Predator density and the functional responses of coral reef fish

Predation is a key process driving coral reef fish population dynamics, with higher per capita prey mortality rates on reefs with more predators. Reef predators often forage together, and at high densities, they may either cooperate or antagonize one another, thereby causing prey mortality rates to be substantially higher or lower than one would expect if predators did not interact. However, we have a limited mechanistic understanding of how prey mortality rates change with predator densities. We re-analyzed a previously published observational dataset to investigate how the foraging response of the coney grouper (Cephalopholis fulva) feeding on the bluehead wrasse (Thalassoma bifasciatum) changed with shifts in predator and prey densities. Using a model-selection approach, we found that per-predator feeding rates were most consistent with a functional response that declines as predator density increases, suggesting either antagonistic interactions among predators or a shared antipredator behavioral response by the prey. Our findings suggest that variation in predator density (natural or anthropogenic) may have substantial consequences for coral reef fish population dynamics.     

CONSEQUENCES OF ALTERNATIVE FUNCTIONAL RESPONSE FORMULATIONS IN MODELS EXPLORING WHALE-FISHERY INTERACTIONS

We evaluated the utility of Ecosim for exploring interactions between cetacean predators, their prey, and fisheries. We formulated six Ecosim parameterizations, representing alternative hypotheses of feeding interactions (functional response) between cetaceans and their main fish prey, and examined differences in the predicted responses to simulated harvesting regimes for minke whales and their prey. Regardless of the type of function response formulated, intense fishing on the main fish prey of minke whales had a longer-lasting negative impact on minke whales than when minke whale biomass was removed directly by harvesting. Consumption rate, biomass, feeding time and mortality of minke whales were all sensitive to the type of functional response specified. Inclusion of "handling time" limited minke whales consumption at high prey densities and predicted higher consumption at low prey densities; features characteristic of a type II functional response. Predicted decline and recovery rates of minke whales were slower than when consumption rates were not limited. Addition of "foraging time" adjustments resulted in more conservative estimates of decline and recovery. However, when "other mortality" was linked to time spent foraging, exposure to higher mortality at low prey densities, and reduced mortality at high prey densities resulted in dramatic differences in predicted biomass trajectory. Sensitivity to the "other mortality" assumption is important for cetaceans whose predation mortality is only a small proportion of total mortality. Differences in the feeding and biomass dynamics were also observed when prey availability to predators was represented by changes in prey vulnerability, confirming earlier reports that Ecosim predictions are sensitive to this parameter.     

Numbers,neighbors, and hungry predators: What makes chemically defended aposematic prey susceptible to predation?

Many chemically defended aposematic species are characterized by relatively low toxin levels, which enables predators to include them in their diets under certain circumstances. Knowledge of the conditions governing the survival of such prey animals—especially in the context of the co‐occurrence of similar but undefended prey, which may result in mimicry‐like interactions—is crucial for understanding the initial evolution of aposematism. In a one‐month outdoor experiment using fish (the common carp Cyprinus carpio) as predators, we examined the survival of moderately defended aposematic tadpole prey (the European common toad Bufo bufo) with varying absolute densities in single‐species prey systems or varying relative densities in two‐species prey systems containing morphologically similar but undefended prey (the European common frog Rana temporaria). The density effects were investigated in conjunction with the hunger levels of the predator, which were manipulated by means of the addition of alternative (nontadpole) food. The survival of the B. bufo tadpoles was promoted by increasing their absolute density in the single‐species prey systems, increasing their relative density in the two‐species prey systems, and providing ample alternative food for the predator. Hungry predators eliminated all R. temporaria individuals regardless of their proportion in the prey community; in treatments with ample alternative food, high relative B. bufo density supported R. temporaria survival. The results demonstrated that moderately defended prey did benefit from high population densities (both absolute and relative), even under long‐term predation pressure. However, the physiological state of the predator was a crucial factor in the survival of moderately defended prey. While the availability of alternative prey in general should promote the spread and maintenance of aposematism, the results indicated that the resemblance between the co‐occurring defended and undefended prey may impose mortality costs on the defended model species, even in the absence of actual mimicry.     

Effects of alternative prey on predation by small mammals on gypsy moth pupae

Previous work shows that predation by small mammals is a dominant cause of mortality of low-density gypsy moths in North America and that declines in small mammal density result in increases in gypsy moth density. Here we examined whether predation by small mammals is density dependent by way of a type III functional response, and how predation is influenced by alternative prey. First we showed that the preference of predators for gypsy moth pupae was low compared to other experimental prey items, such as mealworm pupae and sunflower seeds. Predation on gypsy moth pupae was characterized by a type II functional response with percent predation highest at the lowest prey densities, whereas the functional response to sunflower seeds was characterized by a type III functional response in which predation increased with increasing prey density. These results suggest that predation by small mammals is unlikely to stabilize low-density gypsy moth populations.     

Consequences of size structure in the prey for predator-prey dynamics: the composite functional response

1. Current formulations of functional responses assume that the prey is homogeneous and independent of intraspecific processes. Most prey populations consist of different coexisting size classes that often engage in asymmetrical intraspecific interactions, including cannibalism, which can lead to nonlinear interaction effects. This may be important as the size structure with the prey could alter the overall density-dependent predation rates. 2. In a field experiment with damselfly and dragonfly larvae, 16 treatments manipulated the density of a small prey stage, the presence of large conspecific prey and the presence of heterospecific predators. 3. Size structure in the prey (i.e. when both prey stages were present) decreased the impact of the predator on overall prey mortality by 25-48% at mid and high prey densities, possibly due to density-dependent size-structured cannibalism in the prey. The predation rates on small prey stages were determined by the interaction of large prey and predators. Predation rates increased with prey density in the absence of large prey, but predation rates were constant across densities when large conspecifics were present. 4. The functional response for unstructured prey followed a Holling type III model, but the predation rate for size-structured prey was completely different and followed a complex pattern that could not be explained with any standard functional response. 5. Using additional laboratory experiments, a mortality model was developed and parameterized. It showed that the overall prey mortality of size-structured prey can be adequately predicted with a composite functional response model that modelled the individual functional responses of each prey stage separately and accounted for their cannibalistic interaction. 6. Thus, treating a prey population as a homogeneous entity will lead to erroneous predictions in most real-world food webs. However, if we account for the effects of size structure and the intraspecific interactions on functional responses by treating size classes as different functional groups, it is possible to reliably predict the dynamics of size-structured predator-prey systems.     

Functional feeding responses of piscivorous fishes from the northeast US continental shelf

The functional feeding response forms of piscivorous fishes used in multispecies and ecosystem modeling have been questioned because they were mostly conjectural or solely based on laboratory studies. Here, we investigate the functional feeding response of seven species of piscivorous fishes on four species of their prey from the northeast US continental shelf using field data that spans 30 years. Our study confirmed that Holling’s types II and III functional responses are the most common functional responses for piscivorous fishes in this region. However, our analyses also revealed that differences exist between piscivorous fishes’ functional responses, and, therefore, combining functional responses of piscivores is probably not appropriate in multispecies and ecosystem modeling. In the absence of specific predator–prey functional responses, we suggest that, for cruising, actively attacking predators, a type II functional response is slightly preferable; for a sedentary, ambush predator, a type III functional response is slightly preferable; at low prey densities for a generic fish predator, a type III functional response should be used; and at moderate to high prey densities, either should work sufficiently. Because we have shown that the functional response of a particular predator to individual prey species varies, these relationships must be further evaluated as we continue to develop and employ multispecies and ecosystem modeling.     

Fleeing towards death – leech‐induced behavioural defences increase freshwater snail susceptibility to predatory fish

Prey species are often exposed to multiple predators, which presents several difficulties to prey species. This is especially true when the response to one predator influences the prey’s susceptibility to other predators. Predator‐induced defences have evolved in a wide range of prey species, and experiments involving predators with different hunting strategies allow researchers to evaluate how prey respond to multiple threats. Freshwater snails are known to respond to a variety of predators with both morphological and behavioural defences. Here we studied how freshwater snails Radix balthica responded behaviourally to fish and leech predators, both separately and together. Our aim was to explore whether conflicting predator‐induced responses existed and, if so, what effect they had on snail survival when both predatory fish and leeches were present. We found that although R. balthica increased refuge use when exposed to predatory fish, they decreased refuge use when exposed to predatory leeches. When both predators were present, snails showed a stronger response towards leech than fish and responded by leaving the refuge. This response made the snails more susceptible to fish predation, which increased snail mortality when exposed to both fish and leech compared to fish only. We show that predators that have a relatively low predation rate can substantially increase mortality rates by indirect effects. By forcing snails out of refuges such as rock and macrophyte habitats, leeches can indirectly increase predation from molluscivorous fish and may thus affect snail densities.     

Socializing makes thick-skinned individuals: on the density of epidermal alarm substance cells in cyprinid fish, the crucian carp (Carassius carassius)

In cyprinid fish, density of epidermal club cells (i.e. alarm substance cells) has been found to vary between lakes with different predator fauna. Because predators can be labelled with chemical cues from prey, we questioned if club cell density could be controlled indirectly by predators releasing prey cues. In particular, we suspected a possible feedback mechanism between chemical alarm signals and their cellular source. We raised crucian carp singly and in groups of four. For both rearing types, fish were exposed to skin extracts of either conspecifics or brown trout (without club cells), and provided either low or high food rations. Independent of rearing type, condition factor and club cell density increased with food ration size, but no change was found in club cell density following exposure to conspecific alarm signals. However, the density of club cells was found significantly higher for fish raised in groups than for fish raised alone. We conclude that an increased condition factor results in more club cells, but crucian carp may also possess an awareness of conspecific presence, given by higher club cell densities when raised in groups. This increase in club cell density may be induced by unknown chemical factors released by conspecifics.     

Response of predators to prey abundance: separating the effects of prey density and patch size

We tested the relative and combined effects of prey density and patch size on the functional response (number of attacks per unit time and duration of attacks) of a predatory reef fish (Cheilodactylus nigripes (Richardson)) to their invertebrate prey. Fish attacked prey at a greater rate and for longer time in large than small patches of prey, but large patches had naturally greater densities of prey. We isolated the effects of patch size and prey density by reducing the density of prey in larger patches to equal that of small patches; thereby controlling for prey density. We found that the intensity at which fish attacked prey (combination of attack rate and duration) was primarily a response to prey density rather than the size of patch they occupied. However, there was evidence that fish spent more time foraging in larger than smaller patches independent of prey density; presumably because of the greater total number of prey available. These experimental observations suggest that fish can distinguish between different notions of prey abundance in ways that enhance their rate of consumption. Although fish may feed in a density dependent manner, a critical issue is whether their rate of consumption outstrips the rate of increase in prey abundance to cause density dependent mortality of prey.     

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.     

Effects of satiation on feeding and swimming behaviour of planktivores

Hunger affects the feeding and swimming behaviour in fish. After 36 h of food deprivation, the feeding and swimming behaviour of Pseudorasbora parva (Cyprinidae) was studied under different prey densities (0.5, 1, 2, 5, 10 and 25 of Daphnia pulex per liter). The initial feeding rates showed marked variations in relation to prey availability. Under high prey densities, the initial feeding rate of fish was higher and subsequently decreased faster, when compared to those feeding under low prey densities. At higher prey densities, two factors were involved: that of higher prey encounter rates and also the attainment of food satiation at a faster rate. Across all prey densities, the feeding rates of fish reached a plateau after satiation. The swimming speed of fish was found to be negatively related to the prey density and a significant change in swimming speed was noted as being directly related to the level of satiation. It was found that the increasing satiation level greatly influenced the handling time and reactive volume of predator, which finally caused reduced feeding rates.     

Natural selection and population density-feedback II. The evolution of functional response curves

The nature of the functional response may be qualitatively understood as follows. Sigmoid responses to one food type may arise, in the presence of alternate foods, as a result of optimal feeding and foraging behavior. Sigmoid curves resulting from this cause I term class A curves. The same curve may also arise in the absence of alternate foods as a result of learning, individual variations in the level of food density at which predators begin feeding, or training effects. The latter I have termed class B curves. At very high food densities, a drop in food intake per predator might occur because of the tendency for predators to take easily found and captured items first and to become more selective when food is very common. Such “dome-shaped” curves have been found in the laboratory but should be rare in nature. Computer simulation of a three trophic-level system, using the phenotypic selection model of Emlen, indicates that natural selection acting on prey should encourage sigmoidality in the predator's class B functional response, at least in disturbed environments. The opposite force arises from selection acting on predators. However, given the magnitudes of growth efficiencies (see Eq. (8), it appears that at least for terrestrial vertebrates, selection on prey species is more important than selection on predators for determining functional responses. Accordingly, prey-predator systems occupying highly variable environments are expected to show more marked type III (class B) curves than systems in more stable areas. Finally, the role of functional response for prey-predator stability is discussed. Class A (alternate food) responses may result in population control for prey in multiple prey systems. Peterman and Pikitch have modeled systems in which type III functional response by predators, in systems where predation varies independently of prey, may lead to double equilibria. This picture is clouded, however, when predator populations are interactive with their food, though double equilibria are still possible (J. M. Emlen, 1984, “Population Biology: The Coevolution of Population Dynamics and Behavior,” Macmillan, New York, in press).     

Competition for space by predators in streams: field experiments on a net-spinning caddisfly

SUMMARY. 1. Field experiments in a fishless stream were carried out on an abundant caddisfly with a predatory, net-spinning larva, Plectrocnemia conspersa (Curtis), to assess whether net site availability affects their microdistribution.
2. Net sites were supplemented by adding nought, one or four artificial structures to replicated patches on the stream bed. In each of three experiments at different seasons (summer, autumn and late winter), caddis densities increased significantly in patches with extra net sites.
3. The response of caddis to supplemented net sites could be affected by the subsidiary effects of food and offish. These potential interactions were assessed in each experiment by varying net site density in two additional treatment stretches in which (1) prey abundance was increased by releasing Daphnia , and (2) brown trout ( Salmo trutta L.) were enclosed. The responses of caddis in these two treatments were compared to that in the reference stretch, where only net site density varied.
4. Increased food abundance enhanced the response of caddis to net site supplementation in winter, when natural prey was least abundant, but not in summer or autumn. We suggest that extra food affects the mechanism determining net building only when prey availability is below some threshold.
5. The presence of fish precluded any effect of extra net sites in summer, but had no effect in autumn (the winter fish treatment was lost). We suggest fish predation reduced the densities of caddis in summer, so that net sites no longer limited local densities. In autumn, fallen leaves provided refugia from fish, which consequently were less effective predators of P. conspersa.     

Prey and predator density‐dependent interactions under different water volumes

Predation is a critical ecological process that directly and indirectly mediates population stabilities, as well as ecosystem structure and function. The strength of interactions between predators and prey may be mediated by multiple density dependences concerning numbers of predators and prey. In temporary wetland ecosystems in particular, fluctuating water volumes may alter predation rates through differing search space and prey encounter rates. Using a functional response approach, we examined the influence of predator and prey densities on interaction strengths of the temporary pond specialist copepod Lovenula raynerae preying on cladoceran prey, Daphnia pulex, under contrasting water volumes. Further, using a population dynamic modeling approach, we quantified multiple predator effects across differences in prey density and water volume. Predators exhibited type II functional responses under both water volumes, with significant antagonistic multiple predator effects (i.e., antagonisms) exhibited overall. The strengths of antagonistic interactions were, however, enhanced under reduced water volumes and at intermediate prey densities. These findings indicate important biotic and abiotic contexts that mediate predator–prey dynamics, whereby multiple predator effects are contingent on both prey density and search area characteristics. In particular, reduced search areas (i.e., water volumes) under intermediate prey densities could enhance antagonisms by heightening predator–predator interference effects.     

Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge

Predicting the consequences of predator biodiversity loss on prey requires an understanding of multiple predator interactions. Predators are often assumed to have independent and additive effects on shared prey survival; however, multiple predator effects can be non-additive if predators foraging together reduce prey survival (risk enhancement) or increase prey survival through interference (risk reduction). In marine communities, juvenile reef fish experience very high mortality from two predator guilds with very different hunting modes and foraging domains—benthic and pelagic predator guilds. The few previous predator manipulation studies have found or assumed that mortality is independent and additive. We tested whether interacting predator guilds result in non-additive prey mortality and whether the detection of such effects change over time as prey are depleted. To do so, we examined the roles of benthic and pelagic predators on the survival of a juvenile shoaling zooplanktivorous temperate reef fish, Trachinops caudimaculatus, on artificial patch reefs over 2 months in Port Phillip Bay, Australia. We observed risk enhancement in the first 7 days, as shoaling behaviour placed prey between predator foraging domains with no effective refuge. At day 14 we observed additive mortality, and risk enhancement was no longer detectable. By days 28 and 62, pelagic predators were no longer significant sources of mortality and additivity was trivial. We hypothesize that declines in prey density led to reduced shoaling behaviour that brought prey more often into the domain of benthic predators, resulting in limited mortality from pelagic predators. Furthermore, pelagic predators may have spent less time patrolling reefs in response to declines in prey numbers. Our observation of the changing interaction between predators and prey has important implications for assessing the role of predation in regulating populations in complex communities.     

How does the presence of a conspecific individual change the behavioral game that a predator plays with its prey?

Behavioral games predators play among themselves may have profound effects on behavioral games predators play with their prey. We studied the behavioral game between predators and prey within the framework of social foraging among predators. We tested how conspecific interactions among predators (little egret) change the predator–prey behavioral game and foraging success. To do so, we examined foraging behavior of egrets alone and in pairs (male and female) in a specially designed aviary consisting of three equally spaced pools with identical initial prey (comet goldfish) densities. Each pool was comprised of a risky microhabitat, rich with food, and a safe microhabitat with no food, forcing the fish to trade off food and safety. When faced with two versus one egret, we found that fish significantly reduced activity in the risky habitat. Egrets in pairs suffered reduced foraging success (negative intraspecific density dependence) and responded to fish behavior and to their conspecific by changing their visiting regime at the different pools—having shorter, more frequent visits. The time egret spent on each visit allowed them to match their long-term capture success rate across the environment to their capture success rate in the pool, which satisfies one aspect of optimality. Overall, egrets in pairs allocated more time for foraging and changed their foraging tactics to focus more on fish under cover and fish ‘peeping’ out from their shelter. These results suggest that both prey and predator show behavioral flexibility and can adjust to changing conditions as needed in this foraging game.     

The role of trout in stream food webs: integrating evidence from field surveys and experiments

1. We evaluated the effects of brown trout on boreal stream food webs using field surveys and enclosure/exclosure experiments. Experimental results were related to prey preference of uncaged trout in the same stream, as well as to a survey of macroinvertebrate densities in streams with vs. without trout. Finally, we assessed the generality of our findings by examining salmonid predation on three groups of macroinvertebrate prey (chironomid midges, epibenthic grazers, invertebrate predators) in a meta-analysis. 2. In a preliminary experiment, invertebrate predators showed a strong negative response to trout, whereas chironomids benefited from trout presence. In the main experiment, trout impact increased with prey size. Trout had the strongest effect on invertebrate predators and cased caddis larvae, whereas Baetis mayfly and chironomid larvae were unaffected. Trout impact on the largest prey seemed mainly consumptive, because prey emigration rates were low and independent of fish presence. Despite strong effects on macroinvertebrates, trout did not induce a trophic cascade on periphyton. Uncaged trout showed a strong preference for the largest prey items (predatory invertebrates and aerial prey), whereas Baetis mayflies and chironomids were avoided by trout. 3. Densities of invertebrate predators were significantly higher in troutless streams. Baetis mayflies also were less abundant in trout streams, whereas densities of chironomids were positively, although non-significantly, related to trout presence. Meta-analysis showed a strong negative impact of trout on invertebrate predators, a negative but variable impact on mobile grazers (mainly mayfly larvae) and a slightly positive impact on chironomid larvae. 4. Being size-selective predators, salmonid fishes have a strong impact on the largest prey types available, and this effect spans several domains of scale. Discrepancies between our experimental findings and those from the field survey and meta-analysis show, however, that for most lotic prey, small-scale experiments do not reflect fish impact reliably at stream-wide scales. 5. Our findings suggest that small-scale experiments will be useful only if the experimental results are evaluated carefully against natural history information about the experimental system and interacting species across a wide array of spatial scales.     

Influence of density dependence on predator-prey seabird interactions at large spatio-temporal scales

Theoretical investigations of competitive dynamics have noted that numbers of predator and prey influence each other. However, few empirical studies have demonstrated how a life-history trait of the prey (such as fecundity) can be affected simultaneously by its own density and the density of predators. For instance, density dependence can reduce fecundity with increasing number of prey, while inverse density dependence or Allee effects may occur especially when the prey is a social organism. Here we analysed an intraguild predator-prey system of two seabird species at a large spatio-temporal scale. As expected, we found that fecundity of prey was negatively affected by predator density. Nevertheless, fecundity of prey also increased nonlinearly with its own density and strikingly with the prey-predator ratio. Small groups of prey were probably not able to defend their nests especially against large number of predators. At the highest prey densities (i.e. when anti-predator strategies should be most efficient), prey fecundity also lowered, suggesting the appearance of density dependence mediated by food competition. Allee effects and density dependence occurred across a broad range of population sizes of both the prey and the predator at several local populations facing different ecological environments.     

Interactions between adult and larval bluegill sunfish: positive and negative effects

Adult fish may affect the growth and survival of conspecific larvae through a variety of pathways, including negative interactions via competition for shared limiting resources or via predation (i.e., cannibalism), and positive interactions due to the consumption of larval predators and via resource enhancement (i.e., presence of adults increases availability of larval prey). To examine the overall effect of adult bluegill sunfish (Lepomis macrochirus) on larval bluegill, we conducted a field experiment in which we manipulated adult densities and quantified larval growth and survival, prey abundance, invertebrate predator abundance, and cannibalism. The presence of adult bluegill had a negative effect on final larval mass. This response was consistent with competition for zooplankton prey. Adult bluegill reduced the abundance of large zooplankton (e.g., Chaoborus and Daphnia), which were the dominant prey of bluegill larvae in the absence of adults. Larvae in the no-adult treatment also had significantly more prey in their stomachs compared to larvae in the presence of adults. Larval survival was maximized at intermediate adult densities and the overall production of larvae peaked at intermediate adult densities. The higher larval survival at intermediate adult densities is attributed to a reduction in invertebrate predators in treatments with adult bluegill; invertebrate predators experienced an 80% reduction in the presence of adult fish. Decreased larval survival at the highest adult density was not due to resource limitation and may be due to cannibalism, which was not directly observed in our study, but has been observed in other studies.     

Effects of bottom trawling on fish foraging and feeding

The effects of bottom trawling on benthic invertebrates include reductions of biomass, diversity and body size. These changes may negatively affect prey availability for demersal fishes, potentially leading to reduced food intake, body condition and yield of fishes in chronically trawled areas. Here, the effect of trawling on the prey availability and diet of two commercially important flatfish species, plaice (Pleuronectes platessa) and dab (Limanda limanda), was investigated over a trawling intensity gradient in the Irish Sea. Previous work in this area has shown that trawling negatively affects the condition of plaice but not of dab. This study showed that reductions in local prey availability did not result in reduced feeding of fish. As trawling frequency increased, both fish and prey biomass declined, such that the ratio of fish to prey remained unchanged. Consequently, even at frequently trawled sites with low prey biomass, both plaice and dab maintained constant levels of stomach fullness and gut energy contents. However, dietary shifts in plaice towards energy-poor prey items were evident when prey species were analysed individually. This, together with a potential decrease in foraging efficiency due to low prey densities, was seen as the most plausible cause for the reduced body condition observed. Understanding the relationship between trawling, benthic impacts, fish foraging and resultant body condition is an important step in designing successful mitigation measures for future management strategies in bottom trawl fisheries.