Top-down control of prey increases with drying disturbance in ponds: a consequence of...

Top-down control of prey increases with drying

disturbance in ponds: a consequence of

non-consumptive interactions?

Hamish S. Greig1*, Scott A. Wissinger1,2 and Angus R. McIntosh1

1School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand; and 2Biology

Department, Allegheny College, Meadville, PA 16335, USA

Summary

1. Biotic interactions are often expected to decrease in intensity as abiotic conditions become

more stressful to organisms. However, in many cases, food-web and habitat complexity also

change with abiotic stress or disturbance, potentially altering patterns of species interactions

across environmental gradients.

2. We used a combination of field assays and mesocosm experiments to investigate how dis-

turbance from desiccation moderates top-down control of prey by predators across a gradient

of pond duration in New Zealand.

3. Field manipulations of predator abundance in ponds led to an unexpected decrease in the

top-down control of prey biomass by predatory invertebrates as pond duration increased

(decreasing abiotic stress). Predatory fish, which are restricted to permanent ponds, had negli-

gible effects on prey biomass. Mesocosm experiments further indicated the consumptive

effects of fish are weak; a result that cannot be explained by an increase in physical habitat

refugia in relatively more permanent ponds.

4. Manipulations of invertebrate predator diversity in mesocosms (both substitutive and addi-

tive treatments), and the addition of olfactory fish cues, revealed that strong non-consumptive

effects of fish reduced predation by predatory invertebrates, and these effects overwhelmed

the positive influence of invertebrate predator diversity on prey consumption.

5. These results suggest that decreases in top-down control with increasing pond permanence

are likely a result of non-consumptive effects of fish weakening predation by invertebrate

predators in the more complex food webs of permanent ponds. Therefore, considering non-

consumptive effects of predators in complex food webs will likely improve the understanding

of biotic interactions across environmental gradients.

Key-words: Food-web complexity, interaction modification, intraspecific competition, multi-

ple predator effects, pond permanence, risk reduction, trait-mediated interactions

Introduction

Understanding how the strength of species interactions

changes with abiotic context is essential for predicting the

dynamics of ecological communities (Agrawal et al. 2007),

especially in response to changes along environmental gra-

dients. Several traditional models of community organiza-

tion predict decreases in the importance and intensity of

biotic interactions as abiotic conditions become more

stressful to organisms (Connell 1975; Grime 1977; Peckar-

sky 1983; Menge & Sutherland 1987). For example,

abiotic stress can mediate competitive interactions by

reducing densities of interacting species below resource

carrying capacities (Lubchenco 1980; Crain et al. 2004;

Gerhardt & Collinge 2007), and can weaken predation by

disproportionately influencing the abundance or effective-

ness of predators (Menge & Farrell 1989; Wellborn,

Skelly & Werner 1996).

Several authors have argued, however, that the effects

of abiotic stress on species interactions should vary

depending on environmental and community context*Correspondence author. E-mail: hamish.greig@canterbury.ac.nz

Journal of Animal Ecology 2013, 82, 598–607 doi: 10.1111/1365-2656.12042

(Chesson & Huntly 1997; Crain 2008). For example, phys-

ically benign habitats often have higher taxa diversity

within and across trophic levels and wider body size vari-

ation than disturbed habitats, and hence food webs with

more complex connections (Winemiller 1990; Jenkins,

Kitching & Pimm 1992; Walters & Post 2008). Omnivory,

intraguild predation (IGP) and non-consumptive effects

characteristic of these complex food webs weaken pair-

wise species interactions (Emmerson & Yearsley 2004;

Finke & Denno 2004); whereas the low diversity and

chain-like resource pathways of simple food webs charac-

teristic of disturbed or stressful habitats can strengthen

interactions (Power, Parker & Wootton 1996; Thompson

& Townsend 1999). Furthermore, organisms inhabiting

physically stressful environments often face life-history

constraints that force individuals to trade-off resistance to

biotic interactions with rapid development or efficient

resource use (Power, Parker & Wootton 1996; Wissinger

et al. 2006; Edwards & Stachowicz 2010). These trade-offs

may strengthen top-down control in disturbed habitats.

Finally, changes in habitat morphology along environ-

mental gradients such as habitat size, complexity and

refugia further complicate the community-wide outcome

of biotic interactions across environmental gradients.

Studies that incorporate these parallel and potentially

confounding community and habitat gradients are likely

to reveal more realistic effects of abiotic stress on species

interactions.

Here, we use a combination of field and mesocosm

experiments to investigate how shifts in food-web com-

plexity and habitat structure affect aquatic predator–prey

interactions across a gradient of pond drying disturbance.

The duration and frequency of drying and refilling vary

among individual ponds in a landscape, resulting in a

well-known gradient of abiotic stress across habitat

patches (Wellborn, Skelly & Werner 1996; Williams 1996).

Predator body size and diversity increases with pond

duration and fish are generally restricted to perennial

ponds (Schneider & Frost 1996; Bilton, Foggo & Rundle

2001). Subsequent increases in predation risk with pond

duration are often implicated in species turnover across

the pond permanence gradient (reviewed in Wellborn,

Skelly & Werner 1996; Wissinger 1999). However, pond

area, the abundance of macrophyte refugia (Urban 2004;

McAbendroth et al. 2005) and food-web complexity

(Wissinger et al. 1999) all increase with pond duration,

which may instead weaken community-wide predator–

prey interactions in more permanent ponds. Therefore, if

some predators are able to exploit temporary ponds

through rapid colonization or senescence, patterns of top-

down control of prey biomass across the habitat perma-

nence gradient may be reversed to be most intense in

short duration ponds (Brendonck et al. 2002).

We experimentally manipulated predator biomass in

natural ponds spanning a gradient of permanence to

investigate the influence of drying stress on the strength

of top-down control of prey biomass. We then conducted

two mesocosm experiments to distinguish the mechanisms

driving observed patterns of top-down control across the

natural pond permanence gradient. We first manipulated

the presence of macrophytes and predatory fish in meso-

cosms to examine the potential role of refugia in mediat-

ing predation on benthic invertebrates in permanent

ponds. A second experiment then used additive and sub-

stitutive manipulations of predator diversity (within and

between trophic levels) to determine the influence of

increasing food-web complexity on the strength of

top-down control.

Materials and methods

study sites and natural history

Lentic habitats in the Waimakariri and Rakaia River catchments,

South Island, New Zealand range in size from 2-m diameter

ephemeral pools to large lakes (up to 179 ha) that lie within

fluvio-glacial depressions (Wissinger, Greig & McIntosh 2009).

Pond hydroperiod (duration of inundation) strongly influences

species richness and community composition in the ponds, and

predator species richness, size and biomass increase with pond

permanence (Wissinger, Greig & McIntosh 2009). Most perma-

nent ponds contain small (< 200 mm) predatory benthic fish (Gal-

axias brevipinnis G€unther, Gobiomorphus breviceps Stokell), and

the larger lakes support low-density populations of longfin eels

(Anguilla dieffenbachia Grey), introduced brown (Salmo trutta L.)

and rainbow trout (Onchorynchus mykiss Walbaum) (Jeppesen

et al. 1997; Wissinger, McIntosh & Greig 2006). The biomass of

predatory invertebrate guilds is dominated by odonates in perma-

nent ponds, and beetles and small Anisops spp. backswimmers in

temporary habitats (Wissinger, Greig & McIntosh 2009).

assays of predator impact in natural ponds

Twelve ponds were selected for predator manipulations based on

their likelihood of retaining water throughout the duration of

experiments, and the presence of submerged vegetation in shallow

water (<60 cm deep). Five of those ponds contained predatory

fish (Table S1, Supporting Information). Visual monitoring of

pond hydrology began March 2005 when temporary ponds were

dry and from 12 October 2005 water depth was recorded hourly

in each pond with stage height data loggers (HT-100; TruTrack

Ltd., Christchurch, New Zealand) placed in the deepest possible

point of the pond basin. Pond permanence was quantified with a

multivariate index derived from principal components analysis of

three aspects of pond hydrology: duration (days) of inundation

following winter refilling, maximum proportion of total depth

lost over the observation period, and number of days inundated

per annum (to account for multiple drying and refilling events;

Table S1, Supporting Information).

In November 2005, we manipulated predator biomass in cages

(1�5 mm mesh on a steel wire frame, 0�25 m2 surface area, 50 cm

height) whose bottom edges were pushed into the sediment within

macrophyte beds and sealed with clay and fine gravel. Three

cages were placed 1 m apart in shallow water (mean depth � SE:

26 � 3 cm) in each pond, with each cage representing one repli-

cate of three different treatments: a ‘all predator reduction’ where

all fish and all predatory invertebrates captured in five sweeps

Disturbance increases top-down control 599

were removed from the cages, a ‘fish removal’, and an open ‘con-

trol’ cage (steel frame only) that allowed access to both predatory

fish and invertebrates. Predators were removed with five succes-

sive sweeps of a 1-mm mesh D-net through the water column

and benthic substrates. The contents of each sweep were trans-

ferred to sorting trays, predatory taxa were removed by hand,

and the remaining invertebrates and detritus were returned to the

cage. This procedure left submergent vegetation intact and

removed all fish biomass and 56 � 10% (mean � SE) of preda-

tory invertebrate biomass when compared with cages without

predator removal. The efficacy of predator removal was not influ-

enced by pond permanence (linear regression on % predator bio-

mass reduction, F1,10 = 1�74, P = 0�24). Predatory invertebrates

were classified as species that obtain the majority of their energy

through the consumption of other macroscopic animals. Small-

bodied predators that could move through the cage mesh (Liodes-

sus spp. beetles, mites and cyclopoid copepods) were not removed

in the manipulation. To control for prey mortality during the

predator manipulations, open-sided cages which represented

ambient levels of predation were covered in a temporary sleeve of

mesh and disturbed using the same procedures as above but with-

out the removal of predators.

After 2 weeks, small-bodied invertebrates (crustaceans, chiron-

omids, worms and molluscs) were subsampled in each cage with

five sweeps of a 500-lm mesh net through a PVC pipe (0�020 m2)

pushed into the substrate. Those subsamples were preserved in

70% ETOH and sorted in the laboratory under 109 magnifica-

tion. The remaining taxa in the cage were sampled with five

sweeps of a 1-mm mesh D-net, sorted on-site and preserved in

70% ETOH. Invertebrates were identified to tribe for Chironomi-

dae, family or genus for Crustacea, and to the lowest possible

taxonomic level (usually species) for remaining taxa. Biomass for

each taxon was calculated using length-dry weight regressions

(Benke et al. 1999; Stoffels, Karbe & Paterson 2003; H. S. Greig

unpublished data) on the body length measurements (ocular

micrometre at 10–209 magnification) of a random subset of 10

individuals from each sample. Dry weights were converted to

ash-free dry mass (AFDM) using taxon-specific estimates of %

ash (Benke et al. 1999, H. S. Greig unpublished data).

Predator impact (PI) on prey biomass was calculated using log

ratio of effect size (Berlow et al. 2004) calculated from the ratio

of prey biomass in unmanipulated predator treatments to prey

biomass in predator reduction treatments (Table 1). Fish PI was

determined by comparing invertebrate biomass in the open con-

trol cages with invertebrate biomass in the fish removal cages.

Predatory invertebrate PI was determined by comparing non-

predatory invertebrate biomass in fish removal cages with that

from the all predator reduction cages. Finally, comparisons of

non-predatory biomass between the open control cage and the all

predator reduction cages produced total PI (Table 1).

The effect of fish on prey biomass in permanent habitats was

analysed by comparing deviations of predator impact from zero

using a one-sample t-test for each of the three prey categories: all

invertebrates, all non-predatory invertebrates and ‘unprotected’

non-predators that did not have cases or shells. The effect of

pond permanence on the strength of predatory invertebrate

impact on all primary consumers and unprotected primary con-

sumers was analysed with linear regression. Finally, we used lin-

ear regression on the biomass of predatory invertebrates in

unmanipulated control cages to assess whether ambient predator

biomass was influenced by pond permanence.

mesocosm experiment 1: manipulation ofpredatory fish and submergent vegetation

Whether habitat refugia could explain the apparent weak con-

sumptive effects of fish in permanent ponds was examined by

manipulating the presence and/or absence of complex vegetation

structure and predatory fish in mesocosms (0�8 m2 oval tanks) in

a 2 9 2 factorial design with four replicates of each treatment

combination. The outdoor mesocosms, which were housed at

University of Canterbury’s Cass Field Station, were filled with

groundwater regulated to 25 cm deep throughout the experiment.

Clumps of Myriophyllum and Carex (surface area: 0�1 m2) were

added to the mud and fine gravel substrate of all tanks, and were

cut to soil level for the no-vegetation treatment. Koaro (Galaxias

brevipinnis) were chosen as predators as they are an abundant

native predatory fish in ponds and lake littoral zones in the study

area and they feed on a large range of macroinvertebrates (Rowe,

Konui & Christie 2002).

The prey community in each mesocosm consisted of 11 macro-

invertebrate species that are common in nearby permanent and

temporary ponds (Fig. S1, Supporting Information). The total

biomass of each prey taxa was approximately equal, and com-

bined biomass of all prey fell within the range observed in natu-

ral ponds (H. S. Greig unpublished data). Prey were added on

the 28th February 2007 10 h prior to the addition of fish (one

koaro per tank, mean fork length: 120 � 5�4 mm). After 2 weeks,

fish were removed from tanks and one pipe sample (0�020 m2)

was taken within the largest clump of Myriophyllum to subsample

small-bodied prey (chironomids and crustaceans) in the same

fashion as the predator assay. Following this procedure, all tank

contents were tipped into a 1-mm mesh net whose contents were

then transferred to a tray for sorting. Soil clumps were also

searched for macroinvertebrates. Invertebrates were preserved

and processed in the same manner as the predator assay.

The effects of fish and vegetation structure on total prey bio-

mass were evaluated using 2 9 2 factorial ANOVA with fish and

vegetation as fixed effects and loge-transformed total invertebrate

Table 1. Derivation of predatory impact indices for the field manipulation of predator abundance. Predator impact (PI) was calculated

as the log-ratio effect size PI = ln(Ba/Br) where Ba is the prey biomass in ambient cages and Br is the biomass in predator removal or

reduction cages.

Predator impact type Prey type

Contrasts for PI

Fish PI All invertebrates Open cages Fish exclusion

Predatory invertebrate PI Non-predatory inverts Fish removal All predator reduction

Total PI Non-predatory inverts Open cages All predator reduction

600 H. S Greig, S. A. Wissinger & A. R. McIntosh

AFDM the response variable. Treatment effects on prey commu-

nity composition were assessed with PERMANOVA (PERMANOVA

6; Anderson 2001) on a Bray-Curtis dissimilarity matrix created

from untransformed AFDM of each of the 11 macroinvertebrate

taxa. Significance (P < 0�05) was tested with 999 permutations.

mesocosm experiment 2: multiple predators

The second mesocosm experiment manipulated predator diver-

sity (within and between trophic levels) to determine if increas-

ing food-web complexity dampened top-down control in

permanent ponds. Predator diversity was examined in meso-

cosms using a hybrid design that included both additive and

substitutive manipulations of predator richness (Byrnes &

Stachowicz 2009). This design enabled us to investigate the

changes in intraspecific and interspecific interactions associated

with increases in the density and complexity of the predator

guild with pond permanence (Fig. 1a). We manipulated three

predatory invertebrate taxa including a common beetle, damsel-

fly and dragonfly larva and the non-consumptive effects of a

native and an introduced predatory fish species was also

included in one comparison (Fig. 1b). Treatments were limited

to the subsets of possible combinations that were relevant to

natural predator combinations across the permanence gradient.

The design enabled three models to be tested (indicted by small

cased letters beneath treatments in Fig. 1b): (1) density manipu-

lations (d) of a single widespread predator species, (2) additive

manipulations (a) of multiple predator species in combination

with all possible single species at low density treatments to

enable the calculation of expected predation rates and (3) a sub-

stitutive model (s) at high predator densities in which the effects

of fish chemical cues was also tested. Each of the 11 treatment

combinations (Fig. 1b), including predator-free controls with

and without fish cues, was replicated four times.

Manipulations were conducted in 0�35 m2 white plastic tubs

housed outdoors at the Cass Field Station. Mesocosms were filled

to a depth of 18 cm with groundwater, and three 15-cm high

clumps of plastic aquarium plants, three large cobbles and a layer

of fine sand were added as substrate (Fig. S2, Supporting Infor-

mation). Predator density varied between 4 and 12 individuals

per mesocosm, reflecting the range of predator biomass observed

in natural ponds. The combined cues of two fish species were

added to fish treatments by dripping water (6�2 � 1 L h�1) from

a single tank housing one koaro (145-mm fork length [FL]) and

one rainbow trout (140 mm FL). Fish were fed ad libitum on all

three species of invertebrates used in the experiment to ensure the

complete range of cues from fish feeding was present. A control

drip from an identical tank without fish or invertebrates was

distributed at the same rate into the remaining tanks. Prey were

late instar Chironomus zelandicus Hudson larvae (100 per meso-

cosm), collected from a nearby pond. Chironomus are found in

almost every lentic habitat in the landscape and are an important

component of predator diets. Prey were added at 1600 h on the

31st October 2007 and allowed to acclimate for 24 h before pre-

dators were introduced. Mesocosms were covered with 1 mm

mesh throughout the experiment to contain prey emergence.

After 5 days, adult chironomids that had emerged were hand-

collected, cobbles and artificial plants were washed and

removed, and invertebrates were collected by repeated elutriation

of the tank contents through a 250-lm mesh net followed by an

inspection of the remaining sand. Invertebrates were preserved

in 70% ETOH, enumerated in the laboratory and AFDM

Pond permanence

Control R

PControl R

d,a da a a d,s s a,s a,s Pre

Fig. 1. (a) Change in the complexity of predator guilds across the gradient of water permanence from temporary to permanent lentic

habitats in Canterbury, New Zealand. Letters denote representative beetle (R, Rhantus suturalis Macleay), damselfly (X, Xanthocnemis

zelandica Mclauchlan) and dragonfly taxa [P, Procordulia grayi (Selys)]. Solid and dashed arrows represent consumptive and non-con-

sumptive effects, respectively. (b) Hybrid experimental design used to investigate multiple predator effects along the permanence gradi-

ent. In (b) each box represents one treatment and box size is proportional to predatory invertebrate density. Capital letters correspond

to species in (a) and shading indicates the presence of chemical cues from fish (Oncorhynchus mykiss and Galaxias brevipinnis). Lower

case letters denote treatment combinations used in the single-species density manipulation (d), and the additive (a) and substitutive (s)

diversity manipulations. Two predator-free controls (with and without fish cues) were also included. Prey density was constant across all

treatments.

determined in the manner described earlier. Treatment combina-

tions were grouped according to types of predator manipulation:

(1) Rhantus beetle density treatment, (2) additive diversity

manipulations and (3) substitutive diversity manipulations

(Fig. 1b). Significance of each predator manipulation was tested

using one-way ANOVA with tanks as replicates, followed by

Tukey’s post-hoc comparisons of treatment means. Multiple

predator effects were tested in the additive model by calculating

expected predation rates for the two- and three-species treat-

ments from the low-density single-species treatments using an

additive probability model assuming finite prey resources (Soluk

& Collins 1988). The model was modified for a three species

guild (following Miller 2006:62), whereby expected prey consu-

mption = 100 9 (Pr + Px + Pp � PrPx � PxPp + PrPxPp), where

Pr, Px and Pp are the proportions of initial prey abundance

eaten in the Rhantus, Xanthocnemis and Procordulia single-pred-

ator treatments respectively. The effect of density on intraspe-

cific interactions in Rhantus single-species treatments was also

tested using these models. In this case, expected values were

based on Rhantus low density treatments. Significant differences

between observed predation rates and expected values were

assessed with one-sample t-tests. All analyses for the field and

mesocosm experiments (except PERMANOVA) were conducted in

Statistica 8 (StatSoft 2008).

Results

assays of predator impact in natural ponds

No consistent effects of fish on the biomass of prey were

observed in the in situ assays of predator impact in natu-

ral ponds (Fig. S3, Supporting Information). The biomass

of all invertebrates and primary consumers in cages that

allowed fish access did not differ significantly from cages

that prevented fish access (PI not significantly different

from zero; one-sample t-tests: t4 < 1�14, P > 0�31). The

same pattern was evident when only unprotected prey bio-

mass (species without cases or shells) was considered

(one-sample t-tests: t4 = 1�21, P = 0�29; Fig. S3, Support-ing Information).

The impact of predatory invertebrates on prey biomass

decreased with increasing pond permanence (Fig. 2a). This

pattern strengthened when only prey without morphologi-

cal defences were considered, owing to an increase in PI in

more temporary ponds (Fig. 2b). The biomass of preda-

tory invertebrates in the unmanipulated cages did not vary

significantly with pond permanence when expressed as

either biomass per cage, or proportion of total invertebrate

biomass (Fig. S4, Supporting Information; P > 0�15).

mesocosm experiment 1: manipulation of fishand aquatic vegetation

There was no detectable effect of predatory fish on prey

biomass in the mesocosms (Fig. 3). Total prey biomass

was not significantly different between fish and fishless

treatments (F1,12 = 0�29, P = 0�60; Fig. 3), or between

complex and simple vegetation treatments (F1,12 = 2�74,P = 0�12), and there was no fish by vegetation interaction

(F1,12 = 1�03, P = 0�33). Similarly, PERMANOVA indicated

that there were no treatment effects on the composition

of the prey community (fish: F1,12 = 0�84, P = 0�51; vege-tation: F1,12 = 1�95, P = 0�11; interaction: F1,12 = 1�17,P = 0�28). Lastly, fish had no effect on the total biomass

of large-bodied (>4 mg DW) predatory taxa (ANOVA, fish:

F1,12 = 0�52, P = 0�48, interaction: F1,12 = 0�87, P = 0�37).

mesocosm experiment 2: multiple predators

Predation rates of Rhantus beetles as the sole predator

increased significantly with density (one-way ANOVA:

F2,9 = 7�26, P = 0�013; Fig. 4a), but observed predation

rates in high density treatments were significantly lower

than expected based on additive predation at low densities

(Fig. 4a). The additive manipulation of predator diversity

had significant impacts on the consumption of Chirono-

mus (Fig. 4b, One-way ANOVA: F5,18 = 17�9, P < 0�0001).In treatments with single predator species, predation rates

of Rhantus beetle larvae and Procordulia dragonflies were

almost identical, but Xanthocnemis damselflies were a sig-

nificantly weaker predator on Chironomus (Fig. 4b). The

two-predator species treatment resulted in significantly

higher predation rates than by Xanthocnemis alone, but

was not significantly different from rates for Procordulia

or Rhantus alone. In contrast with the single-species den-

sity manipulation, increasing predator density by increas-

ing diversity led to predation rates almost identical to

expected values calculated from the single-species treat-

ments (Fig. 4b). However, the addition of fish chemical

cues significantly decreased predation rates in the three-

species treatment to a level similar to the two-species

treatment and not significantly higher than for Rhantus

and Procordulia alone at low density (Fig. 4a).

The substitutive manipulation of predator diversity, in

which total predator density was kept constant, signifi-

cantly influenced predation on Chironomus (Fig. 4c, one-

way ANOVA: F3,12 = 4�29, P = 0�028); however, this was

due to a reduction in predation rates with fish cues in the

three-species treatment (Fig. 4c). Post-hoc tests indicated

no significant difference between the one-, two- and three-

species treatments in the absence of fish cues (P > 0�34).

Discussion

Decreases in the intensity of competition and predation

with increasing abiotic stress or disturbance are central to

several models of community organization across environ-

mental gradients (Menge & Sutherland 1987; Wellborn,

Skelly & Werner 1996; Chesson 2000). Our field assays of

predator–prey interactions across a pond drying gradient

revealed patterns opposite to these predictions. Top-down

control of prey biomass decreased with pond permanence

despite an increase in the size, biomass and diversity of

predators in increasingly permanent ponds (Wissinger,

Greig & McIntosh 2009). Our mesocosm experiment sug-

gested that those patterns could result from the non-con-

sumptive effects of fish weakening predation by inverte-

brates in the more complex predator guilds of permanent

ponds. Below we evaluate these unexpected patterns and

their implications for understanding top-down control in

food webs.

consumptive effects of predatory fish

Long-lived predatory vertebrates such as fish and paedo-

morphic salamanders can only persist in perennial fresh-

water habitats. Consequently, they are often implicated as

the key drivers of community shifts across pond perma-

nence gradients (Wellborn, Skelly & Werner 1996;

Wissinger 1999). Unexpectedly, our results revealed negli-

gible consumptive effects of predatory fish on invertebrate

biomass in permanent ponds. We observed no measurable

effect of fish exclusion on prey biomass in cages within

permanent ponds, but variability between ponds led to

low power to detect a significant mean effect of fish across

all fish containing ponds. (minimum detectable effect sizes

at b = 0�8 was 4–10 times greater than those presented in

Fig. S3, Supporting Information). Nevertheless, our first

mesocosm experiment revealed that even in spatially con-

fined environments, predatory fish did not depress prey

biomass. In this experiment, power was sufficient (at

b = 0�8) to detect a 15% difference in prey biomass

between fish and fishless tanks which is lower than effect

sizes observed in other studies of fish predation on littoral

benthic invertebrates (Morin 1984; Hershey & Dodson

1985; Diehl 1992). The absence of fish effects were sur-

prising given that (a) koaro of the size used in the experi-

ment regularly feed on the taxa and size ranges of

invertebrates added to the mesocosms (Rowe, Konui &

Christie 2002), and (b) we observed koaro feeding in the

experiment, which was confirmed by the presence of

Rhantus and Xanthocnemis larvae in the gut contents of

several fish sacrificed at the conclusion of the experiment.

Several hypotheses could explain the apparent absence

of consumptive effects of predatory fish in our system.

First, the structural complexity provided by dense stands

of aquatic vegetation provides prey refugia that can lower

the foraging efficiency of fish and reduce top-down con-

trol of prey (Diehl 1992; Pierce & Hinrichs 1997). Those

refugia are likely to be more effective for prey avoiding

large, actively foraging, visual predators like fish (Swisher,

Soluk & Wahl 1998), than predatory invertebrates that

are similar in body size and habitat use to prey. However,

in our experiment the presence of refugia alone could not

explain weak consumptive fish effects, as there was no dif-

ference in predation between mesocosms with or without

submergent vegetation. A second potential explanation

for minimal consumptive effects of fish is that size-selec-

tive foraging by fish on predatory invertebrates released

primary consumers from consumption by mesopredators

(Wooster 1994; Meissner & Muotka 2006). However, we

Pond permanence index–1·5 –0·5 0·5 1·5 2·5

P = 0·005R2 = 0·57

P = 0·035R2 = 0·37

(a) Total prey biomass

(b) Unprotected prey biomass

Fig. 2. Predatory invertebrate impact index for (a) total prey bio-

mass and (b) unprotected prey biomass (i.e. snails and cased cad-

dis excluded) in ponds varying in permanence due to drying.

Negative predator impacts indicate a decrease in prey biomass

relative to predator removal treatments; higher values on the

X-axis indicate more permanent ponds. Ponds with and without

fish are indicated by triangles and circles, respectively. Regression

equations are y = �0�51 + 0�59x and y = �0�56 + 0�92x for total

prey biomass and undefended prey biomass respectively.

Vegetation coverPresent Absent

400 FishFishless

Fig. 3. Effect of predatory fish (Galaxias brevipinnis) and sub-

merged vegetation on total biomass of 11 invertebrate species

after 14 days in a mesocosm experiment. Means (�SE) were cal-

culated with tanks as replicates. Vegetation cover indicates the

presence or absence of submergent and emergent vegetation in

mesocosms.

did not observe any effects of fish on the biomass of

predatory invertebrates in either the field assay or in the

mesocosm experiment, providing little support for this

hypothesis. Similarly, predatory invertebrate biomass was

not negatively correlated with permanence, which would

be expected if fish consumption suppressed large-bodied

invertebrates. Finally, the effect of fish manipulations

may be limited if the prey community is a preselected sub-

set of the regional species pool that is resistant to fish

predation (Allan 1982; Thorp 1986). However, the prey

community in the mesocosms consisted of species col-

lected from habitats with and without fish. Furthermore,

there was no consistent effect of fish on unprotected prey

species in the assay, indicating that morphologically

defended prey were not responsible for the lack of fish

effects.

The most likely explanation for negligible fish effects is

that weak consumption by fish was balanced by strong

interactions within the invertebrate community in fishless

mesocosms. For example, intraguild predation and canni-

balism within prey communities is generally stronger in

the absence of risk-sensitive behavioural responses to pre-

dators (Schmitz 2007; Rudolf 2008). Regardless of the

mechanism, our results and those in previous studies

(Wissinger, McIntosh & Greig 2006; Wissinger, Greig &

McIntosh 2009), indicate that fish feeding has weak

impact at best on epibenthic invertebrate community com-

position in the lentic habitats of our study region. Impor-

tantly, however, fish may still exert a strong influence on

food-web interactions through non-consumptive effects on

prey individuals (McPeek & Peckarsky 1998; Werner &

Peacor 2003; Peckarsky et al. 2008), and these interaction

modifications were evident in the multiple predator

experiment.

the influence of food web complexity ontop-down control

A second experiment with multiple predators provided

strong evidence that the non-consumptive presence of fish

(as indicated by fish odour) reduced prey consumption by

predatory invertebrates. The presence of fish cues reduced

predation on chironomids in the three-species treatment

to levels more similar to those found in low-density sin-

gle-species treatments. Thus, if the consumptive effects of

fish are as weak, as indicated by the mesocoms experi-

ments and in situ manipulations, the presence of fish in

permanent ponds in our study sites should result in a net

decrease in top-down control of benthic invertebrates. We

contend that the non-consumptive effects of fish weak-

ened the effects of predatory invertebrates in permanent

ponds leading to a decrease in the strength of predator–

prey interactions with increasing pond permanence. The

suppression of predatory invertebrate foraging also pro-

vides a mechanism for the negligible effects of fish on

invertebrate prey communities in the mesocosm experi-

ment. Furthermore, these results provide support for the

Additive predator diversity

Rhantus density per tank

Substitutive predator diversity

R X P RX RXP RXP fish

4 8 12

RXP R RX RXP fish

Fig. 4. Effect of (a) larval Rhantus density, (b) additive predator

diversity and (c) substitutive predator diversity on mean (�SE)

consumption of Chironomus larvae during a 5-day mesocosm

experiment. X-axis labels for (b) and (c) are as follows: R, Rhan-

tus larvae; X, Xanthocnemis larvae; P, Procordulia larvae; fish,

presence of chemical cues from both rainbow trout (Onchoryn-

chus mykiss) and koaro (Galaxias brevipinnis). See Fig. 1 for fur-

ther description of treatments. Means were calculated with tanks

as replicates; letters indicate significant differences (P < 0�05)between treatments (Tukey’s post-hoc comparisons). Dashed lines

indicate expected Chironomus predation calculated from additive

probability models (adjusted for finite prey resources) of low den-

sity conspecifics in (a), and from single-species treatments in (b).

Asterisks indicate significant departures from the expected model

(*0�1 < P < 0�05, **P < 0�05) based on one-sample t-tests.

hypothesis that non-consumptive effects of fish in fresh-

water food webs often outweigh their consumptive effects

(e.g. McPeek & Peckarsky 1998).

Our experiments focused on the most commonly

observed predatory invertebrates across the permanence

gradient, and indicate that increased invertebrate predator

diversity in the absence of fish cues led to small positive

effects of diversity on predator impacts, rather than

antagonistic effects among species. The additive model in

particular revealed that increases in predator density by

enhancing diversity may reduce negative intraspecific

interactions apparent in high densities of a single predator

taxa (as in Griffin et al. 2008). This is consistent with the

assertion that intraspecific interactions among predators

are stronger than interspecific interactions (Byrnes & Stac-

howicz 2009). Predation rates of Rhantus beetle larvae at

high densities were significantly lower than the expected

additive predation rate calculated from low density treat-

ments, but predation rates in high density treatments of

multiple predators were almost identical to expected rates.

The Rhantus only treatment is representative of predator

guilds in the most temporary ponds in our study area

(< 1 month inundated), which we were unable to include

in the field experiment because of the logistical constraints

of their short duration. The small positive effects of pred-

atory invertebrate diversity we observed suggest that

predator impact may follow a hump-shaped relationship

with pond permanence when the full range of pond dura-

tion is considered.

Differences we observed in the effects of diversity by

adding trophic levels or adding species within trophic lev-

els reinforce the contention that horizontal and vertical

diversity components of food webs have different but

interactive effects on species interactions (Duffy et al.

2007; Srivastava & Bell 2009). Vertical diversity can

increase top-down control, for example, when top preda-

tors increase spatial overlap of mesopredators and prey

(Grabowski & Kimbro 2005). However, in many cases,

the addition of predator trophic levels should dampen

top-down control. Body size generally increases with tro-

phic level (Woodward et al. 2005), so increasing vertical

diversity in food webs generates size asymmetry between

predator species that promotes intraguild predation and

density- and trait-mediated foraging suppression of meso-

predators. This is analogous to the effects of introducing

size-structure within predator populations (Rudolf 2007).

These negative interactions among trophic levels may

overwhelm positive effects of within-trophic level diver-

sity, as observed in our study when fish cues reduced the

foraging of three species predator guilds to rates similar

to single species guilds.

Several aspects of food web complexity in addition to

diversity may have contributed to the decreased predator

impact with more permanent ponds. Many permanent

pond species have semivoltine life histories, which results

in overlapping cohorts at a given time. Consequently,

size-structured interactions such as cannibalism and intra-

guild predation that can weaken top-down control (Polis

1991; Padeffke & Suhling 2003) are likely to be more pre-

valent in permanent ponds than in temporary ponds

where drying and refilling promotes developmental syn-

chrony within populations. Permanent ponds also often

contain a higher proportion of morphologically defended

prey species (e.g. snails and cased caddisflies) than tempo-

rary ponds, although the negative relationship between

predator impact and permanence actually strengthened

when we excluded morphologically defended prey from

the analysis (Fig. 3b). Finally, prey in resource-limited or

time-constrained habitats such as temporary ponds may

be less likely to exhibit risk-sensitive foraging and other

antipredatory responses, which should strengthen

top-down control.

Conclusions

Interactions between the same sets of species can reverse

in direction or change in strength depending on environ-

mental and consumer context (Crain 2008). Our study

provides evidence that changes in the properties of food

webs along environmental gradients from structurally sim-

ple, chain-like food webs in disturbed habitats, to com-

plex, reticulate food webs in physically benign habitats

are likely to dampen top-down control and generate unex-

pected relationships between abiotic stress and the

strength of species interactions. These results emphasize

that considering food web complexity, especially the non-

consumptive effects of top predators, is essential to under-

stand species interactions across environmental gradients.

Acknowledgements

We thank A. Klemmer, P. Jellyman, E. Isherwood, C. Ross and M.

Galatowitsch for field and laboratory assistance. N. Etheridge and V.

Greig constructed the cages, and M. Fraundorfer, R. Hill, J. Westenra, R.

Smith and the Dept. of Conservation granted access to research sites. We

thank B. Peckarsky, R. Didham, B. Sorrell, M. Winterbourn, A. Hildrew

and G. Closs for valuable comments and discussion. The research was

funded by the Miss E.L. Hellaby Indigenous Grassland Research Trust.

HSG was supported by a Top Achiever Doctoral Scholarship and a Foun-

dation for Science, Research and Technology Postdoctoral Fellowship and

SAW was supported by an Erskine Fellowship from the University of

Canterbury.

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Received 30 July 2012; accepted 29 November 2012

Handling Editor: Karl Cottenie

Supporting Information

Additional Supporting Information may be found in the online version

of this article.

Table S1. A list of environmental variables for each pond, includ-

ing hydrological parameters underlying the multivariate pond

permanence index, and the identity of predatory fish.

Figure S1. Photos and description of the mesocosm experiment

manipulating the presence and absence of fish and vegetation.

Figure S2. Photo of the mesocosms used in the predator diversity

manipulation.

Figure S3. The impact of predatory fish on invertebrate biomass in

the in situ cage experiment.

Figure S4. Regression of predatory invertebrate biomass in unma-

nipulated cages against pond permanence for the in situ cage

experiment.

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