Interspecific differences in antipredator strategies determine the strength of non‐consumptive predator effects on stream detritivores

Animal species differ considerably in their response to predation risks. Interspecific variability in prey behaviour and morphology can alter cascading effects of predators on ecosystem structure and functioning. We tested whether species‐specific morphological defenses may affect responses of leaf litter consuming invertebrate prey to sit‐and‐wait predators, the odonate Cordulegaster boltonii larvae, in aquatic food webs. Partly or completely blocking the predator mouthparts (mandibles and/or extensible labium), thus eliminating consumptive (i.e. lethal) predator effects, we created a gradient of predator‐prey interaction intensities (no predator < predator – no attack < predator – non‐lethal attacks < lethal predator). A field experiment was first used to assess both consumptive and non‐consumptive predator effects on leaf litter decomposition and prey abundances. Laboratory microcosms were then used to examine behavioural responses of armored and non‐armored prey to predation risk and their consequences on litter decomposition. Results show that armored and non‐armored prey responded to both acute (predator – non‐lethal attacks) and chronic (predator – no attack) predation risks. Acute predation risk had stronger effects on litter decomposition, prey feeding rate and prey habitat use than predator presence alone (chronic predation risk). Predator presence induced a reduction in feeding activity (i.e. resource consumption) of both prey types but a shift to predator‐free habitat patches in non‐armored detritivores only. Non‐consumptive predator effects on prey subsequently decreased litter decomposition rate. Species‐specific prey morphological defenses and behaviour should thus be considered when studying non‐consumptive predator effects on prey community structure and ecosystem functioning.     

Indirect interactions in a rice ecosystem: density dependence and the interplay between consumptive and non‐consumptive effects of predators

1. Density‐ and trait‐mediated indirect interactions (DMIIs and TMIIs, respectively) in food chains play crucial roles in community structure and processes. However, factors affecting the relative strength of these interactions are poorly understood, including in widespread and important freshwater rice ecosystems. 2. We studied the strength of DMIIs and TMIIs in a food chain involving a predator (the Reeve’s turtle Chinemys reevesii), its herbivorous prey (the apple snail Pomacea canaliculata) and a plant (rice Oryza sativa) in outdoor containers simulating rice fields. We also evaluated consumptive and non‐consumptive effects of the predator on the snail. We removed a fixed proportion of snails every 2 days to simulate prey consumption and introduced a caged turtle that was fed daily with snails to simulate non‐consumptive effects. 3. Direct consumptive effects increased growth of the remaining snails and their per capita feeding rate. Moreover, consumptive and non‐consumptive effects, and their interaction, affected the proportion of snails buried in the soil. This interaction was presumably because increasing food availability per snail induced their self‐burying behaviour. 4. Both DMIIs and TMIIs affected the number of rice plants remaining, whereas their interaction term was not significant. 5. In summary, density dependence and interactions between consumptive and non‐consumptive effects influenced snail growth and behaviour, respectively. However, no cascading effects of these complicated interactions on rice plants were detected.     

Non‐consumptive effects of a natural enemy on a non‐prey herbivore population

1. Predator–prey interactions have traditionally focused on the consumptive effects that predators have on prey. However, predators can also reduce the abundance of prey through behaviourally‐mediated non‐consumptive effects. For example, pea aphids (Acyrthosiphon pisum Harris) drop from their host plants in response to the risk of attack, reducing population sizes as a consequence of lost feeding opportunities. 2. The objective of the present study was to determine whether the non‐consumptive effects of predators could extend to non‐prey herbivore populations as a result of non‐lethal incidental interactions between herbivores and foraging natural enemies. 3. Polyculture habitats consisting of green peach aphids (Myzus persicae Sulzer) feeding on collards and pea aphids feeding on fava beans were established in greenhouse cages. Aphidius colemani Viereck, a generalist parasitoid that attacks green peach aphids but not pea aphids, was released into half of the cages and the abundance of the non‐host pea aphid was assessed. 4. Parasitoids reduced the population growth of the non‐host pea aphid by increasing the frequency of defensive drops; but this effect was dependent on the presence of green peach aphids. 5. Parasitoids probably elicited the pea aphid dropping behaviour through physical contact with pea aphids while foraging for green peach aphids. It is unlikely that pea aphids were responding to volatile alarm chemicals emitted by green peach aphids in the presence of the parasitoid. 6. In conclusion, the escape response of the pea aphid provided the opportunity for a parasitoid to have non‐target effects on an herbivore with which it did not engage in a trophic interaction. The implication is that natural enemies with narrow diet breadths have the potential to influence the abundance of a broad range of prey and non‐prey species via non‐consumptive effects.     

Plant resistance attenuates the consumptive and non‐consumptive impacts of predators on prey

Plant resistance and predation have strong independent and interacting effects on herbivore survival, behavior, and patterns of herbivory. Historically, research has emphasized variation in the consumption of herbivores by enemies. Recent work, however, demonstrates that predators also elicit important changes in the traits of their prey, but we do not know how this is influenced by plant quality. In this study, we quantify how the consumptive and non‐consumptive effects of predators vary along a gradient of plant resistance using tomato plants (Solanum lycopersicum), tobacco hornworms (Manduca sexta), and predaceous stinkbugs (Podisus maculiventris). We manipulated resource quality using three tomato lines that vary in the expression of the jasmonate pathway, a phytohormonal pathway that is central in mediating resistance to insects. Resistant plants had higher levels of defensive proteins and glandular trichomes than low resistance plants. The consumptive and non‐consumptive effects of predators were quantified on the three tomato lines by comparing the impact of ‘lethal’ predators that both kill and scare prey with ‘risk’ predators whose mouthparts were surgically impaired to prevent killing. Across several field experiments, the total cascading effect of predators on plant damage was 80.4% lower on jasmonate‐overex‐pressing (highly resistant) plants compared to that on wild‐type or jasmonate‐insensitive (low resistance) plants. This dramatic attenuation of predator effects was due to a 66% reduction in consumption on high resistance plants, and also because of a 65% decline in non‐consumptive effects. Numerous studies in natural and agricultural habitats have documented that predator effects tend to be weaker on well‐defended plants; our results provide novel mechanistic insight into this pattern by demonstrating that plant resistance substantially weakens both the consumptive and non‐consumptive impacts of predators.     

Independent and combined effects of multiple predators across ontogeny of a dominant grazer

Ecosystems host multiple coexisting predator species whose interactions may strengthen or weaken top–down control of grazers. Grazer populations often exhibit size‐structure, but the nature of multiple predator effects on suppression of size‐structured prey has seldom been explicitly considered. In a southeastern US salt‐marsh, we used both field (additive design) and mesocosm (additive‐substitutive design) experiments to test the independent and combined effects of two species of predatory crab on the survival and predator‐avoidance behavior (i.e. a non‐consumptive effect) of both juveniles and adults of a dominant grazing snail. Results showed: 1) juvenile snails were more vulnerable to predation; 2) consumptive impacts of predators were hierarchically nested, i.e. the larger predator consumed both juvenile and adult snails, while the smaller‐bodied predator consumed only juvenile snails; 3) there were no emergent multiple predator effects on snail consumption; and 4) non‐consumptive effects differed from consumptive effects, with only the large predator inducing predator‐avoidance behavior of individuals within either snail ontogenetic class. The smaller predator therefore played a functionally redundant trophic role across the prey classes considered, augmenting and potentially stabilizing trophic regulation of juvenile snails. Meanwhile, the larger predator played a complementary and functionally unique role by both expanding the size‐spectrum of prey trophic regulation and non‐consumptively altering prey behavior. While our study suggests that nestedness of consumptive interactions determined by predator and prey body sizes may allow prediction of the functional redundancy of particular predator species, it also shows that traits beyond predator body size (e.g. habitat domain) may be required to predict potentially cascading non‐consumptive effects. Future studies of multiple predators (and predator biodiversity) should continue to strive towards greater realism by incorporating not only size‐structured prey, but also other aspects of resource and environmental heterogeneity typical of natural ecosystems.     

Defence Cheats Can Degrade Protection of Chemically Defended Prey

Many species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non‐defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non‐defended ‘cheats’ affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (‘cheats’) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency‐dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste‐rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste‐rejected because with acute time constraints, wild birds do not have time to make fine‐grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.     

Piscivore addition causes a trophic cascade within and across ecosystem boundaries

The addition of predators can play a key role in structuring ecological communities through both consumptive and non‐consumptive effects. Stocking of piscivorous fish in lakes and similar experimental introductions have provided fundamental evidence in support of trophic cascade theory. Yet, the impact of piscivore addition on cross ecosystem subsidies and meso‐predator resource use has not been well studied. Here, we use a replicated pond experiment to document the trophic impacts of a piscivore, cutthroat trout Onchorhynchus clarkii, on aquatic communities already containing a meso‐predatory fish (threespine stickleback Gasterosteus aculeatus) and neighbouring terrestrial ecosystems. We find that piscivore addition led to a trophic cascade that extended across an ecosystem boundary: trout addition increased the biomass and average size of insects emerging into the terrestrial system. Piscivores caused a diet shift in stickleback, a non‐consumptive effect that was likely mainly responsible for the increase in emerging insect biomass. We additionally show that heterogeneity in the strength of the pelagic trophic cascade was more closely correlated with the magnitude of diet shift (reflecting a non‐consumptive effect) than decreases in stickleback abundance (a consumptive effect). Taken together, our experiment demonstrates that the addition of a piscivore causes a trophic cascade that can extend beyond the aquatic system and suggests that non‐consumptive effects may more strongly influence the strength of a trophic cascade than has been previously recognized.     

The effect of predation pressure and predator adaptive foraging on the relative importance of consumptive and non‐consumptive predator net effects in a freshwater model system

An important challenge in community ecology is identifying the functional characteristics capable of predicting the nature and strength of predator effects on food webs. We developed an individual‐based model, based on a shallow lake model system, to evaluate the total, consumptive, and non‐consumptive indirect effect that predators have on basal resources when the predators differ in their foraging types (active adaptive foraging or sedentary foraging). Overall, both predator types caused similar total indirect effects on lower trophic levels. However, the nature net effects of predators diverged between predator foraging types. Active predators caused larger non‐consumptive effects, relative to the total indirect effect, irrespective of predation pressure levels. On the other hand, sedentary predators caused larger non‐consumptive effects for lower predation pressure levels, but consumptive effects became more important as predation pressure increased. Our simulations showed that the reliance on a particular mechanism driving consumer–resource interactions is altered by predator foraging behavior and highlight the importance of both prey and predator foraging behaviors to predict the causes and consequences of cascading effects observed in food webs.     

Predator presence dramatically reduces copepod abundance through condition‐mediated non‐consumptive effects

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Selection of aphid prey by a generalist predator: do prey chemical defences matter?

1. For predators, prey selection should maximise nutrition and minimise fitness costs. In the present study, it was investigated whether a generalist predator [Chrysoperla carnea (Stephens) lacewing larvae] rejected harmful, chemically‐defended prey [Brevicoryne brassicae (Linnaeus) aphids] when non‐defended prey [Myzus persicae (Sulzer) aphids] were available. 2. It was tested: (i) whether consuming different prey species affects predator mortality; (ii) whether naïve predators reject chemically‐defended prey while foraging when non‐defended prey are available; (iii) whether the relative abundance of each prey affects the predator's prey choice; and (iv) whether predators learn to avoid consuming chemically‐defended prey after exposure to both prey species. 3. Consumption of B. brassicae yielded greater C. carnea mortality than M. persicae consumption, but naïve C. carnea did not reject B. brassicae in favour of M. persicae during foraging. When presented at unequal abundances, naïve predators generally consumed each aphid species according to their initial relative abundance, although, predation of non‐defended prey was less than expected when defended prey were initially more abundant, indicating a high consumption of B. brassicae impeded M. persicae consumption. With experience, C. carnea maintained predation of both aphid species but consumed more M. persicae than B. brassicae, indicating a change in behaviour. 4. Although prey choice by C. carnea may change with experience of available prey, prey chemical defences do not appear to influence prey choice by naïve predators. This inability to avoid harmful prey could facilitate wider, indirect interactions. Myzus persicae may benefit where high consumption of B. brassicae hinders predators in the short term, and in the long term, increases predator mortality.     

Predator-induced diapause in Daphnia magna may require two chemical cues

The production of diapausing eggs by Daphnia magna stimulated by fish exudates can be explained as an anti-predator defence ensuring genome protection in periods of high risk from fish predation. The combined effects on the induction of D. magna diapause of an “alarm” chemical originating from injured conspecific prey and fish kairomones were tested. The results of the experiment showed that the cues when present together promote both the production of ephippial eggs and male formation, indicating their role in the synchronization of the entire mode of Daphnia sexual reproduction. Ephippial eggs were only produced in the presence of both fish kairomone and conspecific alarm chemicals, while male offspring occurred in the treatments where both, one or none of the cues were present. However, production of males was the highest when both cues were provided. D. magna responded similarly to the tested cues whether or not the hypothetical alarm substance associated with predator odour came from Daphnia specimens actually eaten by fish or from crushed conspecific individuals. However, chemicals from crushed chironomid larvae combined with fish kairomones did not induce a similar response in D. magna. The relative advantage of utilization of alarm cues or predator kairomones in the induction of defence responses in prey organisms is discussed. Received: 8 June 1998 / Accepted: 11 January 1999     

Predators weaken prey intraspecific competition through phenotypic selection

Predators have a key role shaping competitor dynamics in food webs. Perhaps the most obvious way this occurs is when predators reduce competitor densities. However, consumption could also generate phenotypic selection on prey that determines the strength of competition, thus coupling consumptive and trait‐based effects of predators. In a mesocosm experiment simulating fish predation on damselflies, we found that selection against high damselfly activity rates – a phenotype mediating predation and competition – weakened the strength of density dependence in damselfly growth rates. A field experiment corroborated this finding and showed that increasing damselfly densities in lakes with high fish densities had limited effects on damselfly growth rates but generated a precipitous growth rate decline where fish densities were lower – a pattern expected because of spatial variation in selection imposed by predation. These results suggest that accounting for both consumption and selection is necessary to determine how predators regulate prey competitive interactions.     

Sensory cues of a top‐predator indirectly control a reef fish mesopredator

Behavioural trophic cascades highlight the importance of indirect/risk effects in the maintenance of healthy trophic‐level links in complex ecosystems. However, there is limited understanding on how the loss of indirect top–down control can cascade through the food‐web to modify lower level predator–prey interactions. Using a reef fish food‐web, our study examines behavioural interactions among predators to assess how fear elicited by top‐predator cues (visual and chemical stimuli) can alter mesopredator behaviour and modify their interaction with resource prey. Under experimental conditions, the presence of any cue (visual, chemical, or both) from the top‐predator (coral trout Plectropomus leopardus) strongly restricted the distance swum, area explored and foraging activity of the mesopredator (dottyback Pseudochromis fuscus), while indirectly triggering a behavioural release of the resource prey (recruits of the damselfish Pomacentrus chrysurus). Interestingly, the presence of a large non‐predator species (thicklip wrasse Hemigymnus melapterus) also mediated the impact of the mesopredator on prey, as it provoked mesopredators to engage in an ‘inspection’ behaviour, while significantly reducing their feeding activity. Our study describes for the first time a three‐level behavioural cascade of coral reef fish and stresses the importance of indirect interactions in marine food‐webs.     

The importance of honeydew as food for larvae of Chrysoperla carnea in the presence of aphids

Larvae of the common green lacewing Chrysoperla carnea are predacious and feed on a wide range of small, soft‐bodied arthropods. In addition to their feeding on prey arthropods to cover their nutritional requirements for growth and development, the consumption of non‐prey foods such as honeydew has been reported. It is commonly believed that these food supplements are primarily exploited by the larvae when prey is scarce or of low nutritional quality. Here, we assess whether C. carnea larvae also use honeydew when high‐quality aphid prey are readily available. In a choice experiment, the feeding behaviour of C. carnea larvae was observed in the presence of both aphids and honeydew. The larvae were starved, aphid‐fed, or honeydew‐fed prior to the experiment. The time spent feeding on honeydew compared with feeding on aphids was highest for starved larvae and lowest for honeydew‐fed larvae. Among the three treatments, the aphid‐fed larvae spent the most time resting and the least time searching. In an additional experiment food intake was assessed in terms of weight change when larvae were provided with an ad libitum supply of either aphids or honeydew. Larvae yielded a significant lower relative weight increase on honeydew compared with aphids. The reduced weight increase on honeydew was compensated when larvae were subsequently provided with aphids, but not when honeydew was provided again. This study showed that (i) prior honeydew feeding reduces overall aphid consumption, and (ii) larvae do consume honeydew even after they have been given ad libitum access to aphids. The fact that larvae of C. carnea still use honeydew as a food source in the presence of suitable prey underlines the importance of carbohydrates as foods.     

Associational resistance or susceptibility: the indirect interaction between chemically‐defended and non‐defended herbivore prey via a shared predator

Many organisms possess chemical defences against their natural enemies, which render them unpalatable or toxic when attacked or consumed. These chemically‐defended organisms commonly occur in communities with non‐ or less‐defended prey, leading to indirect interactions between prey species, mediated by natural enemies. Although the importance of enemy‐mediated indirect interactions have been well documented (e.g. apparent competition), how the presence of prey chemical defences may affect predation of non‐defended prey in terrestrial communities remains unclear. Here, an experimental approach was used to study the predator‐mediated indirect interaction between a chemically‐defended and non‐defended pest aphid species. Using laboratory‐based mesocosms, aphid community composition was manipulated to include chemically‐defended (CD) aphids Brevicoryne brassicae, non‐defended (ND) aphids Myzus persicae or a mixed assemblage of both species, on Brassica oleracea cabbage plants, in the presence or absence of a shared predator (Chrysoperla carnea larvae). Aphid population growth rates, aphid distributions on host plants and predator growth rates were measured. In single‐species treatments, C. carnea reduced M. persicae population growth rate, but had no significant impact on B. brassicae population growth rate, suggesting B. brassicae chemical defences are effective against C. carnea. Chrysoperla carnea had no significant impact on either aphid species population growth rate in mixed‐species treatments. Myzus persicae (ND) therefore experienced reduced predation in the presence of B. brassicae (CD) through a predator‐mediated indirect effect. Moreover, predator growth rates were significantly higher in the M. persicae‐only treatments than in either the B. brassicae‐only or mixed‐species treatments, suggesting predation was impaired in the presence of B. brassicae (CD). A trait‐mediated indirect interaction is proposed, consistent with associational resistance, in which the predator, upon incidental consumption of chemically‐defended aphids is deterred from feeding, releasing non‐defended aphids from predatory control.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Phosphorus availability mediates plasticity in life-history traits and predator–prey interactions in Daphnia

We analysed growth plasticity of two Daphnia pulex clones under low‐phosphorus (LP) and high phosphorus (HP) conditions, in the presence of Chaoborus kairomones to examine how food quality (P‐availability) might impact life‐history responses and vulnerability to predation. Overall, clone 1 grew faster, and was larger at maturity. Under HP, both clones responded to kairomones by increasing growth, age and size at maturity, and decreasing fecundity. Under LP, both clones suffered reduced growth, and fecundity. However, the magnitude of response to kairomones depended on a clone by P‐availability interaction. Chaoborus presented a 1 : 1 clonal mixture under HP or LP, consumed more individuals under LP. Moreover, fewer clone 1 individuals were consumed. Studying the effects of P‐availability on life histories, and predator–prey interactions may help us understand the mechanisms generating and maintaining plasticity, as well as influencing genotypic diversity and microevolutionary processes in natural populations.     

Variation in ephippial buoyancy in Daphnia pulicaria

1. Freshwater zooplankton often produce diapausing eggs to survive environmental stress. The diapausing eggs of Daphnia (Crustacea, Cladocera) are encased in an ephippium that either floats at the surface or sinks to the sediment. These two types of ephippia may represent different strategies between spatial (floaters) and temporal (sinkers) dispersal of offspring. 2. We observed floating and sinking characteristics of ephippia obtained from eight lakes. We then conducted an experiment with 26 Daphnia pulicaria clones obtained from six of these lakes and observed the production of buoyant and non‐buoyant ephippia under high and low food conditions. 3. Ephippia were more often non‐buoyant than buoyant both from females caught in nature and those reared in the laboratory. The experiment revealed that each clone was able to produce both types of ephippia, but that there was considerable among‐clone variation in the percentage of non‐buoyant ephippia produced. 4. We conclude that production of non‐buoyant versus buoyant ephippia may be driven by both genetic and environmental factors.     

Does group feeding by toxic prey confer a defensive benefit? Aristolochic acid content,group size and survival of first‐instar pipevine swallowtail (Battus philenor L.) larvae

1. Aggregative feeding of larvae is widespread in the Lepidoptera, and many hypotheses have been proposed to explain the adaptive significance of this trait. Group feeding occurs disproportionately more in species with aposematic, chemically defended larvae compared with species with cryptic, non‐chemically defended larvae, consistent with the hypothesis that group feeding provides an enhanced aposematic signal to natural enemies. Most species characterised as having chemically defended larvae are cryptic during the first instar, when they are most highly aggregated and most vulnerable to predation. 2. The benefits of group feeding in terms of decreased predation were explored for first‐instar larvae of the pipevine swallowtail, Battus philenor, a species that sequesters aristolochic acids from its Aristolochia host plant and exhibits aposematism in later instars and as adults. We found that groups of larvae with experimentally enhanced aristolochic acid content had significantly lower survivorship due to predation both in the field and in laboratory experiments compared with groups of larvae without enhanced chemical defence. 3. A laboratory experiment found that aristolochic acid does not deter the generalist predator Hippodamia convergens. 4. No evidence was found that was consistent with the hypothesis that group feeding and increased sequestered chemical defence interact to decrease rates of larval mortality in non‐aposematic, first‐instar larvae. Future research on chemical defence, aposematism, and aggregative feeding should continue to appreciate that particular chemical defences and feeding behaviours are not universally effective against all natural enemies.