so depleted that omnivores and predators and other generalist predators
at higher trophic levels did not respond
(Scharroba et al., 2012). What should be clear from the preceding dis-
Since crops grown in organic farming sys- cussion is that it will be quite difficult to
tems are never exposed to pesticides, and restore food webs in agricultural soils to any-
plants obtain nutrients through mineralization thing approaching the structure and diversity
of organic matter, it could be argued that food of natural soils. Some level of disruption is
webs should be more structured on organic inevitable in agroecosystems, and since omni-
than conventional farms. However, this is not vorous and predatory nematodes are particu-
always the case, presumably because the soil is larly vulnerable to disturbance, the regulatory
frequently disturbed by tillage. In a long-term services they provide are easily squandered.
experiment in California, predacious and The key to maintaining the structured food
omnivore nematodes were low in both organic webs that provide regulatory services is to
and conventional farming systems (Ferris develop a farming system where carbon
et al., 1996), while differences in maturity indi- inputs are continuous and the soil biological
ces were not observed in a survey of conven- community is not constantly disrupted by
tionally and organically managed farms in tillage and harmful chemical inputs. Therefore,
North Carolina (Neher et al., 1999a). farming systems must embrace practices such
The fact that soil food webs in perennial as minimum tillage; optimal nitrogen man-
cropping systems are more structured than agement; legumes and biomass-producing
in annual crops (Neher and Campbell, 1994; cover crops in the rotation sequence; and a
Neher, 1999b) suggests that a combination of permanent cover of crop residue or organic
continuous organic inputs and an absence of mulch on the soil surface. Practices likely to
tillage may be required to enhance omnivorous be detrimental to soil organisms (e.g. solar-
and predatory nematodes in annual cropping ization and bare fallowing; fumigants, nemati-
systems. However, it has proved quite difficult cides and most soil-applied pesticides; some
to consistently demonstrate this. A long-term above-ground chemical inputs; and excessive
experiment sampled by Okada and Harada amounts of nitrogen fertilizer), must be
(2007) in Japan clearly showed that K-strategy avoided. Since the benefits from modifying
nematodes were enhanced by combining no- the farming system in this way are likely
till with organic fertilizer, while similar benefits to take many years to eventuate, regular
were obtained in Hawaii when mulch was monitoring is required to confirm that a well-
combined with strip tillage, a tillage system in structured biological community eventually
which only a small proportion of the seed row develops, and that full remediation occurs.
is cultivated and most of the field remains In situations where omnivorous and preda-
undisturbed (Wang et al., 2011). In contrast, tory nematodes have been eliminated by dec-
observations in a long-term farming systems ades of inappropriate management, the option
experiment in California (Sanchez-Moreno of reintroducing them from undisturbed
et al., 2006; Minoshima et al., 2007), and at an locations nearby may have to be explored
adjacent organically managed site (DuPont {Tomich et al., 2011). However, when this was
et al., 2009), indicated that omnivore and preda- attempted by transferring undisturbed cores
tor nematodes were scarce, and did not become from a natural forest to an agricultural soil,
more abundant under continuous cropping re-establishment was not immediately suc-
and no tillage. Thus, it is possible that in some cessful, as populations of the introduced
situations, the desired response will never be nematodes had not increased after 1 year
obtained because nematodes at higher trophic (DuPont et al., 2009).
Generalist Predators of Nematodes 171

Ferris (2010) provides a good summary of populations can by reduced by species of


the issues that must be considered when Mononchoides has been presented (Khan and
attempts are being made to maintain or Kim, 2005; Bilgrami et al., 2008). This work is
enhance the structure and functions of the soil discussed in Chapter 12, but as inundative bio-
food web. What is clear from that review, and control is likely to be limited by economics to
from any text in soil ecology, is that properly small areas and valuable crops, future research
functioning soil food webs contain a multitude should focus on understanding the feeding
of organisms with apparently similar func- habits of predatory nematodes; the factors
tions, and that these organisms collectively that influence their occurrence in the soils used
provide a range of services, including regu- for agriculture; and the practices required to
lation of nematode populations. Enhancing maintain them at reasonable population dens-
soil biological diversity provides the system ities in agricultural soils.
with functional resilience, as it ensures that a
particular service will continue when condi-
tions are unfavourable to one of the guilds that
normally provide that service. Thus, a study Microarthropods as Predators
by Griffiths et al. (2010) in the UK showed that of Nematodes
when arable fields were subjected to various
amendment and rotation treatments, there The main members of the soil mesofauna:
were times when faunal groups such as mites, Collembola and Symphyla
enchytraeids and predatory nematodes were
reduced. However, when this occurred, there
Mites, collembolans and symphylans (Fig. 6.4),
were compensatory increases in functionally
together with a variety of small insects collec-
equivalent groups such as earthworms and
tively known as microarthropods, are ubiqui-
mesostigmatid mites. In the same way, popu-
tous in soil. They are particularly abundant in
lations of omnivorous nematodes were low
natural habitats such as grasslands and for-
and predatory nematodes were never observed
ests, where soil organic matter has accumu-
in the soil used for a vegetable farming sys-
lated over many years, root biomass is high,
tems experiment in Australia, but suppressive-
roots are permanently present and the soil
ness to root-knot nematode was still enhanced
surface is always covered by a layer of decay-
by some treatments, presumably because a
ing litter. In such situations, particular groups
subset of the natural enemies normally found
of microarthropods can reach population dens-
in a healthy soil were still effective (Stirling,
ities greater than 100,000/m2•
2013). Collectively, these observations suggest
Mites are the most abundant arthropods
that when management practices are being
in soil, and are found in four major taxonomic
considered to sustain regulatory services in
groups: the Oribatida (formerly Cryptostig-
agricultural soils, the focus should be on
mata), Prostigmata, Mesostigmata and Astig-
developing a diverse and active soil biological
mata. More than 50,000 species have been
community rather than on increasing popula-
described.
tions of specific predatory nematodes.
• Oribatids (suborder Oribatida) are by
far the most numerous soil mites, but in
Predatory nematodes contrast to other microarthropods, they
and inundative biocontrol reproduce relatively slowly and are, there-
fore, considered K strategists. Although
In the years since Cobb (1920) first suggested mainly fungivores and detritivores, some
that plant-parasitic nematodes could be con- are predacious.
trolled by introducing predacious nematodes • The Prostigmata are the most diverse
into infested fields, there have been many opti- group of soil mites, displaying a huge
mistic pronouncements about the potential of range of morphological and behavioural
these nematodes as biocontrol agents. In recent variation. Many above-ground species
years, attention has shifted from mononchids to are serious pests of plants and vertebrates,
the diplogasterids, and evidence that nematode but terrestrial species are also important,
172 Chapter 6

Fig. 6.4. Examples of common microarthropods in soil: a mite, collembolan and symphylan.

and sometimes outnumber all other soil crop pests, as they will consume plant roots.
mites. Soil-inhabiting prostigmatic mites Some species are predators of arthropods
generally feed on fungi or algae, or ingest and nematodes.
particulate matter, but some are preda-
tors, feeding on other arthropods or their
eggs, or on nematodes.
• Mesosti.gmati.d mites are not as numerous as Evidence of nematophagy in various
oribati.ds or prostigmati.c mites, but are uni- groups of microarthropods
versally present in soil. A few species are
fungal feeders, but most are predators. The Results from field observations, feeding
larger species tend to feed on small arthro- studies and analyses of gut contents
pods or their eggs, whereas the smaller spe-
In his comprehensive coverage of interactions
cies are mainly nematophagous.
that occur within the soil food web, Wardle
• The Astigmata are the least common of
(2002) pointed out that microarthropods com-
the soil mites. In agroecosystems, they are
monly prey on other members of the soil
most abundant in situations where crop
fauna, and provided several examples where
residues or manures have been incorpo-
populations of springtails, enchytraeids and
rated into soil under moist conditions.
nematodes were regulated by top predators.
Collembolans (springtails) are primitive However, determining who is eating what
insects that sometimes rival mites in their in soil is fraught with the same difficulties
abundance in soil. Many species are oppor- discussed earlier for predatory nematodes.
tunistic r-strategists capable of rapid popu- Microarthropods are grouped into five feeding
lation growth when decomposing organic categories (bacterivores, fungivores, plant feed-
matter and its associated microbes are avail- ers, omnivores and predators), but omnivory
able as a food source. They primarily feed on is common, even among animals that may exist
fungi, but many species are omnivorous and primarily on one food source. Thus, many
some are known to consume nematodes. arthropod predators are generalists, and may
Symphylans, relatively large translu- attack nematodes, lumbricid and enchytraeid
cent arthropods that resemble centipedes, oligochaetes, tardigrades, insects, myriopods
are widespread in soil but nowhere near and mites (Moore et al., 1988). Determination
as common as collembolans. Since they are of trophic behaviour requires a combination of
photophobic and can move rapidly, they laboratory observations, gut content analyses of
hide in voids when soil is disturbed, and are, field-collected specimens and experimenta-
therefore, rarely seen. Although generally tion, but as with all predators in soil, none of
considered detritivores, they can also be these methods is entirely satisfactory.
Generalist Predators of Nematodes 173

With regard to observations on arthropod- species indicated that there was little rela-
nematode interactions, studies by David tionship between the structure of their
Walter and colleagues in the late 1980s, but chelicerae and feeding habits. Most mesos-
particularly the observations made by Walter tigmatic mites consumed nematodes and
and Ikonen (1989), are worthwhile summarizing arthropod prey, and some were also able
here, as they provide a good summary of what to feed on fungi. Thus, three categories of
was known about nematophagous micro- nematophagous arthropods were recog-
arthropods at that time. Although this research nized: omnivores feeding on microbes and
focused specifically on grassland soils in nematodes; general predators of soil inver-
Colorado, the observations made over several tebrates; and nematode specialists. How-
years provide a good indication of the types of ever, it was recognized that the specialized
microarthropods that prey on nematodes, and group could attack a variety of prey.
their feeding habits and behaviour in soil. • Nematophagy could not be confirmed
for tydeid mites, despite the fact that
• Feeding studies with 14 species of meso-
studies in other environments (Santos
stigmatic mites showed that they ate 4-8
et al., 1981) had previously shown that
nematodes (Acrobeloides sp.) per day,
this group of mites were able to prey on
which equates to between 22°/o and 109°/o
free-living nematodes.
of their body weight. The amount of nema-
• Species in the families Rhodocaridae, Diga-
tode biomass consumed was strongly
masellidae and Ascidae were considered
related to the body weight of the preda-
to represent a 'small-pore nematophagous
tor. When mites were given a choice of
mite guild' characterized by: (i) an ability to
nematode prey, there was no significant
maintain continuous cultures on nematode
indication of preference.
prey; (ii) the presence of chelicerae adapted
• The most important nematophagous taxa
to feeding on nematodes and arthropods;
in Colorado grasslands were the Acari
and (iii) a small body size and convergent
(mites) and Symphyla. The latter group
body plan that allowed these animals to
are generally considered detritivores or
access prey residing in small pore spaces.
root feeders, but observations of symphy-
Since species in this guild were able to colo-
lans collected from grasslands showed
nize soils to a depth of 30 em, they could
that they primarily had nematodes and
access a much larger proportion of the soil
arthropods in their gut contents, and little
profile than larger mites.
fungal, detrital or plant material.
• All four main acarine sub-orders were Other studies have also shown that nema-
found in grassland soils, and each order todes are likely to be a component of the diet
contained nematophagous and fungiv- of many different mites. For example, mites
orous species. This indicates that the feeding from four different orders (Mesostigmata,
habits of mites are a species-level phenom- Endeostigmata, Oribatida and Astigmata)
enon, and cannot be inferred from morpho- were tested against entomopathogenic nema-
logy or relationships to higher-level taxa. todes in the laboratory and the majority
• Mesostigmatic mites appeared to be the were able to consume Steinernema feltiae and
most important group of nematophagous Heterorhabditis heliothidis. Although most spe-
arthropods, as only six of 63 species tested cies also fed on arthropods, some required
did not readily feed on nematode prey. In nematode prey for reproduction (Epsky et al.,
the presence of only nematode prey, most 1988}. Observations in a strawberry field in
of the nematophagous species produced Turkey indicated that when white grubs
eggs and developed into adults. were killed by entomopathogenic nematodes,
• Although it had previously been sugges- a species of Sancassania (Acari: Acaridae}
ted that nematophagous mesostigmatids moulted to the adult stage and began feeding
had developed specialized mouthparts on the host tissues and/ or microbes associ-
(designated types 1,2 or 3), and that gen- ated with the cadavers, and also consumed
eralist predators were equipped with type exiting infective juveniles. In the laboratory,
4 mouthparts, observations on 30 mite this mite consumed about 40 nematodes per day;
174 Chapter 6

was more likely to consumeS. Jeltiae than stable isotope ratios (i.e. 15N/ 14N). When this
H. bacteriophora; and was able to kill more method was used to evaluate trophic niche
nematodes in sand than in a loamy soil differentiation in oribatid mites from four
(Karagoz et al., 2007). When the stylets of plant- forest sites in Germany, the results suggested
parasitic nematodes were counted in the faecal that these mites spanned three or four trophic
pellets of an oribatid mite (Pergalumna sp.), the levels, and that different species occupied
data obtained in a laboratory study showed different trophic niches (Schneider et al., 2004).
that on average, about 18 Meloidogyne javanica Several taxa had much higher 15N signatures
and 42 Pratylenchus coffeae were consumed per than their litter habitat, suggesting that they
day (Oliveira et al., 2007). Collectively, these lived predominantly on an animal diet that
studies indicate that many mites are generalist possibly included nematodes. The value of
feeders, but they are capable of killing signifi- this method is that it reflects nutrition over a
cant numbers of nematodes in some situations. long period of time and, therefore, allows an
Although the contribution of nematodes to animal's predominant diet and trophic niche
the diet of Collembola has not been studied to to be determined. However, stable isotope
the same extent as mites, there is certainly evi- analysis is of limited value for identifying
dence that some species can consume large precise food resources, and so a more com-
numbers of nematodes. For example, Gilmore plete picture of an animal's trophic position
(1970) showed that ten of the 12 Collembola can be obtained by combining it with molecu-
species tested fed on nematodes in the labora- lar gut content analysis (Maraun et al., 2011).
tory, and that two species (Entomobryoides Numerous molecular approaches for
similis and Sinella caeca) consumed more than detecting prey remains in the guts, faeces and
25 nematodes/ day in a mixture of soil and ver- regurgitates of predators are now available (see
miculite. In another experiment in which two reviews by King et al., 2008 and Pompanon et al.,
species of Collembola (Thllbergia krausberi and 2012), and a study by Read et al. (2006) demon-
Onychiurus armatus) were introduced into a strated for the first time that they can be used
sandy soil, the number of Tylenchorhynchus to measure predation by soil-dwelling arth-
dubius on ryegrass seedlings was reduced by ropods on nematodes. A PCR-based approach
about SOo/o after 77 days (Sharma, 1971). Altho- was developed for detection of three species
ugh both these studies were carried out in of entomopathogenic nematodes, and a collem-
highly artificial environments, the high num- bolan and mesostigmatid mite were employed
bers of prey consumed suggests that nematodes to calibrate post-ingestion prey detection times.
are likely to be part of the diet of many collem- Detection times for nematode DNA within the
bolans. However, it is important to recognize guts of the predator were found to be longer for
that consumption of nematodes in the labora- Collembola than for mites, with half-lives· (SOo/o
tory does not necessarily mean that predation of the samples testing positive) of about 9 and 5 h,
occurs in soil. Proisotoma nr. sepulchris reached respectively. Predatory activity in the field was
high population densities in greenhouse cul- confirmed by retrieving microarthropods from a
tures of root-knot nematode (more than barley field where the nematode Phasmarhabditis
10,000 individuals/L soil) and was associated hermaphrodita had been applied 12 h earlier. Prey
with decreased numbers of nematodes in pots, DNA was detected in three of the four most
but observations of gut contents revealed only abundant microarthropod taxa recovered from
decaying roots and associated microflora the field, indicating that some species had fed on
(Walter et al., 1993). the introduced nematodes (Fig. 6.5). Since a pre-
vious DNA-based study had shown that one of
Detection of predation using stable isotope the collembolans was preyed upon by linyphiid
ratios and molecular techniques spiders, there are clearly opportunities to use
molecular technologies to better understand the
Since animal tissues are more enriched in 15N trophic linkages that occur within highly com-
than their food source, one way of determin- plex soil food webs.
ing whether an animal occupies a distinct The primers designed by Read et al.
trophic niche within soil food webs is to study (2006) have since been used to study predation
Generalist Predators of Nematodes 175

100
90
80
70
~
~ 60
UJ

~UJ 40
50
0
a. 30
20
10
0
lsotoma Lepidocyrtus Mesostigmatid /sotomurus
viridis cyaneus mites palustris

Fig. 6.5. Percentage of field-caught microarthropods (the Collembola lsotoma viridis, Lepidocyrtus cyaneus
and lsotomurus palustris, and mesostigmatid mites) testing positive for predation on the nematode
Phasmarhabditis hermaphrodita using species-specific primers targeting mitochondrial DNA. (From Read
eta/., 2006, with permission.)

and scavenging by three mite taxa: Oribatida, if generalist predators are nurtured and soil
Gamasina and Uropodina (Heidemann et al., structural characteristics allow them access to
2011). Several species of oribatid mites that root systems, they could play an increasingly
are normally considered detritivores were important role in suppressing plant-parasitic
found to consume nematodes when they were nematodes as populations rise. It also suggests
offered in a no-choice laboratory experiment. that when entomopathogenic nematodes are
Living and freeze-killed Phasmarhabditis her- applied in high numbers for insect pest con-
maphrodita and Steinernema feltiae were then trol, microarthropods that normally survive
added to forest soil and 48 h later, mites were on fungi, detritus and other food sources may
retrieved and checked for the presence of the limit their efficacy by switching to preying on
inoculated nematodes. Not surprisingly, the recently added nematodes.
predatory gamasid and uropodid mites con-
sumed nematodes, but interestingly, several Studies of 'fungivorous' and 'predatory'
of the oribatid mite species also ate living arthropods in microcosms
nematodes, even though they could have
selected different food in the field (Fig. 6.6). A microcosm experiment by Hyvonen and
DNA from dead nematodes was also found Persson (1996) demonstrates some of the com-
in their guts, indicating that these mites were plexities that occur when microarthropods and
also capable of scavenging for food. nematodes interact in an environment where
One of the main conclusions that can be numerous species with a wide range of feed-
drawn from these studies is that current ing habits are present. Microcosms containing
trophic groupings for Collembola and oribatid a complete microbial, nematode and tardi-
mites are inadequate. Many putative detriti- grade community and a defaunated humus
vores actually function as predators, fun- substrate were established and then three dif-
givores or scavengers, and this has important ferent arthropod treatments were imposed: a
implications for the structure and functioning no-arthropod control, fungivores only and
of detritivore food webs. Although many of fungivores + predators. The arthropods used
these omnivores will only feed opportunisti- as inoculum were collected from the field,
cally on nematodes, these findings suggest but in the fungivore treatment, prostigmatid,
that a huge range of microarthropods is astigmatid and mesostigmatid mites were
potentially predatory, particularly in situations removed to avoid adding potential preda-
where nematodes are readily available. From tors, and so the inoculum consisted of 14 col-
an agricultural perspective, this suggests that lembolan species and 17 species of oribatid
1 76 Chapter 6

• Phasmarhabditis hermaphrodita alive D Steinernema feltiae dead


A

100

lc 80
.Q
t5
Q) 60
Q)
"0
Q)

-g 40
Cii
E
Q)
z 20

0
Pergam. Uropod . Liacar. Chamob. Platyn. Nothru. Stegan.
(1 00) (17) (8) (17) (11) (12) (18)
------------------------------------
Oribatid mites

• Phasmarhabditis hermaphrodita dead D Steinernema feltiae alive


B

100

~ 80
~
c
0
:g
Q) 60
Q)
"0
Q)
"0
0
40
Cii
E
Q)
z 20

0
Pergam . Uropod. Liacar. Chamob. Platyn. Nothru. Stegan.
(82) (8) (3) (11) (126) (33) (43)
--------------------~--------------------
Oribatid mites

Fig. 6.6. Detec tion of (A) liv ing Phasmarhabditis hermaphrodita and dead Stein ernema feltiae and (B)
dead Phasmarhabditis hermaphrodita and living Steinernema feltiae in the gut of seven m ite species
(Pergam. = Pergamasus septentrionalis; Uropod. = Uropoda cassidea; Liacar. = Liacarus subterraneus; Platyn. =
Platynothrus peltifer; Nothru. = Nothrus silvestris; Stegan. = Steganacarus magnus; Chamob. = Chamobates voigtsl)
in th e field using part of the CO l gene as a molecular marker. Data represent percen tages of mite indiv iduals
in which nematodes were detected in the gut (the number of tested individuals is given in parentheses). The upper
and lower confidence limits are indicated as error bars. (From Heidemann eta/., 2011, w ith perm ission.)

mite that were considered 'fungivorou s'. When n em atode populations w ere
Microcosms with fungivores + predators were assessed after 103 and 201 days, the results
supplied with the same fungivores, but also showed that the 'fungivorous' arthropod
received a mixture of pros tigma tid and m es- community reduced nematode abnndance,
ostigmatid mites. and that this suppressive effect was further
Generalist Predators of Nematodes 177

strengthened by the addition of predatory relationships between nematodes, tardigrades,


arthropods. The data did not support the arthropods and other soil organisms were
hypothesis that the reduction in nematode more complicated than expected (Fig. 6.7),
populations was due to competition between demonstrating the difficulties involved in
fungivorous arthropods and fungivorous working with multiple interactions in soil
nematodes for food, as both bacterial- and food webs.
fungal-feeding nematodes were affected
(e.g. Wilsonema, Metateratocephalus, Acrobel-
oides and Aphelenchoides spp.), and estimates Mesostigmata as predators of
of fungal hyphae did not indicate clear differ- nematodes in agroecosystems
ences between the arthropod treatments.
Predation appeared to be the main reason that Although a wide range of mites are able to
nematode populations declined, and preda- utilize nematodes as a food source, the
cious activity was probably due in part to micro- Uropodina and Gamasina, two major taxo-
arthropods that would be better considered nomic groups within the Order Mesostig-
omnivores rather than fungivores. mata (= Gamasida), are the most specialized
Although the experiment was not set up predators of nematodes. However, it should
to assess the impact of tardigrades, it became be apparent from the previous discussion
obvious during the study that their role in the that most of the studies of nematode preda-
system also had to be considered. Tardigrades tion by mesostigmatids have been done
seemed to be efficient predators of nematodes, in relatively undisturbed natural habitats,
but their numbers, in turn, were strongly where these mites are always an important
reduced by predatory arthropods. Thus, trophic component of the microarthropod community.

Tardigrades
0 ----------------- -- ... Predatory
arthropods
,,
I
I
I

Nematodes

Bacteria Fungi

Dead organic matter

Fig. 6.7. Conceptual diagram of trophic relationships in a microcosm study with bacterial-feeding
nematodes (BF), fungal-feeding nematodes (FF) and omnivore/predator nematodes (0/P). Unbroken arrows
indicate material fluxes and broken arrows denote negative impacts. (From Hyvonen and Persson, 1996,
with kind permission from Springer Science+ Business Media B.V.)
178 Chapter 6

Table 6.3. Approximate benchmark figures for mite a digesting liquid to pre-orally digest
abundance and species richness of mesostigmatid their food, and then suck up the prey.
mites in grassland and arable field soil at a depth of • Nematodes play a central role as prey for
0-15 em. Gamasina in agroecosystems. Some spe-
Grassland Arable field cies feed exclusively on nematodes, but
most can also utilize other food sources
Abundance (individuals/m 2 ) (e.g. insect larvae and eggs, Enchytra-
Acari 100,000 50,000 eidae, Acari and Collembola).
Gamasina 10,000 5,000 • Size rather than motility may be critical
Uropodina 5,000 2,000
for success when these mites prey on
Species number
Gamasina 15 7
nematodes. The predator must be able
Uropodina 10 2 to access soil pores and microhabitats
where prey density is high.
(from Koehler, 1999, with permission.) • The low abundance and diversity of
Gamasina in agricultural soils is the
result of continual mechanical disturb-
Forests will support many more mesostigma-
ance; the lack of a litter layer; and com-
tid species than any other habitat, and as can
paction of the soil by farm machinery.
be seen from Table 6.3, the Gamasina and
• The Gamasina species that survive in the
Uropodina occur in much greater numbe~s
disturbed and compacted soils used for
and are more speciose in grasslands than m
agriculture are relatively small in body size
agricultural fields. Thus, the nematophagous
and have a high reproductive capacity.
activity that has been observed in natural
• Pesticides toxic to arthropods or their
environments does not necessarily occur in
prey (e.g. aldicarb) have much the same
the soils used for agriculture.
effect as soil compaction, reducing the
Of the two groups of mesostigmatids
Gamasina to an assemblage dominated
mentioned above, the Uropodina are the
by one or two species.
least important from an agricultural per-
• The Gamasina are a good indicator of soil
spective, as they are only found in large
health. A healthy agricultural soil should
numbers in organic materials such as com-
contain a diverse range of Gamasina spe-
post, manure, older sewage sludge, decay-
cies that are adapted to different habitats.
ing wood and deciduous forest litter. Thus,
Such a community would contain surface
they are not abundant in most agricultural
dwellers; species that live in organic
soils. Some genera of Uropodina are myco-
accumulations; species that survive read-
phagous, but most feed on nematodes and
ily in upper soil layers; and euedaphic
insect larvae. Their distribution is highly
species capable of living in deeper soil to
specific, as they are only found in rich
depths of 20 em.
organic habitats where populations of bact~­
rivorous and fungivorous nematodes will
always be high. Since such habitats are usu- Management to enhance
ally ephemeral, the mites must disperse to microarthropod abundance and
fresh sources of organic matter when decom- diversity in agricultural soils
position is complete.
The Gamasina are much more important
Since soil microarthropods are unable to
predators in agroecosystems, and a review by
make their own burrows, they are entirely
Koehler (1999) provides a good summary of
dependent on air-filled pores that are at least
their biology and ecology. The most import-
as large as their body width. Their abundance
ant observations made in that review are:
is, therefore, closely linked to soil physical
• The majority of Gamasina are mobile conditions, particularly the volume of habit-
predators. They utilize chemical or tactile able pore space and the connectivity of soil
stimuli to locate their prey, pierce or cut pores. However, when soil is used for agricul-
the body with their chelicerae, produce ture, soil structure is markedly altered due to
Generalist Predators of Nematodes 179

tillage and compaction from farm machinery. continuous inputs of organic matter; no till-
Bulk density increases and total porosity age; and controlled traffic. That knowledge
declines, and these structural changes not also indicates that this package of require-
only affect aeration, water movement, solute ments must be adopted in its entirety if soil
transport, nutrient availability and root growth, structure is to be optimized, as all components
but also reduce the living space for micro- are important for the following reasons.
arthropods. Thus, changes in the physical
structure of soils are almost certainly one of • A cover of mulch or plant residues on the
the main reasons that microarthropods are soil surface provides a habitat that is similar
not abundant in many of the soils used for to the litter layer or 'forest floor' environ-
agriculture. ment of natural ecosystems, which is domi-
Two studies provide a good example of nated by microarthropods. It also increases
the impact of soil porosity on microarthro- the population density and activity of micro-
pods. In the first, populations of various arthropods by dampening moisture and
groups of microarthropods were monitored temperature fluctuations (Badejo et al., 1995).
at sites in the Netherlands that varied in soil • Organic inputs from crop residues and
type and land use, and relationships between roots are the energy supply for the bac-
biomass, organic matter and pore size distri- teria and fungi that enmesh soil particles
bution were examined (Vreeken-Buijs et al., into aggregates; and for the earthworms,
1998). In general, microarthropod biomass enchytraeids and other ecosystem engi-
was higher in sandy soils than in loamy soils, neers that create the voids and macropo-
and higher in grasslands than in wheat fields. res required by microarthropods. Plant
Analyses of data from the grassland sites roots also make a contribution by imp-
showed that biomass of the four principal fun- roving subsoil macroporosity, a process
ctional groups of microarthropods was nega- that has been termed 'biological drilling'
tively correlated with the smallest pore size (Cresswell and Kirkegaard, 1995).
class {<1.2 J.llll.), while biomass of three of the • Eliminating tillage is essential because it
groups (predatory mites, non-cryptostigm.atic accelerates soil carbon losses, eliminates
mites and omnivorous Collembola) was posi- earthworms and large invertebrates, des-
tively correlated with the largest class (>90 J.llll.). troys soil aggregates, and disrupts the
In a second study carried out in the labora- fungal hyphae responsible for aggrega-
tory, soil was compressed to six levels of bulk tion. Tillage is particularly harmful to
density (1.02-1.56 g/cm3), and populations of microarthropods because its main nega-
three species of Collembola were found to be tive impacts are on the upper 20 em of the
reduced by compaction due to the loss of soil profile, their primary habitat.
coarse pores (> 120 ~). The data obtained • Farm machinery must be confined to traffic
from bulk densities typically found in wheel zones to minimize compaction problems.
tracks indicated that abundance was reduced Many soils become uninhabitable to micro-
by about 80°/o compared to loose soil (Larsen arthropods following a single pass with a
et al., 2004). tractor or other pieces of farm equipment.
Clearly, the only way to provide condi-
tions suitable for microarthropods in an agro- Although conservation tillage is now
ecosystem is to adopt a farming system that widely practised in some regions of the
preserves and enhances the soil's physical world, concern is sometimes expressed that
structure. Based on our knowledge of the role soil microarthropods do not always increase
of plants and organic matter in maintaining in abundance under no-till, particularly in
soil structure (see Chapter 2) and the manage- fine-textured soils. For example, ·a Japanese
ment practices required to improve soil health study in a humus-rich volcanic soil showed
(see Chapter 4), the key requirements for that no-till plots had more earthworms
achieving structural characteristics suitable and enchytraeids than conventionally tilled
for microarthropods in agricultural soils plots, but population densities of mites and
are obvious: permanent plant residue cover; collembolans were similar in both treatments
180 Chapter 6

(Miura et al., 2008). A review of 162 German (or any other soil organism) is that the
studies also showed that tillage adversely environment will always limit what is
affected earthworm populations, whereas the achievable. In a study at three sites in
response of microarthropods was dependent Western Australia, for example, Osler and
on soil texture (van Capelle et al., 2012). Murphy (2005) recovered relatively few spe-
Collembolans were not affected by tillage cies of oribatid mites from natural vegeta-
intensity in coarse-textured and silty soils, tion, and found that population densities
but were adversely affected in fine-structured were extremely low (440-1720 individuals/
loams. Although more work is required at a m 2). Only eight of the 22 species found in
local level to understand the reasons for these natural vegetation were recovered from
effects, a series of Australian papers (Bridge adjacent fields cropped with grains, legumes
and Bell, 1994; Bell et al., 1995, 1997, 1998) and pastures, and oribatid population dens-
are well worth 'consulting, as they address ities were generally reduced by more than
many of the issues involved in restoring the 80°/o. These low populations are undoubt-
physical fertility of fine-textured soils that edly a response to the relatively harsh envir-
have been degraded by decades of continuous onment at the study sites (hot dry summers;
cropping. annual rainfall of 355-420 mm; soils with
The studies cited focused on the phys- >80°/o sand and low levels of soil organic
ical and chemical fertility of ferrosols (kraz- matter), as oribatid populations are much
nozems) in a high-rainfall, subtropical higher and more speciose in more benign
environment. Ferrosols are some of the most environments. Thus, in any particular envir-
fertile soils in Australia, but after years of onment, climate and soil type will limit what
continuous cropping, they showed reduced improved agricultural management might
water infiltration rates, high bulk densities achieve. Nevertheless, data from natural
and increased penetration resistance. Organic vegetation provide a useful indication of
carbon levels were often as low as 10 g C/kg what may be attainable.
soil, or about 25°/o of the level in untilled soil, One of the reasons for attempting to
and this was associated with low aggregate increase microarthropod abundance and
stability, crusting of the soil surface and low diversity is to enhance the suppressive services
cation exchange capacity. Ley pastures were provided by the soil food web. Fortunately,
a useful tool in restoring the physical fertility there is some evidence that this is a worth-
of these soils, but the benefits were affected while approach, at least with regard to
by ley management (e.g. the pasture species, enhancing suppressiveness to plant-parasitic
ley duration and grazing management), as nematodes. For example, in a study of the
well as the tillage method used to return the nematode and arthropod communities in
ley area to cropping. The message to soil ecolo- conventionally and organically managed
gists from these studies is that when soils vegetable plots in California, predatory, omniv-
have been degraded by many years of in- orous and fungivorous mites were not
appropriate management, it takes more than only found to be more abundant in the
a change to no-till till and a few biomass- organic treatment, but also exhibited very
producing crops to correct the problem. In similar temporal patterns to predatory nema-
some soils, many years of careful nurturing, todes (Sanchez-Moreno et al., 2009). Since
and perhaps even a pasture phase, may be previous work had shown that suppressive-
required before there is any chance of re- ness to root-knot nematode was related to
creating a habitat suitable for soil micro- the prevalence of omnivore and predator
arthropods. In fact, it could be argued that nematodes (Sanchez-Moreno and Ferris,
the reappearance of large numbers of mites 2007), it seems that the pr~sence of organ-
and Collembola is a sign that soil physical isms at a high trophic level in the soil food
fertility has been restored. web is the critical issue with regard to achiev-
The other important point that must be ing a suppressive service. It may not matter
recognized when steps are taken to increase whether those organisms are mites, nema-
the number and diversity of microarthropods todes or some other generalist predator.
Generalist Predators of Nematodes 181

A study by McSorley and Wang (2009) mass of prey and predator, and the behav-
provided further evidence that plant-parasitic ioural response of prey to attack (Hohberg
nematodes are suppressed in soils with long and Traunspurger (2005)). More than 50 nema-
and complex food webs. Final populations of todes were consumed by M. richtersi per day
root-knot nematode (Meloidogyne incognita) on agar, but predation rates were reduced in
were 78-95°/o lower in natural soils from fine sand because small pores provided a ref-
Florida than in adjacent agricultural soils, uge for the prey. Follow-on work revealed
and suppressiveness was associated with the that the functional response of the predator
abundance of Collembola and mites. Given was best predicted by a model that accounts
that nematodes are an important food source for increasing satiation of the predator as it
for some groups of rnicroarthropods and are feeds over time (Jeschke and Hohberg, 2008).
consumed opportunistically by many others, During a study by Sanchez-Moreno and
such a result is not unexpected. The fact that Ferris (2007) on the suppressive services pro-
tardigrades were also more abundant in the vided by omnivorous and predatory nema-
suppressive soils is a reminder that the natural todes in California soils, it was observed that
soil biological community is complex, and naturally occurring tardigrades also had an
contributions from other members of that impact on the nematode community. This
community cannot be ignored. prompted further investigations which showed
that two tardigrade species (M. richtersi and
M. hannswortht) had the capacity to significantly
reduce nematode biomass (Sanchez-Moreno
Miscellaneous Predators of Nematodes et al., 2008). Populations of tardigrades var-
ied markedly between sampling times, prob-
Since nematodes are the most numerous mul- ably because they have the capacity to feed
ticellular organisms found in soil, it is hardly on bacteria, fungi, protozoa, algae, yeasts,
surprising that many groups of soil organ- nematodes, rotifers and plant roots, and are,
isms, other than those discussed earlier, have therefore, able to quickly respond to food
been reported to prey on nematodes. Small sources when they become available. How-
(1988) reviewed the isolated reports in the lit- ever, perhaps the most important result from
erature on predation of nematodes by proto- this study was that when the regulatory func-
zoans, turbellarians and tardigrades, and the tion provided by predatory nematodes disap-
contents of that review highlight how little peared due to predation pressure and/ or
we have learnt about some of these predators unfavourable environmental conditions, the
in the last 25 years. For example, a study of a suppressive service was maintained due to
turbellarian flatworm (Adenoplea sp.) by Sayre the high abundance of tardigrades. Thus, this
and Powers (1966) remains the only serious observation reinforces the point made earlier
study of this group of generalist predators. that if diversity and functional resilience is
Nevertheless, there has been a limited amount built into the soil biological community, nema-
of work on tardigrades and protozoans, and tode populations will always be subjected to
it has extended our knowledge of these regulatory forces.
organisms and provided a clearer picture of Small (1988) failed to mention copepods
their role in regulating nematode populations. in his review, but Muschiol et al. (2008) cited
Based on the observations of Hyvonen four reports of copepod predation on free-
and Persson (1996), in an experiment dis- living and plant-parasitic nematodes. These
cussed previously, tardigrades can be both authors then presented results of laboratory
predators of nematodes and prey for micro- experiments showing that Diacyclops bicuspi-
arthropods. Nematode--tardigrade interactions datus, a common copepod in northern regions
were later studied in a system where per cap- of the world, was a voracious feeder on nema-
ita feeding rates could be measured, and the todes. Starved copepods were able. to consume
results showed that consumption of nema- about 45 nematodes in 2 h, or the equivalent
todes by Macrobiotus richtersi depended on of 44o/o of their body mass. Although nor-
temperature, prey density, the individual body mally found in aquatic habitats, copepods also
182 Chapter 6

occur in soil, raising questions about their on soil nematodes is likely to be quite vari-
role as predators of nematodes in terrestrial able, and will depend on the properties of the
habitats. habitat, the feeding biology of the particular
Most reports of protozoan predation on earthworm species, and the composition of
nematodes have involved Theratromyxa the nematode community (llieva-Makulec
weberi, a naked amoeba with a feeding stage and Makulec, 2002). Enchytraeids are also
that can engulf nematodes in a few hours substrate ingesters, and although they may
(Small, 1988). However, Yeates and Foissner consume some nematodes during the feeding
(1995) observed that two testate amoebae process, their main food source is fungal
were also able to prey on large filiform-tailed mycelium, decaying organic matter and the
nematodes in forest litter. However, the microbes associated with it (Bardgett, 2005).
broader ecological significance of this finding
was uncertain, as the testacea and their nema-
tode prey may have been restricted to moist
open-textured habitats, and the food sources Generalist Predators as
of the amoebae and their capacity to cap- Suppressive Agents
ture relatively motile nematodes were not
assessed. Laboratory observations have also Based on the material presented in this chap-
shown that when the common soil flagellate ter, it should be apparent that the nematodes
(Cercomonas sp.) and the nematode Caeno- and microarthropods capable of preying on
rhabditis elegans compete for a bacterial food nematodes are also able to utilize many other
source, the nematode sometimes consumes food sources. Although individual taxa vary
the flagellate and becomes the dominant bac- in the range of organisms they consume and
terial predator, while in other situations the relative importance of nematodes in their diet,
flagellate attacks and kills its much larger the feeding habits of predatory invertebrates
competitor (Bjernlund and !Wnn, 2008). Thus, are best described by terms such as omni-
it is possible that interactions of this nature vorous, polyphagous or generalist. With regard
determine the relative importance of flagel- to food preferences within the nematode com-
lates and nematodes in the soil environment, munity, the prey chosen by invertebrates may
as both groups are always competing for the be influenced by factors such as the size and
same food source. motility of the victim, but most predators are
Small (1988) considered whether oli- relatively non-selective and are best considered
gochaetes were potential predators of nema- as generalists. Certainly there is little evidence
todes, and cited several papers which showed to suggest that they prefer plant-parasitic
that earthworms consumed nematodes or their nematodes over free-living species. This
eggs as they ingested their food, and that they generalist categorization also applies to the
sometimes markedly reduced populations of nematophagous fungi discussed in Chapter 5,
plant-parasitic nematodes. Most of those stud- as most have some capacity to live as sapro-
ies were also discussed in a later review by phytes, and very few parasitize or prey spe-
Brown (1995). However, it would be a gross cifically on particular nematodes.
misunderstanding to think of earthworms Given the huge number of organisms
as predators of nematodes. Earthworms may that reside in soil, and the fact that they com-
inadvertently consume nematodes that are pete with and prey on each other, multi-species
associated with plant litter, decomposing interactions are common. Diverse communi-
roots or humus (Hyvonen et al., 1994), but ties containing many different species share
their role as litter transformers and ecosystem common food resources and interact through
engineers means that they also modify soil complex networks of competition, parasitism
physical and chemical properties, soil water and predation. Plant-parasitic nematodes are
regimes and soil nutrient cycling processes one of the many parties involved, but the
to such an extent that they have many indir- effects of these interactions on this group of
ect effects on the nematode community herbivorous nematodes are difficult to predict
(Brown, 1995). Thus, the effect of earthworms because numerous trophic relationships may
Generalist Predators of Nematodes 183

occur simultaneously (e.g. intra-specific preda- may occur when several biological control
tion, intraguild predation and obligate agents interact with a plant-parasitic nema-
secondary predation). Intra-specific preda- tode. However, when soil organic matter and
tion involves cannibalism and is, therefore, other soil organisms are also included in the
easy to comprehend, but the other types of picture, the interactions depicted in the figure
interactions are more complex and are are even more complex, as the effects of preda-
depicted in Fig. 6.8. If these trophic webs tors on the target pest will be influenced by at
are viewed from the perspective of whether least the following factors: (i) predators may
the herbivore will be suppressed by its show some preference for free-living nema-
associates within the soil food web, it is todes over the plant parasite; (ii) the predators
clear that obligate secondary predation will and herbivores may be in different patches in
have an impact, as all biological control the soil profile, particularly if the organic mat-
agents are subject to parasitism or preda- ter is spatially separated from the root system;
tion. However, intraguild predation may (iii) the prey selected by the mononchid may
also influence the level of suppression, par- vary with its developmental stage; (iv) in some
ticularly in soil where a diverse range of situations the mononchid predator may be can-
hosts and prey is present, because many nibalistic; (v) if a suitable organic substrate is
predators will share a common prey (the available, the nematode-trapping fungus may
herbivore) and will also prey on each other. survive saprophytically; (vi) one nematode-
Rosenheim et al. (1995) used the trophic trapping fungus may impact on others thro-
web in Fig. 6.9 to show that intraguild predation ugh mycoparasitism; and (vii) the omnivorous

A B

Predator2 Predator 2 .....~.----~~..~ Predator 1

Herbivore Herbivore

t
Plant
t
Plant

c
Secondary predator Obligate hyperparasitoid Bacteriophage

t
Primary predator
t
Primary parasitoid
t
Bacterial pathogen

t
Herbivore
t
Herbivore
t
Herbivore

t
Plant
t
Plant
t
Plant

Fig. 6.8. Trophic webs demonstrating the distinction between intraguild predation and obligate secondary
predation. (A) Unidirectional intraguild predation, in which predators 1 and 2 share a common prey (the
herbivore), and predator 2 eats predator 1. (B) Bidirectional intraguild predation, which is the same as (A),
except that predators 1 and 2 eat each other. (C) Obligate secondary predation, in which the secondary
predator (which is shown as a secondary predator, an obligate hyperparasitoid or a bacteriophage) attacks
the primary consumer but does not attack the herbivore. Thus, the primary and secondary consumers cannot
compete for a common resource. {From Rosenheim eta/., 1995), with permission.)
184 Chapter 6

Schwiebia rocketti that attack the females and eggs of major


(mite) pests. The role of generalist predators as sup-

\
Arthrobotrys
pressive agents has received much less
attention. In the same way, entomologists
have concentrated on 'classical' biocontrol,
oligospora where populations of pests are reduced by
(fungus) \ specialist natural enemies, especially para-
sitoids. However, there is now renewed
rhossiliensis
interest in the long-recognized, but little
(fungus) exploited, background level of suppression
provided by assemblages of mainly gener-
t
Mononchus aquaticus
alist predators. A review of this subject by
Symondson et al. (2002) is, therefore, rele-
(nematode) vant. Although it mainly considers issues
associated with general predation on above-

Meloidogyne incognita
/ ground insect pests, many of the issues that
are likely to be critically important in the
(nematode) much more complex terrestrial ecosystem
are addressed.
t
Plant
The main disadvantage of generalists as
regulatory agents is that they do not respond
as well as specialists to an increase in prey
Fig. 6.9. lntraguild predation among biological density. Their functional response levels off
control agents of nematodes in soil ecosystems. The as they become satiated, and this response
nematode-trapping fungus Arthrobotrys oligospora may be further modified when alternative
has a broad host range and may attack both plant- prey become available. However, there are
parasitic nematodes such as Meloidogyne incognita
trade-offs between the respective merits of
and predacious nematodes such as Mononchus
aquaticus. Arthrobotrys oligospora may also be
specialists and generalists, and so the disad-
mycoparasitic, that is, it may parasitize other fungi vantages of generalists are offset to a great
such as Hirsutella rhossi/iensis. H. rhossiliensis does extent by the following features:
not attack other fungi but may parasitize both plant- • The polyphagous food habits of general-
parasitic and predacious nematodes. Finally, the
ist predators help sustain them when
mite Schwiebea rocketti eats both nematodes and
nematophagous fungi. (From Rosenheim eta/., pest populations are low.
1995, with permission.) • Populations of soil organisms will fluc-
tuate with temperature, moisture, season
of the year and many other factors.
Having a diverse range of generalist
mite may consume the two nematophagous
predators means that their function (pro-
fungi or the predatory nematode, or may sur-
viding suppressive services) will be
vive on alternative food sources within the maintained over time.
soil community. In such circumstances, it is
• Opportunistic feeding habits allow gen-
almost impossible to predict the outcome of eralists to rapidly exploit a food resource
these interactions, but what is clear is that the
that becomes available when pest popu-
two-species interactions often studied by
lations increase.
biological control researchers are a highly
• Generalists may drive pests to extinction
simplistic version of what actually happens
at a local or microsite level, but because
in soil.
they have the ability to use alternative
Because of the difficulties involved in
foods, predator numbers do not neces-
studying numerous organisms in complex
sarily decline.
soil systems, research on biological control of
nematodes has focused on relatively specific Symondson et al. (2002) also collated
parasites (e.g. Pasteuria penetrans) and fungi data from more than 40 years of manipulative
Generalist Predators of Nematodes 185

field studies with insect pests, and used the these two groups should not be considered in
results to show that single generalist preda- isolation from perhaps the most important
tors, or assemblages containing several gen- generalist predators in soil: the nematopha-
eralists, reduced pest numbers significantly gous fungi. Thus, these concluding remarks
in about 75°/o of cases. They also discussed consider generalists collectively; reflect on
how predator populations might be manipu- their role in providing regulatory services;
lated to enhance pest control, and interestingly, and argue that high population densities and
mulching and no-till, two of the practices pro- diversity of these organisms provide an indica-
moted in this book as a means of enhancing tion that an agroecosystem is self-regulatory,
suppressiveness to plant-parasitic nematodes, and has the capacity to prevent pests such as
were found to be useful against insect pests. plant-parasitic nematodes from becoming
Although generalist predators clearly dominant. Comments are also made on the
have the potential to suppress populations of crop and soil management practices required
plant-parasitic nematodes, they will only do to develop self-regulating agroecosystems, and
so if they are co-located with the target nema- the need for soil ecologists, agricultural scien-
tode. Soil biological communities are distrib- tists and farmers to work more collaboratively
uted in patches centred on resources (either to improve current best-practice systems.
roots or organic matter) and communities in
different patches do not necessarily interact
(Ferris, 2010). Thus, there may be high popu-
lations of microarthropods, predatory nema- Generalist predators as indicators
todes and nematophagous fungi in an organic of ecological complexity and
litter layer or in the upper few centimetres of a capacity to suppress pests
the soil profile, but management practices
must ensure that they interact with plant-parasitic The nematode management component of
nematodes, which are mainly associated with this book is based on the premise that in a
roots further down the profile. Maintaining properly functioning ecosystem, any increase
ecosystem engineers such as earthworms and in the population density of a nematode pest
enchytraeids must, therefore, be an important will invariably be met with limitations that
management objective, because these organ- will be due to the actions of its natural enemies.
isms not only create macropores but also If that premise is true, and there is a plethora
move organic materials from the surface into of evidence to suggest it is, then the challenge
deeper soil layers. Since the microfauna and of agricultural management is to create an
mesofauna associated with decomposing active and diverse biological community
roots of previous crops provide a food source capable of providing this regulatory service.
for generalist predators, and the channels One way of looking at that task is to consider
they occupy are large enough to be occupied the natural enemies that should be key
by microarthropods, they must also be pre- components of that community. Although
served. Thus, the management challenge in nematologists tend to focus on omnivorous
annual cropping systems is to grow the next and predatory nematodes, I suspect that
crop in such a way that its roots, and the nematophagous fungi and microarthropods
plant-parasitic nematodes that are inevitably are much more important, as they are by far
associated with them, come into contact with the most numerous and diverse groups of
these microsites of predatory activity (see nematophagous organisms in undisturbed
also an earlier discussion with regard to soils. Since they have been reduced to low
nematophagous fungi in Chapter 5). population densities in most agroecosystems,
their collective abundance and diversity is
likely to be the best indicator of whether regu-
Concluding Remarks latory services have been restored and are
likely to be operating. Although there are
Although this chapter has focused mainly on dangers in singling out one or two groups of
predatory nematodes and microarthropods, natural enemies in complex ecosystems, the
186 Chapter 6

advantage of doing so is that it focuses the pests. Instead of using specialist biocontrol
mind on the specific practices required to agents as magic bullets, assemblages of native
enhance soil biodiversity. If nematophagous natural enemies are exploited as one of sev-
fungi and microarthropods are restored to eral regulatory mechanisms for controlling
agricultural soils, predatory nematodes, tar- pests. Other authors have used different terms,
digrades and many other natural enemies with Vandermeer (2011) referring to it as 'auto-
will also have returned. nomous biological control'. The approach is
Since all agricultural soils were mechani- the same, and is based on the premise that
cally tilled until the 1980s, and most are still the internal functioning of the ecosystem will
routinely cultivated, soil fungi are disadvan- result in the regulation of all potential pests.
taged relative to bacteria, and decomposition The ecosystem is constructed by the farmer in a
channels in the soil are generally bacterially way that autonomously keep~ the problems at
dominant. The widespread use of nitrogen bay. Note that regardless of the term used,
fertilizers has exacerbated this trend. Micro- ecological knowledge is being used to develop a
arthropods have also declined because the self-regulating agroecosystem, and that the key
soil voids that harbour them are no longer to success is the aptitude of the land manager.
habitable due to compaction, or have been The basis of conservation biological con-
destroyed by tillage. Additionally, the huge trol is that an increase in inputs of organic
decline in levels of soil organic matter that matter, together with a reduction in disturb-
has occurred since soils under natural vege- ance and various detrimental inputs, will
tation were converted to agriculture has result in an increase in populations of bac-
affected both groups of organisms: fungi no teria, fungi and numerous other soil organisms
longer have access to the substrates required that were referred to by Ferris et al. (2012a) as
to support their saprophytic activity, while amplifiable prey. These additional organisms
the loss of the energy source required by pri- provide resources for generalist and specialist
mary decomposers means that the food sup- predators in the system, and their greater
ply available to microarthropods is not only abundance will increase top-down pressure
reduced in quantity, but is also less diverse. on other potential prey: root-feeding organ-
Since the practices that must be changed to isms that were referred to as target prey. These
return fungi and microarthropods to agricul- authors then developed a simple model
tural soils are well known, the creation of (Fig. 6.10) to explain how a cascading system
soils with biological activity and complexity of amplification of predacious nematodes
resides in the hands of land managers. And could lead to the regulation of plant-feeding
the important point from a nematode man- nematodes. Although analyses of data obtained
agement perspective is that if that job is done from banana plantations in several countries
well, the end result will be a soil with an suggested that an increase in levels of ampli-
enhanced capacity to suppress plant-parasitic fiable prey resulted in greater predator pres-
nematodes. sure on the target prey, there were few
obvious relationships among links in the
above model. This led to a revised model
being proposed (Fig. 6.11) to accommodate
Conservation (or autonomous) more fully the numerous interactions that
biological control occur within the soil food web. The value of
such a model is that it encapsulates the key
In a review of the role of generalist predators elements of conservation biological control:
in agroecosystems, Symondson et al. (2002) (i) systems level regulation of soil pest species
referred to the pest management approach occurs when resources to predators are pro-
discussed in the previous paragraph as con- vided through a trophic web of carbon and
servation biological control. It is a process energy exchanges; (ii) the development and
that uses a range of habitat management and maintenance of an abundance of predators
diversification techniques to enhance natural requires either a consistent supply of food to
enemy numbers and their ability to suppress that trophic level or the presence of long-lived
Generalist Predators of Nematodes 187

Amplifiable prey

Microbial biomass

+
Plant roots

Fig. 6.10. Model of the cascading system of amplification of predacious nematodes leading to the
regulation of target prey through apparent competition. Regulation of the target prey becomes suppression
when the rate of flow from target prey to predators (a function of predator abundance and consumption
rates) exceeds the rate of increase in target prey biomass (a function of target prey abundance, growth rates
and resource availability). The triangles are regulator symbols indicating that flow down an arrow is
regulated or controlled by some factor that is not explicitly included in the model diagram. Impact
regulators marked A indicate the need for favourable conditions for sensitive predator species; those marked
B indicate the need for co-location of predators and prey. (From Ferris eta/., 2012a, with permission.)

Protozoa
~+
~
Microbial biomass

@ Nematophagous fungi
Rhizosphere bacteria

Fig. 6.11. An expanded model to reflect the importance of cascade diversion in a food web system that
leads to regulation of target prey through subtle apparent competition and functional complementarity.
See Fig. 6.1 0 for details of the regulator symbols. Expansions of the simple model depicted in Fig. 6.1 0 are:
E1 -resource diversion to other predators of the amplifiable prey which may also consume target prey;
E2- resource diversion to other consumers of amplifiable prey, including protozoa of which some may
consume target prey and some become resources for amplifiable prey; E3 - root associate nematodes are
stimulated by roots and organic matter; they contribute to the amplifiable prey and function as resources for
predators; E4- access of generalist predators to other resources besides amplifiable prey; ES- nematophagous
fungi are stimulated by roots and organic matter and are generalist predators of both target prey and
amplifiable prey; E6- rhizosphere bacteria stimulated by roots may have antibiotic and other effects on
target prey. (From Ferris eta/., 2012a, with permission.)
188 Chapter 6

predators with slow turnover rates; (iii) regu- are the building blocks on which sustainable,
lation will not occur unless predators and the self-regulating agroecosystems can be built.
target pest are co-located; and (iv) regulatory The key practices discussed here are not
services will decline if physical or chemical really contentious, as they form the basis of con-
constraints are imposed. servation agriculture, a farming system that is
already widely practised in some countries
(see Chapter 4). Thus, the challenge of the future
is to integrate the second-tier practices into such
Practices associated with developing farming systems, and understand how they
self-regulating agroecosystems influence the soil biological community. Critical
issues from an ecological perspective are
The management practices required to whether the move to conservation agriculture
enhance the regulatory services provided by has actually resulted in a more active and
the soil food web will not be discussed in diverse biological community; whether nutri-
detail here, as they are mentioned throughout ents and other inputs can be managed in ways
this book and are covered specifically in that benefit, or at least minimize any detrimen-
Chapters 11, 13 and 14. Instead, they have tal effects on key indicators such as nematopha-
been categorized into two groups and are gous fungi or microarthropods; and whether
listed below. the site-specific management practices associ-
ated with precision agriculture can be better
• Key practices. Permanent plant residue
utilized to avoid the biological diminution asso-
cover; a diverse rotation sequence; con-
ciated with excessive inputs of nutrients. With
tinuous inputs of organic matter; reduced
regard to the provision of suppressive services
tillage; and avoidance of compaction
against nematode pests, the key question is
through traffic control.
what level of suppressiveness has been gener-
• Second-tier practices. Biomass-producing
ated under current best practice, and is it suffi-
cover crops; inclusion of legumes in the
cient to reduce populations of the target
rotation; integrated crop and livestock
nematode below the damage threshold? Once
production; organic mulches; improved
the answer to that question is known, it will be
nitrogen use efficiency; optimized water
possible to decide whether other practices need
management; site-specific management of
to be integrated into the farming system to
inputs; and integrated pest management.
reduce losses from nematodes to acceptable lev-
Although all of the above practices are els. If that is necessary, practices that enhance
important, they have been separated into two the activity of specific suppressive agents could
groups because it is recognized that improv- be utilized, thereby providing an even more
ing a farming system is an incremental pro- effective and resilient form of suppressiveness
cess, and it is not feasible to implement all the (see Chapters 7 and 10).
desired practices at once. Nevertheless, the
five practices listed first are essential, as with-
out them it is impossible to produce a soil that
can harbour the fungi, microarthropods and The disconnect between agricultural
other organisms responsible for providing scientists, soil ecologists and
suppressive services. Roger-Estrade et al. the farming community
(2010) provided a thorough overview of the
biological benefits associated with reduced Over the last three decades, there has been a
tillage, but also pointed out that soil manage- major increase in research in soil microbial
ment involves much more than minimizing ecology, and the scientific literature is replete
or eliminating tillage. Compaction must be with books, reviews and papers on soil biodi-
prevented, diverse organic inputs from rota- versity, decomposition processes, the soil
tion crops are required, and crop residues food web, rhizosphere effects, microorganism-
must be managed effectively. Thus, the five invertebrate interactions and many other rela-
key practices must be adopted together. They ted topics. We now know much more about
Generalist Predators of Nematodes 189

the soil biological community than we did need to understand the impact of soil
30 years ago, but this knowledge has not been organisms on processes such as plant
translated into improvements in the way soil productivity in forests and grasslands,
organisms are managed on-farm. For example, plant species diversity, plant succession
research has shown that nematode pests and plant invasiveness. Also, the knowl-
can be suppressed by naturally occurring edge generated in natural systems can be
parasites and predators, and ecologists often utilized in agroecosystems. However,
indicate that biological suppressiveness is an disconnection occurs when ecologists
important ecosystem service, but most farm- fail to accept that agriculture is a man-
ers have no knowledge of these issues. They aged system. Some level of disturbance
assume that crop losses from nematodes are is inevitable when land is cropped or ani-
inevitable, and are usually not aware that mals are grazed, and so the biodiversity
nematodes have natural enemies that could that exists in natural systems will never
possibly provide an alternative to nemati- be recreated in an agroecosystem.
cides and resistant cultivars. • Ecologists often compare agricultural sys-
In my opinion, the above situation is the tems to undisturbed grassland. Again,
result of the detachment that exists between that is an understandable and acceptable
agricultural scientists, soil ecologists and the practice, but such research sometimes
farming community. The lack of interaction does not address ecological issues of
between the former groups is particularly importance to modem agriculture. For
concerning, and is manifested in some of the example, Postma-Blaauw et al. (2010, 2012)
issues outlined as follows. showed that various biological parame-
ters were detrimentally affected when
• Many agricultural scientists do not view land was converted from grassland to
agriculture from an ecological perspec- arable cropping. However, such a result is
tive. They focus on maximizing the pro- not surprising, given that the arable plots
visioning services provided by cropping were deeply and regularly tilled. What is
and livestock enterprises, and give little more relevant from an agricultural per-
thought to the many other services that spective is whether the same result would
an agroecosystem should provide. Their have been achieved if conversion had
understanding of the energy flows and been done in a less aggressive manner
nutrient cycling processes that occur (e.g. spraying the grassland with a herbi-
within agroecosystems is generally rela- cide such as glyphosate and then direct-
tively simplistic, and their knowledge of drilling the first and following crops).
soil biological processes is limited. This • ~the introductory sections of soil ecology
lack of detailed ecological knowledge, papers, or in reviews of the ecological
particularly as it relates to soil biology, literature, misleading statements are
means that agricultural scientists are often made about agricultural practices.
unlikely to read the ecological literature, The most common fault is to use the gen-
and rarely talk to soil ecologists. Much eral term 'pesticide' to cover the chem-
the same criticism could be applied to icals used against weeds, insect pests,
discipline-based specialists who work plant pathogens and nematodes, and
with soil. They tend to work with a lim- then imply that they are all detrimental
ited range of organisms, and their eco- to the soil biological community. Chem-
logical knowledge is often limited to icals need to be considered individually,
understanding how abiotic factors such as some will have negative effects and
as temperature or moisture influence others will have little impact. An insecti-
particular soilborne pests or pathogens. cide/nematicide such as aldicarb, for
• Much ecological research is conducted in example, will affect many components of
natural ecosystems and that is quite the soil biological community, whereas
understandable. These systems cover a the herbicide glyphosate is much more
large part of the earth's surface and we environmentally benign, binds tightly to
190 Chapter 6

soil constituents, and has little or no conducted in environments where dis-


effect on soil organisms at commercial turbance has been minimized for only a
rates (Haney et al., 2000; Weaver et al., few years. Observations made in such
2007; Duke and Powles, 2008). Of course, situations are simply not relevant to the
we always need to be on the lookout for many farmers who have been using some
subtle impacts (Zabaloy et al., 2012) or for form of conservation agriculture for more
long-term or cascading effects on soil than 20 years.
food webs (Helander et al., 2012), but • Intensification of agriculture is almost
such studies must be done with the invariably seen as a negative by soil eco-
knowledge that each chemical has differ- logists. Thus, the detrimental effects of
ent properties, and that effects will be increasing fertilizer and pesticide inputs are
influenced by rate of application and highlighted and the positives are generally
environmental conditions. ignored. Intensification can take many fonns,
• In the same way, fertilizers need to be and may involve: (i) increased plant diver-
considered individually. Nutrients are sity through crop rotation, cover cropping
exported when crops are harvested or or intercropping; (ii) nitrogen inputs from
farm animals are sold, and so they must legumes; (iii) higher carbon inputs through
be replaced if the agricultural system is greater biomass production, more intensive
to be sustainable. However, the ecological cropping, or the use of organic amendments
literature often argues that fertilizers or mulches; (iv) a reduction in the negative
are detrimental to the soil biological impacts of bare fallows by cropping more
community, and usually ignores the frequently; and (v) lower pesticide inputs
beneficial effects that arise from nutri- due to the adoption of integrated pest man-
ent inputs (e.g. increased biomass pro- agement. Land managers require more
duction and its flow-on effects to soil than a list of negative impacts: they need to
organic matter). The critical issue from know what type of soil biological commu-
an agroecological perspective is the nity is possible when the farming system is
type of biological community that can intensified under the best management
be sustained in systems where key crop practices currently available.
management practices are optimized
and fertilizer use efficiency is high. The disconnection between scientists with
Knowledge of the effects of different some understanding of soil ecology and the
formulations, application rates, timings farming community is another concern. This
and placement on various soil organ- issue was discussed in Chapter 4 and is a major
isms is also important, because it may impediment to progress. Closer collaboration
indicate how detrimental effects from between these groups would see farmers
fertilizers can be reduced. increasing their understanding of ecological
• Many papers written by soil ecologists processes, and soil ecologists becoming more
provide insufficient detail on the man- aware of the many variables that interact in
agement practices used in the farming farming systems. Fortunately, this has already
systems that were studied. Vague terms occurred in some regions of the world, with a
such as 'conventional', 'organic', 'inte- sustainable farming systems project in California
grated' or 'improved' are often used. To being one such example (Temple et al., 1994).
be useful to agriculturalists, authors must Additionally, there are excellent farmers in
provide specific information on tillage many countries who have long been committed
practices, herbicide usage, fertilizer inputs to the principles of ecological agriculture. Since
and the many other practices likely to they are now well down the pathway towards
influence the soil biota. enduring sustainability, soil ecologists with an
• Although soil ecologists agree that it takes interest in agriculture must make an effort to
many years to restore biological commu- learn from their experiences.
nities in agricultural soils, most ecological Earlier in this chapter and elsewhere in this
studies in agroecosystems have been book, the basic requirements for improving the
Generalist Predators of Nematodes 191

sustainability of farming systems, enhancing cropped fields tended to have more omnivor-
soil health and increasing suppressive services ous and predatory nematodes. The lower nema-
have .been discussed. To reiterate, the key prac- tode Channel Ratio in four of the five cropped
tices are permanent plant residue cover, a fields indicated that fungi were playing a
diverse rotation sequence, continuous inputs of greater role in the detritus food web in these
organic matter, reduced tillage and avoidance fields than in adjacent less-disturbed sites.
of compaction through traffic control. In most Additionally, Pratylenchus neglectus, the main
regions of the world, farmers can be found who nematode pest of cereals in southern Australia
have been using most, if not all of these prac- (Vanstone et al., 2008) was present, but popula-
tices for many years, and are now dealing with tion densities were relatively low in all of the
a range of second-tier improvements to their cropped soils.
farming system. Since few research sites with The data presented below are encourag-
such histories are available, soil ecologists need ing, as they suggest that the biology of
to locate appropriate on-farm sites, study them cropped soils is not necessarily decimated by
intensively, and determine what is possible agricultural management. However, this con-
under best-practice management in specific clusion must be confirmed by assessing more
environments. My own experience in the grain- sites; by studying fungi, microarthropods
growing soils of southern Australia suggests and other soil organisms in more detail;
that it may be surprising what can be achieved. and by monitoring the temporal population
Based on the results of preliminary nematode dynamics of some of the biota. From a nema-
community analyses, soils managed using most tode management perspective, the critical
of the above practices for more than 15 years questions are whether the relatively low
were better in some respects than adjacent soils populations of Pratylenchus observed in these
under grassland or natural vegetation (fable 6.4). preliminary samples result from biological
Free-living nematodes rather than plant para- suppressiveness, and if so, whether the regu-
sites dominated both land uses, but soils in latory service that has been established is

Table 6.4. Nematode communities at five sitesa in South Australia where grain-growing soils had been
subjected to minimum-till, residue-retained management for more than 15 yearsb, and in adjacent
undisturbed areas maintained as grassland or natural vegetationc.

Nematodes/g soil

Pratylenchus Total free-living Nematode


neglectus Dorylaimids Mononchids nematodes Channel Ratiod

Site Crop Natural Crop Natural Crop Natural Crop Natural Crop Natural

1 1.2 0.3 0.26 0.16 0.020 0 12.7 13.2 0.41 0.78


2 0.2 0.2 0.12 0.25 0.028 0.010 14.2 14.5 0.50 0.73
3 0.1 0.1 0.39 0.19 0.000 0.008 12.7 14.2 0.66 0.79
4 2.6 6.4 0.48 0.42 0.031 0 14.6 13.0 0.73 0.58
5 0.4 0 0.23 0.03 0.016 0 9.8 9.3 0.70 0.95

aAII sites were in a Mediterranean climate (predominantly winter rainfall with hot, dry summers). Sites 1-4 were sandy clay
loam soils (chromosols or calcarosols) in areas with an annual rainfall of about 450 mm. Site 5 was a fine sand with an
annual rainfall of 260 mm. Sites were sampled in early April 2012, about 1 month before the next crop was due to be
planted. Data are means of three replicate samples from 0-15 em.
bCrops in the rotation sequence included wheat, barley, oats, canola and peas. None of the soils had been tilled for at least
15 years; crop residues were retained on the soil surface; weeds were managed with glyphosate and other herbicides; and
fertilizer inputs were determined on the basis of crop type, nutrients removed in the previous harvest and the results of soil
tests. Farm traffic was not controlled, so some soil compaction would have occurred.
cNatural sites were adjacent each cropped field and consisted of undisturbed grassland at sites 1-4; and natural vegetation
at site 5 consisting of mallee (Eucalyptus) with a Psilocaulon and Atriplex understory.
dNumber of bacterivorous nematodes/(number of bacterivorous + fungivorous nematodes)
(G.R. Stirling and K. Unsell, unpublished data)
192 Chapter 6

sufficient to maintain nematode populations farm traffic had not been controlled.
at levels that do not cause economic damage. However, there are fields in the same region
From the farmer's perspective, he or she that have been under minimum-till for
needs to know whether subtle changes to 25-30 years, and where controlled traffic
the rotation sequence, fertilizer placement or using GPS guidance was introduced in the
some other practice can further improve what last 5 years. Such sites provide opportunities
is currently considered a relatively produc- for soil ecologists to not only assess the bio-
tive and sustainable farming system. logical impact of what has been considered in
One problem with the sites chosen for this book as best-practice management, but
this study is that the cropped soils would also add value to what progressive farmers
have been compacted to some extent, as are already achieving.