Bulletin of Entomological Research (2006) 96, 637–645
DOI: 10.1079/BER2006467
Biodiversity vs. biocontrol: positive and
negative effects of alternative prey on
control of slugs by carabid beetles
W.O.C. Symondson1 *, S. Cesarini1, P.W. Dodd1,
G.L. Harper1y, M.W. Bruford1, D.M. Glen2·,
C.W. Wiltshire3 and J.D. Harwood1z
1
Cardiff School of Biosciences, Cardiff University, PO Box 915, Cardiff
CF10 3TL, UK: 2IACR-Long Ashton Research Station, Department of
Agricultural Sciences, University of Bristol, Long Ashton, Bristol,
BS41 9AF, UK: 3Arion Ecology, The Brambles, Stinchcombe Hill,
Dursley, Gloucestershire, GL11 6AQ, UK
Abstract
Environment-friendly farming techniques seek to increase invertebrate biodiversity in part with the intention of encouraging greater numbers of predators that
will help to control crop pests. However, in theory, this effect may be negated if the
availability of a greater abundance and diversity of alternative prey diverts
predators away from feeding on pests. The hypothesis that access to alternative
prey can lead to reduced pest suppression under semi-field conditions was
tested. Alternative prey type and diversity were manipulated in 70 mesocosms
over 7+ weeks in the presence of the carabid Pterostichus melanarius (Illiger),
a known predator of slugs, and reproducing populations of the slug Deroceras
reticulatum (Müller). Significantly fewer slugs survived where no alternative prey
were provided. Maximum slug numbers and biomass were found in treatments
containing either carabids plus a high diversity of alternative prey (many species
of earthworm and three of Diptera larvae) or a single additional prey (blowfly
larvae, Calliphora vomitoria Linnaeus). In these treatments slug numbers and
biomass were as high as in plots lacking predators. The effects of alternative prey
were taxon-specific. Alternative prey strongly affected carabid fitness in terms of
biomass and egg load. The fittest predators (those with access to high alternative
prey diversity or C. vomitoria larvae) reduced slug numbers the least. The mean
individual slug weights were greater in treatments with alternative prey than
where no alternative prey were provided to the carabids. These results suggest that
pests may survive and reproduce more rapidly in patches where predators have
access to alternative prey.
*Fax: +44 (0)29 20 874 305
E-mail: Symondson@Cardiff.ac.uk
·Honorary Professor of Cardiff University and independent consultant at Styloma Research and Consulting, Phoebe,
The Lippiatt, Cheddar, BS27 3QP, UK
yPresent address: School of Applied Sciences, University of Glamorgan, Pontypridd, Mid-Glamorgan, CF37 1DL, UK
zPresent address: Department of Entomology, University of Kentucky, S-225 Agricultural Science Center North,
Lexington, KY 40546-0091, USA
638
W.O.C. Symondson et al.
Keywords: Carabidae, Deroceras reticulatum, diet, generalist predators, predator
fitness, Pterostichus melanarius, slugs
Introduction
Alternative prey help to sustain and retain generalist
predators within crops when target pests are absent or at low
density. This dietary flexibility of generalists can, in theory,
give them a significant advantage over specialist natural
enemies, allowing them to be present within a crop early
in the year before the pests arrive in any significant numbers
(Murdoch et al., 1985; Chiverton, 1987; Chang & Karieva,
1999; Harwood et al., 2004). Certain agricultural practices can
encourage greater numbers of alternative prey during this
early period, allowing predators to reach high densities
by the time the crop needs to be protected from immigrating
or rapidly reproducing pests (Settle et al., 1996). Such
systems depend upon temporal separation between periods
of maximum alternative prey availability and periods of
pest abundance. In many circumstances this is probably not
achievable and practices such as conservation tillage
(minimal tillage systems including direct drilling that are
designed to conserve the soil (Köller, 2003)) are now
employed, in part, to maximize biodiversity (Kladivko,
2001), in the hope that this will foster a larger and more
diverse predator community that will go on to control the
pests. Empirical studies have shown that this is often an
effective strategy for increasing predator numbers (Stinner &
House, 1990), but the effects of mechanical operations
(cultivation, harvesting) on predators and their prey can be
complex and taxon-specific (El Titi, 2003; Holland &
Reynolds, 2003; Holland, 2004; Thorbek & Bilde, 2004). The
additional predators in minimal or no-tillage systems may
sometimes go on to increase predation pressure on pests, but
in other instances predator numbers, pest numbers and crop
damage may all increase (Stinner & House, 1990), a problem
that has been particularly noted with slugs (Kendall et al.,
1995; Symondson et al., 1996; Glen & Symondson, 2003).
A theoretical problem with the conservation tillage scenario
is that alternative prey may divert predators away from
feeding on target pests (Halaj & Wise, 2002; Symondson
et al., 2002a; Koss & Snyder, 2005; Rypstra & Marshall, 2005),
and the more numerous and diverse the community of
alternative prey, the more likely it would be that prey
choice would favour one or more of these alternative prey
species rather than the target pests. This may happen
through simple substitution (non-pest for pest) or through
switching behaviour as relative densities of prey species
change (Holt & Lawton, 1994). Food web theory suggests
that, within a more diverse system, many of those alternative
prey will be other predators, and that predation on each
other potentially decreases the ability of the predator
community as a whole to limit herbivore (pest) numbers
(Polis et al., 1989; McCann et al., 1998; Finke & Denno,
2004). And so the question remains, what happens when
farming systems encourage a numerous and diverse fauna
within a crop coincident with periods when pest density is
likely to be high? May the goals of encouraging alternative
prey and biodiversity, and seeking biocontrol of pests,
sometimes conflict? May not the fittest predators, replete
with alternative prey, be the least effective at controlling
pests?
Prey diversity has been shown to have a powerful effect
on predator nutrition, reproduction and survival. Greenstone (1979) suggested that predators seek to diversify their
diets in order to balance their amino acid requirements and,
more recently, Mayntz et al. (2005) demonstrated that
invertebrate predators are capable of selective foraging in
order to balance their intake of proteins and lipids. Other
studies have shown the benefits of a mixed diet, either to
balance dietary needs or to avoid prey toxins that affect
predator fitness (e.g. Toft & Wise, 1999; Oelberman & Scheu,
2002; Fisker & Toft, 2004). Importantly, however, beneficial/
detrimental effects of a mixed diet are taxon-specific. J.D.
Harwood, S.W. Phillips, K.D. Sunderland, D.M. Glen, M.W.
Bruford, G.L. Harper, and W.O.C. Symondson (unpublished
data) have demonstrated that both linyphiid spiders and
carabid beetles benefit from a diverse diet; for example
carabids fed a more diverse diet weighed more, laid more
eggs, continued to lay eggs for longer and the eggs
developed and hatched more rapidly. Carabids and spiders
fed on pests only (slugs or aphids) were the least fit. There is
some evidence that these effects translate to the field where
carabids in more complex habitats, with more diverse prey,
were larger and contained more eggs (Bommarco, 1998,
1999). Clearly, prey diversity, if exploitable by the predator,
improves predator fitness and between years this may lead
to increased predator numbers, even of univoltine species
such as carabid beetles. The predators may go on to limit
growth in pest numbers, although where the pests form a
substantial proportion of the total available prey, suppression may lead to subsequent limitation of predator densities
through loosely-coupled feedback mechanisms (Symondson
et al., 2002b). However, in the medium term (within a year)
univoltine carabids do not have time to respond numerically
to prey abundance and diversity. For flightless species such
as the ground beetle Pterostichus melanarius (Illiger) field
boundaries have been shown to be effective barriers to
movements (Thomas et al., 1998), preventing significant
aggregative responses to prey, although within-field aggregation to pest density can take place (Bohan et al., 2000;
Winder et al., 2005a,b). Thus, P. melanarius responses to
dietary components and prey diversity will be restricted to
the prey available in the fields in which they are sampled,
and the fitness of those predators will depend upon the
abundance and diversity of available food resources. Within
year, therefore, reproductive numerical responses will not
have time to operate, and spatial numerical responses will be
limited, restricting responses by the predators to alternative
prey to functional responses. If this is correct, then the
presence of alternative prey is likely to lead to reduced
predation on the target prey (slugs) (Harmon & Andow,
2004).
The carabid P. melanarius is a highly generalist predator
eating a wide variety of prey (Sunderland, 1975, 2002;
Symondson et al., 2000). However, Symondson et al. (1996)
found, using anti-slug antibodies and enzyme linked
immunosorbent assays, that over 80% of P. melanarius
captured in the field in one year contained slug proteins in
their guts, clearly demonstrating that slugs are a significant prey item. These carabids have now been shown, in
Alternative prey reduce predation on pests
semi-field and field experiments, to be capable of affecting
the temporal and spatial dynamics of slugs (Symondson
et al., 1996, 2002b; Bohan et al., 2000; McKemey et al., 2003,
reviewed in Symondson, 2004). We therefore tested the
hypothesis that, despite these high rates of predation by
P. melanarius on slugs reported in the field, when numerical
responses by the predators was prevented slug survival/
reproduction would be greater where alternative prey were
available to the predators. At the same time we tested the
hypothesis that alternative prey, and prey diversity, would
have a positive effect upon carabid fitness. We further tested
the hypothesis that the strength of this effect would be prey
taxon-specific. In addition, we tested the hypothesis that a
higher diversity of alternative prey would reduce still
further the ability of the beetles to limit slug numbers.
Overall, we wished to challenge the assumption that the
fittest beetles would be most effective at controlling pest
(slug) populations. Where reproductive numerical responses
are not possible, and immigration severely limited, as we
argue may often be the case in the field for this predator–
prey system, we would expect that functional response by
the beetles to the total prey available to lead to increased
survival of the pests in the presence of alternative prey.
We also tested the hypothesis that predation by the
beetles would affect the size structure of the slug population.
McKemey et al. (2001) demonstrated a preference for the
smallest slugs in laboratory trials, but could find no size
preferences where trials were performed, as here, in semifield miniplots (McKemey et al., 2003). If the beetles showed
a preference for smaller slugs, then treatments with the
fewest slugs at the end of the experiment (i.e. those subject to
the highest predation pressure) would be expected to have
the largest slugs.
Materials and methods
Experiments were conducted in outdoor mesocosms
(miniplots). These were circular plastic tubs (35 cm diameterr18 cm deep), with drainage holes around the base
covered with fine mesh to prevent invertebrates escaping or
entering. The surface area of soil in each mesocosm was
0.08 m2. The tubs were half filled with a mixture of steamsterilized sandy loam (50%), peat (30%) and grit (20%). Over
the summer a crop of spring wheat was grown in the tubs,
then harvested and cut to within a few centimetres of the soil
and experiments conducted on the stubble. The inner rim of
each plot was regularly painted with FLUON (polytetrafluoroethylene – Whitford Plastics, Runcorn, UK) to prevent
slugs (Symondson, 1993) and other invertebrates from
climbing out (McKemey et al., 2003). Each plot contained a
refuge for the beetles consisting of a piece of polystyrene tile
(10 cmr10 cm), weighted down with a stone to prevent it
from blowing away. The plots were protected by netting to
prevent birds from eating the predators or prey. The area
surrounding the plots was regularly treated with slug pellets
containing metaldehyde to destroy any other slugs in the
vicinity. Plots were watered as and when necessary to
maintain moist surface conditions and encourage slug and
earthworm activity.
There were seven treatments (table 1) with 10 replicate
plots for each treatment. Numbers of alternative prey per
mesocosm are shown in table 1. All treatments included
slugs, Deroceras reticulatum (Müller), at a density of 28 per
plot, equivalent to 350 m2, a high number but densities of
639
Table 1. Invertebrates added to each of 10 replicate mesocosms
for each of seven treatments. The target slug prey, Deroceras
reticulatum, were added to all plots (28 per plot), and carabid
beetle predators (two female Pterostichus melanarius per plot)
were added to the appropriate treatments.
Treatment
A
B
C
D
E
F
G
Prey species
Slugs
Slugs+beetles
Slugs+beetles+earthworms (E. hortensis) (50)
Slugs+beetles+Diptera larvae (C. vomitoria) (9a)
Slugs+beetles+earthworms (mixed speciesb)
(50)+Diptera larvae (three speciesc) (9a)
Slugs+earthworms (E. hortensis) (50)
Slugs+Diptera (C. vomitoria) (9a)
a
This number of larvae was added every week. Where three
species of Diptera were provided, three individuals of each
species were added each week. In every other instance the
invertebrates were added just once, at the start of the
experiment.
b
In this high diversity treatment mixed species of earthworms
(Allolobophora chlorotica, Aporrectodea caliginosa, Aporrectodea longa
and Octolasion cyaneum) were collected directly from the field.
Forty five of these mixed species were added, at random, to each
plot plus five Eisenia hortensis.
c
The three species were Calliphora vomitoria, Lucilia caesar and
Fannia canicularis.
Numbers of alternative prey introduced to each plot are given in
parentheses.
this order are reported from arable fields (Glen et al., 1988;
Symondson et al., 1996). Each of the 70 mesocosms contained
20 larger slugs, which had been collected directly from the
field, and eight neonate slugs, hatched in the laboratory. A
subset of 20 of the slugs from the field were weighed and
ranged from 125 to 415 mg (mean 214 mg, SE 24.9), while
neonate slugs were all between 2.2 and 3.3 mg. There were
three control treatments without predators: slugs only (A),
slugs plus the earthworms Eisenia hortensis (Michaelsen) (F)
and slugs plus Diptera larvae, Calliphora vomitoria Linnaeus
(G). These treatments were designed to measure background
rates of slug population increase and any possible effects of
other invertebrates (earthworms and Diptera) on slug
numbers. There were four treatments with beetles (B, C, D
and E, table 1) where two female P. melanarius were added to
each plot. Two beetles is a higher density than might usually
be encountered in the field but were used to compensate for
the expectation that at least one beetle might die during the
course of this prolonged experiment (in practice a mean of
1.45 beetles per plot survived, see Results). Treatment B
contained beetles and slugs only. Treatment C contained
beetles, slugs and the earthworms E. hortensis, and treatment
D contained beetles, slugs and the Diptera larvae
C. vomitoria. Treatment E contained the highest prey
abundance and diversity with slugs plus mixed earthworm species, together with three species of Diptera larvae,
C. vomitoria, Lucilia caesar Linnaeus and Fannia canicularis
Linnaeus. Although none of these species would be
commonly found as larvae in the soil they acted as a readily
available surrogate for the many species that are common in
arable fields, such as crane flies (Tipulidae), cluster flies
(Calliphoridae) and many species of Phoridae. The mean
weights of each species of Diptera larvae were found to be
(n = 10): C. vomitoria 99.4 mg (SE 3.10), L. caesar 39.7 mg (SE
640
W.O.C. Symondson et al.
1.34) and F. canicularis 24.2 mg (SE 2.15). Mixed earthworms
were collected from an arable field near Cardiff while it was
being ploughed. A subset were identified to species and
comprised Allolobophora chlorotica (Savigny) 27.8%, Aporrectodea caliginosa (Savigny) 30.6%, Aporrectodea longa (Ude)
19.4%, Octolasion cyaneum (Savigny) 2.8% plus unidentified
juveniles 19.4%. Earthworms were not weighed individually,
but a sample batch of 50 E. hortensis had a mean individual
weight of 0.93 g while a batch of 50 mixed earthworms
collected from the field had a mean individual weight of
0.331 g. The P. melanarius beetles were obtained by pitfall
trapping in a field of winter wheat.
Slugs and earthworms were introduced to the plots,
directly from the field, over nine days. This was designed to
avoid potential problems caused by disease transmission
between invertebrates in the laboratory, especially the slugs
which are highly susceptible to the slug parasitic nematode
Phasmarhabditis hermaphrodita (Schneider) (Wilson et al., 1993)
and the pathogen Microsporidium novacastriensis (Jones &
Selman) which debilitates D. reticulatum in laboratory
cultures (Jones & Selman, 1985). The beetles were then
weighed and introduced to the plots on 12 September 2003,
along with (in appropriate treatments) the first batch of
Diptera larvae (table 1). Diptera larvae, unlike the other prey,
were added weekly because otherwise they would have
pupated, hatched and escaped. After 12 days, when
temperatures began to fall (which would have limited beetle
activity), the plots were moved to a glasshouse with
temperature control. During the 12 days outdoors the mean
minimum temperature was 11.6 C (SE 1.15, lowest 2.7 C)
and the mean maximum 20.8 (SE 0.91, highest 24.9 C).
During the 40 days under glass the minimum temperature
(on every day) was 16 C, controlled by a thermostat
and heater. The mean daily maximum was 25.2 C (SE 0.51,
highest 32 C). Weeds growing in the plots were regularly
removed mainly to prevent them from providing escape
routes for predators and prey, but also because they were
found to attract aphids.
After the experiment had been running for five weeks,
any beetles found under refuges were collected and frozen.
Where one or no beetles were found we did not know at that
stage whether the beetles were still present in the plots,
buried in the soil, or whether they had died. After three days
of checking under the refuges, 35 of the plots were gradually
flooded over 10 days, forcing the slugs and any remaining
beetles to the surface. This technique is considered the most
accurate method for assessing slug populations (Glen et al.,
1989; Symondson et al., 1996). Each slug was identified and
weighed. The process was repeated with the remaining 35
plots 14 days later. The plots were processed in two batches
because the flooding unit could not accommodate all 70 at
once. Each batch contained five replicates of each treatment.
Initial analyses of the data treated these two batches as
separate blocks in analysis of variance (ANOVA) but, as
there were no significant differences found for slug numbers,
biomass and mean size data (P > 0.2), ‘block’ was excluded
from subsequent analyses.
All beetles were weighed and frozen as soon as they were
collected from the plots. They were then dissected and their
egg loads recorded. At the end of the experiment 21 plots
still contained two beetles, 16 contained one and just three
had no live beetles. We cannot rule out the possibility that
some beetles may have drowned, and thus failed to come to
the surface, during gradual flooding. All plots were included
in subsequent analyses, regardless of how many beetles were
found. As the error caused by loss of beetles from some plots
through mortality would have reduced our chances of
finding differences between treatments, any remaining
significant differences would have had to have been strong
to be detectable. The large number of replicates per treatment (10) was designed to minimize this predictable
problem.
Data were analysed by ANOVA, with data transformed
when necessary to stabilize variances. Where ANOVAs were
significant, means were compared using Least Significant
Differences (LSD for P £ 0.05).
Results
The numbers, biomass and mean weight of slugs
extracted from the mesocosms at the end of the experiment
are shown in fig. 1. Overall the treatments had a significant
effect on slug numbers (F6, 63 = 4.59, P < 0.001) and total slug
biomass per plot (F6, 63 = 5.83, P < 0.001). There was no
significant difference between the three treatments without
beetles, showing that neither earthworms nor Diptera were
directly affecting slug numbers. Fewest slugs were (and
lowest slug biomass was) recovered from plots with slugs
and beetles only. Plots with slugs and beetles contained
significantly fewer slugs (and lower slug biomass) than plots
with slugs only, showing that the beetles were reducing
slug numbers. However, where there were additional prey
species in treatments D (slugs, beetles and C. vomitoria
larvae) and E (the highly diverse diet treatment with slugs,
beetles, mixed earthworms and mixed Diptera larvae), the
plots contained significantly greater numbers and biomass of
slugs than plots with slugs and beetles alone, demonstrating
that alternative prey were diverting the beetles away from
feeding on slugs. However, treatment C (slug, beetles and
E. hortensis), did not contain a significantly greater number
or biomass of slugs than plots with slugs and beetles only.
The presence of beetles in treatment D (slugs, beetles and
C. vomitoria) did not reduce slug numbers and biomass
significantly compared with treatment G (slugs and
C. vomitoria but no beetles), suggesting that these Diptera
were diverting the beetles away from feeding on slugs.
However, beetles in treatment C (slugs, beetles and
E. hortensis) did reduce slug numbers and biomass compared
with treatment F (slugs and E. hortensis but no beetles), again
suggesting that this species of earthworm was not significantly diverting the beetles from preying on the slugs.
In addition to slug numbers and biomass, we analysed
mean slug weights to see whether these varied between
treatments at the end of the experiment. Overall, there were
significant differences between treatments (F6, 63 = 3.28,
P = 0.007). Treatment B (slugs and beetles only) contained
significantly smaller slugs than in any other treatment
(fig. 1c). Few, if any, of the adult slugs had survived to
the end of the experiment and the mean size of slugs
extracted from all treatments was much smaller than the
mean size introduced to plots. In treatment B (slugs and
beetles only) the mean size was that of very small neonates
(back-transformed mean 1.5 mg). There was no significant
difference between the remaining treatments, with a pooled
back-transformed mean of 7.2 mg, still very small but r4.8
larger than in treatment B.
Two measures of predator fitness, beetle biomass and egg
load, were analysed. At the beginning of the experiment
Alternative prey reduce predation on pests
3
2.5
a
LSD
2
1.5
1
0.5
0.2
0.15
0.1
0.05
6
5
LSD
0
4
b
25
3
2
20
1
Egg number
Loge ind. slug weight (mg)
c
Loge tot. slug biomass (mg)
0
b
0.25
LSD
Beetle weight (g)
Loge slug number
a
641
0
3
2.5
LSD
LSD
15
10
5
2
1.5
0
1
0.5
0
A
B
C
D
E
F
B
C
D
E
Beetles
Beetles
Worms
Beetles
Beetles
Worms+
Diptera+
Diptera
G
Beetles Beetles Beetles Beetles
Worms+ Worms
Worms
Diptera Diptera+
Diptera
Treatments
Fig. 1. Mean numbers (a), total biomass per plot (b), and mean
individual weights (c) of slugs (Deroceras reticulatum) in seven
mesocosm treatments at the end of the experiment (n = 10 per
treatment). Slugs, D. reticulatum, were added to all plots, while
additional prey added are indicated. ‘+’ indicates multiple
species. For full details of treatments A–G see table 1. LSD bars
are for P £ 0.05.
there was no significant difference between the weights of
beetles in the different treatments (F3, 76 = 0.23, P = 0.879).
However, by the end of the experiment there were highly
significant differences (F3, 33 = 13.44, P < 0.001) (fig. 2a), with
significantly greater beetle biomass in treatments D (beetles,
slugs and Diptera) and E (beetles, slugs and diverse prey)
than in treatments B (beetles and slugs only) and C (beetles,
slugs and the worm E. hortensis). Similarly, analysis of the
egg loads within these beetles showed highly significant
differences (F3, 33 = 16.19, P < 0.001) (fig. 2b) with beetles in
treatments D (beetles, slugs and Diptera) and E (beetles,
slugs and diverse prey) containing significantly more
eggs than beetles in treatments B (beetles and slugs only)
and C (beetles, slugs and the worm E. hortensis). Beetle
weights at the end of the experiment were highly correlated
with egg load (beetle weight = 0.167+0.0025 egg load, r2
58.3%, P < 0.001).
A number of regression analyses were performed to
examine the relationship between slug numbers and biomass
per plot at the end of the experiment and beetle fitness
Treatments
Fig. 2. Graphs of measures of beetle (Pterostichus melanarius)
fitness at the end of the experiment in terms of mean numbers of
eggs within the beetles (a) and beetle weights (b). Slugs,
Deroceras reticulatum, were added to all plots, while additional
prey added are indicated. ‘+’ indicates multiple species. For full
details of treatments A–G see table 1. LSD bars are for P £ 0.05.
(table 2). Overall, the fitter the beetles (in terms of weight
and egg load at the end of the experiment) the greater the
number and biomass (per plot) of slugs surviving. Relationships between beetle fitness parameters and mean individual
slugs weights at the end of the experiment proved to be nonsignificant once missing data (plots with zero slugs) were
removed from the analyses.
Discussion
This carabid, P. melanarius, has been shown in many
previous studies to feed on slugs in the laboratory
(Symondson, 1997; McKemey et al., 2001; Oberholzer &
Frank, 2003; Oberholzer et al., 2003), microcosms and
miniplots (Buckland & Grime, 2000, Thomas, 2002; McKemey et al., 2003) and field (Cornic, 1973; Tod, 1973;
Symondson et al., 1996, 2002b; Bohan et al., 2000; Dodd
et al., 2003; Harper et al., 2005), and together these results
provide clear evidence that they are killing, consuming and
in many cases reducing the number of these pests. This
experiment was designed to measure the effects of the
presence of alternative prey, and prey diversity, on the
ability of P. melanarius to limit slug numbers when numerical
responses were not possible. As might be expected, lowest
642
W.O.C. Symondson et al.
Table 2. Relationships between beetle weights and egg loads, at the end of the experiment, with
slug numbers and biomass.
Response (Y)
Beetle weight
Beetle egg load
Predictors (X)
Loge
Loge
Loge
Loge
slug
slug
slug
slug
number
biomass
number
biomass
residual slug numbers and biomass were found in the
treatment where there were no alternative food resources
(B, beetles and slugs only). In all other treatments containing
P. melanarius, residual slug number and biomass were
greater (fig. 1) in most cases significantly so, providing
direct evidence that the presence of alternative prey reduced
the rate of predation on slugs. The one exception was
treatment C (beetles, slugs and the worm E. hortensis), where
the earthworms E. hortensis were provided as alternative
prey. Eisenia hortensis is closely related to Eisenia fetida
(Savigny), a species known to generate defensive chemicals
within coelomic fluid exuded by dorsal pores when attacked
(Sims & Gerard, 1985). It is possible that such deterrent
chemicals exist in E. hortensis and are effective against
P. melanarius, especially, as here, where the carabids have the
option of eating other prey, the slugs, instead. At the end
of the experiment, beetles in treatments with slugs plus
E. hortensis were no fitter (in terms of their biomass and
egg loads) than beetles in plots with slugs only, possibly
suggesting that these two prey species were of approximately the same quality to the predator. The only significant
effect of the presence of E. hortensis was on slug size; slugs
with beetles only were significantly smaller at the end of the
experiment than in any other treatment, including treatment
C ((beetles, slugs and the worm E. hortensis)), suggesting that
predation pressure on the slugs may have been marginally
lower where these worms were present.
In the two other treatments that included predators plus
alternative prey, treatment D (beetles, slugs and Diptera)
and treatment E (the high prey diversity treatment), slug
numbers, biomass and mean weight were all significantly
greater than where slugs alone were present with beetles. In
addition, beetles in treatments D and E with alternative prey
were the fittest, with significantly greater predator biomass
and egg loads. The latter two are likely to be correlated as
beetle weight is affected by egg load, and this proved to be
the case. There was no evidence that the high diversity
treatment had any different effect on predation on slugs or
predator fitness than the one incorporating just slugs and fly
larvae. Fly larvae and pupae are used commercially (e.g.
GAB Biotechnologie GmbH) as a complete diet for rearing
carabid larvae such as Poecilus cupreus (Linnaeus) and have
been used to maintain P. melanarius adults in the laboratory
for over a year (W.O.C. Symondson, unpublished data). It
is likely that a diet of slugs plus C. vomitoria contained most
of the nutritional requirements of these beetles and a more
diverse diet provided no significant additional benefit.
Theory suggests that predators presented with an abundant
and diverse diet should be more selective, taking the most
profitable prey (Pyke, 1984; Stephens & Krebs, 1986), which
in this case may have been the Diptera larvae. By contrast,
a diet of slugs plus E. hortensis was significantly worse than a
highly diverse diet, showing that there is a taxon-specific
Equation
r2 %
Probability
Y = 0.170+0.0171 X
Y = 0.239+0.0104 X
Y = 3.06+5.85 X
Y = 25.5+3.22 X
25.2
24.6
31.5
25.3
P = 0.002
P = 0.002
P < 0.001
P = 0.002
interaction between dietary quality and diversity, as shown
previously by Toft & Wise (1999), Oelberman & Scheu (2002)
and Fisker & Toft (2004).
Our experimental design was not, in retrospect, ideal
with respect to the high/low diversity comparison. We did
not realize beforehand that E. hortensis would prove to be a
non-preferred prey item and therefore the comparison
between high and low diversity of worms was confounded
by this factor. Molecular analyses using both monoclonal
antibodies and DNA primers have shown that earthworms
are frequently the largest component of the diet of
P. melanarius, but these techniques did not distinguish
between predation on different species (Symondson et al.,
2000; Harper et al., 2005 and unpublished data).
In a previous miniplot trial, under similar conditions,
McKemey et al. (2003) could find no significant difference in
predation rates on different size classes of slugs. It was
concluded that the preference shown in the laboratory for
smaller slugs (McKemey et al., 2001) was counteracted by
environmental heterogeneity, which provided a greater
number and diversity of refugia for the smaller slugs.
However, in the current experiment this seems to have gone
one step further, with the smallest slugs found in the
treatment subject to the greatest predation pressure (treatment B, slugs and beetles only). The mean size of the slugs
was, at 1.5 mg, smaller than the smallest slugs used in
McKemey et al. (2003) and it is probable that these neonate
slugs were either overlooked by the predator or found
numerous refugia in the soil and within the stems of the
wheat stubble. Many other studies have shown that there is a
lower size threshold below which predators ignore prey (e.g.
Greene, 1975; Finch, 1996).
The length of the experiment was designed to allow time
for the slugs to reproduce. The size of the slugs recorded at
the end of the experiment suggests that most hatched from
eggs laid by adults during the experiments and that,
following egg laying, most adults died. Predation on slug
eggs, as well as neonates, was possible (Oberholzer & Frank,
2003; Symondson, 2004) but could not be tracked.
The use of LSD to define post-ANOVA differences
between treatment means is widely used, but often restrictions are placed on the number of comparisons that are
allowable, usually x-1 where x is the number of treatments
(e.g. Fry, 1993). However, often more a priori comparisons
are ecologically justified, especially where more than one
control is used (as here). It has been argued that where more
than x-1 comparisons are made, Bonferroni adjustments are
necessary. However, this has been strongly criticized in
recent papers by Perneger (1998) and Moran (2003), who
argue that Bonferroni is too conservative, and that the more
treatments that are included in the experiment, and the more
controls there are in place (normally considered a good
thing), the greater the chances that type II errors will occur
Alternative prey reduce predation on pests
(i.e. real significant differences will be missed). Moran (2003)
argues that this is particularly relevant to ecological studies,
where variances are usually high. Both authors argue for
simply presenting the data, pointing out where significant
differences lie (as here, with an LSD bar), and leaving
interpretation to the reader. We have followed this policy.
All of the comparisons we made were, a priori, predictably
meaningful.
We accept that the definition of ‘fitness’ used in this
paper is limited, given that the experiment ran for only a few
weeks and we do not know what longer-term consequences
greater beetle weight or egg load would have on survival or
reproduction. Nevertheless, there were significant associations between these measures of fitness and slug number
and biomass in the plots. These analyses show that
the beetles that were fittest had the least impact on slug
populations and were found in association with the highest
residual numbers of slugs. Although predictable from our
results, and an effect of treatment rather than fitness per se,
this may appear counter intuitive and could easily lead to
misinterpretation of data from the field. Spatial associations
between generalist predators and a target prey species in the
field may be interpreted in very different ways. If predator
and target prey numbers are positively spatially associated it
might be concluded that the predators are aggregating to the
prey in order to feed on them (Symondson et al., 1996; Bohan
et al., 2000; Winder et al., 2005a,b). However, if high predator
density is associated with low prey density this may also be
seen as evidence of high predation pressure (prey density
has been reduced by the predators) (Bohan et al., 2000).
In practice one would expect transient dynamics with lag
phases, such that highest predator density is associated with
previous, rather than current, prey densities, as found by
Winder et al. (2005a). Both interpretations could be true
under different circumstances, but availability of alternative
prey is rarely, if ever, considered as the primary factor
driving the observed dynamics. Our results suggest that an
equally valid interpretation of the same data might be that
pest species may survive and reproduce more rapidly in
patches where the predators are feeding on alternative prey.
This would be predictable from theory (Harmon & Andow,
2004) in that the predators are reproducing on an annual
time scale, but responding to total prey on much shorter
timescales, primarily in terms of functional responses.
Symondson et al. (1996) found greater numbers of slugs and
P. melanarius in long-term no-tillage plots compared with
plots that had been subjected to various forms of tillage over
many years. Analysis of the beetles’ gut contents using
antibodies showed that where there was greater slug
biomass in the soil each beetle was eating greater quantities
of slug. However, ratio-dependent predation pressure on the
slugs in the no-tillage plots must have been lower, because
by September (just before cultivation and therefore an effect
of treatments applied one year previously) there were
1.8 times as many beetles in the no-tillage plots compared
with those that were tilled, but 91 times more slug in terms
of biomass. The beetles in the no-tillage plots were the best
fed, with the greatest fore-gut biomass, but apparently the
least capable of limiting slug numbers. It is probable that
prey in general were more numerous and diverse in the
no-tillage treatment, as has been found in many other studies
(Stinner & House, 1990; Kladivko, 2001; Holland, 2004), and
that as a result the slugs in this treatment were under the
least predation pressure.
643
This simple plot experiment must, however, be interpreted with caution. It does not, for example, tell us anything
about how much alternative prey will be available in the
field or how temporal change in alternative prey availability
might affect predator–target prey interactions (e.g. Settle
et al., 1996). Although the plots were designed to emulate
field conditions, they inevitably restrict the movement
patterns of predators and prey as well as the choice of prey
available. Nevertheless, we believe the implications for
interpretation of field data are profound. Our results suggest
that future field studies of interactions between generalist
predators and particular prey species should ideally monitor
consumption of alternative, competing prey (Symondson
et al., 2000; Agustı́ et al., 2003), which is now possible using
one of the molecular approaches now being applied in the
field (Symondson, 2002; Sheppard & Harwood, 2005;
Sunderland et al., 2005), especially multiplex polymerase
chain reactions (PCRs) (Harper et al., 2005). Examination of
just one small part of a food web, especially one involving
generalist predators, cannot be relied upon to reveal the
ecological processes leading to observed dynamics.
Acknowledgements
The authors wish to thank Ms Jenna Willis and Ms Clare
Armsworth for supplying the neonate slugs, Mr Simon
Shayler for identifying the fly larvae and, with Dr Samuel
Sheppard, helping to collect slugs, and Mr Lyndon Tuck for
recording temperatures and watering the mesocosms. The
authors also thank the Biotechnology and Biological Sciences
Research Council of the United Kingdom for funding this
work as part of a larger study of the effects of biodiversity on
biological control of crop pests.
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