On the implications of predator avoidance

The question to what extent predators regulate the populations of their food species has a long history of debate, and today top-down control of plankton dynamics still is a major issue in limnology. Over the last decade a fascinating extra dimension of this topic has been revealed. Fish, zooplankton and algae can sense their potential predators through chemical cues and adjust their life style in a flexible way to minimize the risk of being eaten. Although much progress has been made in elucidating the mechanisms involved, the implications of such predation avoidance for the potential of predators to reduce the abundance of their food populations are still poorly understood. Model analyses suggest that predation avoidance leads to more stable food webs in which the effects of nutrient enrichment are more evenly distributed over the trophic levels. In this article it is argued that the cost which predation avoidance usually has in terms of food conditions implies a tricky caveat in interpreting observations on predation rates and nutritional status in natural populations. Prey that sense the presence of predators and aggregates at safe sites where food conditions are poor, may appear starved and actual predation losses may be low. Such observations suggest that food limitation is the dominant force limiting their population development, but although starvation may indeed be the proximate cause of poor growth and reproduction, predation is clearly the ultimate factor involved in this situation. Thus when predation avoidance occurs, standard demographic analyses will tend to underestimate the importance of predators in regulating the dynamics of their prey in the field.     

Seasonal migration determined by a trade-off between predator avoidance and growth

Migration is a common phenomenon in many organisms, terrestrial as well as aquatic, and considerable effort has been spent to understand the evolution of migratory behaviour and its consequences for population and community dynamics. In aquatic systems, studies on migration have mainly been focused on commercially important fish species, such as salmon and trout. However, seasonal mass-migrations may occur also among other freshwater fish, e.g. in cyprinids that leave lakes and migrate into streams and wetlands in the fall and return back to the lake in spring. In a conceptual model, we hypothesized that this is an adaptive behaviour in response to seasonal changes in predation (P) and growth (G) and that migrating fish change habitat so as to minimise the ratio between predation mortality and growth rate (P/G). Estimates from bioenergetic modelling showed that seasonal changes in the ratio between predator consumption rate and prey growth rate followed the predictions from the conceptual model and also gave more precise predictions for the timing of the habitat change. By quantifying the migration of more than 1800 individually marked fish, we showed that actual migration patterns followed predictions with a remarkable accuracy, suggesting that migration patterns have evolved in response to seasonally fluctuating trade-offs between predator avoidance and foraging gains. Thus, the conceptual model provides a mechanistic understanding to mass-migration in prey fish. Further, we also show that the dominant prey fish is actually absent from the lake during a major part of the year, which should have strong implications for the dynamics of the lake ecosystem through direct and indirect food-web interactions.     

Shovelnose sturgeon exhibit predator avoidance behaviour in the presence of a hungry predator

An experiment was designed to test whether age‐0 shovelnose sturgeon (Scaphirhynchus platorynchus) exhibited predator avoidance behaviour in response to a channel catfish (Ictalurus punctatus) predator. It was hypothesized that shovelnose sturgeon would not exhibit any innate predator avoidance behaviour because previous reports have shown a congener of the shovelnose sturgeon, the pallid sturgeon (S. albus), to be an unfavourable prey item for channel catfish. The results, however, indicated that shovelnose sturgeon generally avoided space occupied by the catfish predator and spent a greater proportion of time in the predator avoidance zone within the experimental tank. Bitten fish, in particular, spent a greater period of time in the predator avoidance zone. Of all sturgeon used in this experiment (N = 30), 73% swam within the fork length (350 mm) of the catfish predator. The results seem to indicate that shovelnose sturgeon were initially oblivious to the risk of predation by the catfish predator, but after interaction (e.g. being chased or bitten) appeared to display predator avoidance behaviour. Predator avoidance behaviour in shovelnose sturgeon may thus be suggested as a learned rather than an innate behaviour.     

Spatial interactions between sympatric carnivores: asymmetric avoidance of an intraguild predator

Interactions between intraguild species that act as both competitors and predator–prey can be especially complex. We studied patterns of space use by the black-footed ferret (Mustela nigripes), a prairie dog (Cynomys spp.) specialist, and the American badger (Taxidea taxus), a larger generalist carnivore that competes for prairie dogs and is known to kill ferrets. We expected that ferrets would spatially avoid badgers because of the risk of predation, that these patterns of avoidance might differ between sexes and age classes, and that the availability of food and space might influence these relationships. We used location data from 60 ferrets and 15 badgers to model the influence of extrinsic factors (prairie dog density and colony size) and intrinsic factors (sex, age) on patterns of space use by ferrets in relation to space use by different sex and age categories of badgers. We documented asymmetric patterns of avoidance of badgers by ferrets based on the sex of both species. Female ferrets avoided adult female badgers, but not male badgers, and male ferrets exhibited less avoidance than female ferrets. Additionally, avoidance decreased with increasing densities of prairie dogs. We suggest that intersexual differences in space use by badgers create varying distributions of predation risk that are perceived by the smaller carnivore (ferrets) and that females respond more sensitively than males to that risk. This work advances understanding about how competing species coexist and suggests that including information on both intrinsic and extrinsic factors might improve our understanding of behavioral interactions between sympatric species.     

Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits

Predation is a strong selective force with both direct and indirect effects on an animal’s fitness. In order to increase the chances of survival, animals have developed different antipredator strategies. However, these strategies have associated costs, so animals should assess their actual risk of predation and shape their antipredator effort accordingly. Under a stressful situation, such as the presence of predators, animals display a physiological stress response that might be proportional to the risk perceived. We tested this hypothesis in wild European rabbits (Oryctolagus cuniculus), subjected to different predator pressures, in Doñana National Park (Spain). We measured the concentrations of fecal corticosterone metabolites (FCM) in 20 rabbit populations. By means of track censuses we obtained indexes of mammalian predator presence for each rabbit population. Other factors that could modify the physiological stress response, such as breeding status, food availability and rabbit density, were also considered. Model selection based on information theory showed that predator pressure was the main factor triggering the glucocorticoid release and that the physiological stress response was positively correlated with the indexes of the presence of mammalian carnivore predators. Other factors, such as food availability and density of rabbits, were considerably less important. We conclude that rabbits are able to assess their actual risk of predation and show a threat-sensitive physiological response.     

The evolution of traits affecting resource acquisition and predator vulnerability: character displacement under real and apparent competition

This article investigates some simple models of the evolutionary interaction between two prey species that share a common resource and a common predator. Each prey species is characterized by a trait that determines both the rate of resource capture and vulnerability to a predator. In a simple model of a three-species food chain, such traits usually increase in response to an imposed reduction in resource density. When the per capita growth rates of each of two prey species depend linearly on resource density, such traits will change in opposite directions when the two prey come into sympatry. In addition, the ratio of the effect of the predator on prey fitness to the effect of the resource on prey fitness will diverge from the corresponding ratio in a second prey species when those species coexist in sympatry. These simple predictions need not hold under several alternative assumptions, which may be more common in biological systems. Parallel changes in sympatry may occur if the relationship between resource consumption and prey growth is nonlinear, if the prey species have partial overlap in the set of resources used or in the set of predators that consume them, or if prey experience direct intraspecific competition. The responses to a second prey can also differ significantly from those predicted by the simplest model if separate traits affect vulnerability to predators and resource acquisition rate. It is important to determine whether examples of character displacement previously interpreted as responses to competition for resources might also reflect responses to altered predation risks in sympatry.     

Oviposition-site shift in phytophagous mites reflects a trade-off between predator avoidance and rainstorm resistance

Predators can reduce prey population densities by driving them to undertake costly defences. Here, we report on a remarkable example of induced antipredator defence in spider mites that enhances the risk to rainstorms. Spider mites live on the undersides of host plant leaves and usually oviposit on the leaf undersurface. When they are threatened by predatory mites, they oviposit on three-dimensional webs to avoid egg predation, although the cost of ovipositing on webs has not yet been clearly determined. We prepared bean plants harbouring spider mite (Tetranychus kanzawai) eggs on either leaf surfaces or webs and exposed them to rainstorms outdoors. We found that fewer eggs remained on webs than on leaf surfaces. We then examined the synergistic effect of wind and rain by simulating both in the laboratory. We conclude that ovipositing on webs comes at a cost, as eggs are washed off the host plants by wind and rain. This may explain why spider mite populations decrease drastically in the rainy season, although they inhibit leaf undersides where they are not directly exposed to rainfall.     

The trade-off between feeding, mate seeking and predator avoidance in copepods: behavioural responses to chemical cues

The behavioural responses of adult Temora longicornis to chemicalsignals from predators and potential sexual partners was studiedusing an automated three-dimensional (3-D) tracking system anda 2-D high-resolution filming set-up. The animals adapted theirswimming speed and turning behaviour in reaction to chemicalsignals to increase or decrease encounter probability with otherorganisms. Female copepods were shown to react to the smellof males with little ‘hops’, quite distinct fromboth their normal smooth swimming motion and escape responses.These hops are likely to be signals intended to increase theencounter probability with males. Swimming behaviour was shownto be a trade-off between conflicting motivations such as predatoravoidance on the one hand, and the search for food and sexualpartners on the other.     

From overlooking to concealed: predator avoidance in an apex carnivore

Many prey species select bed sites that reduce the risk of being caught off guard. We investigated bed sites used by an apex predator (gray wolf, Canis lupus) before and after individuals were approached by humans (N?=?48 trials). On 9 out of 10?days, the unprovoked wolves rested at sites high in the terrain with a good overview (overlooking sites). After being approached, they resettled on more concealed sites lower in the terrain. Solitary yearlings used less overlooking sites than adults both before and after disturbance. The study provides experimental evidence that wolves’ behavioural response to approaching humans is analogous to predator avoidance in prey species.     

Genetic control of predator avoidance behaviour in Daphnia

1. The vertical migration behaviour in electrophoretically distinguishable clones of Daphnia magna Straus was investigated. 2. Clones differed significantly in their tendency to stay near the surface of the tank during the light phase of the daily light/dark cycle, indicating that vertical migration has a genetic component. 3. There was a significant difference in behaviour between juvenile and adult Daphnia: overall the juveniles stayed closer to the water surface than the adults, but the characteristic pattern of clonal differences persisted in the juveniles. 4. When an adult population of each clone was exposed to a fish predator in an experimental tank, the position a clone maintained in the tank at the start of the day had a direct effect on its survival. Clones remaining near to the surface of the water suffered greatest predarion.     

The mate pursuit-predation avoidance tradeoff in the virile crayfish, Orconectes virilis

To better understand the tradeoff between mate pursuit and predation risk avoidance, the responses of male virile crayfish (Orconectes virilis) to female sex pheromone and conspecific alarm cue, alone and in combination were tested. Male crayfish were more active and exhibited less antipredator behavior in the pheromone treatment than in either the pheromone + alarm or alarm treatment. The results suggest a tradeoff in favor of risk avoidance when pheromone and risk stimuli are encountered together.     

The mate pursuit-predation avoidance tradeoff in the virile crayfish,Orconectes virilis

To better understand the tradeoff between mate pursuit and predation risk avoidance, the responses of male virile crayfish (Orconectes virilis) to female sex pheromone and conspecific alarm cue, alone and in combination were tested. Male crayfish were more active and exhibited less antipredator behavior in the pheromone treatment than in either the pheromone?+?alarm or alarm treatment. The results suggest a tradeoff in favor of risk avoidance when pheromone and risk stimuli are encountered together.     

Ecology shapes the evolutionary trade‐off between predator avoidance and defence in coral reef butterflyfishes

Antipredator defensive traits are thought to trade‐off evolutionarily with traits that facilitate predator avoidance. However, complexity and scale have precluded tests of this prediction in many groups, including fishes. Using a macroevolutionary approach, we test this prediction in butterflyfishes, an iconic group of coral reef inhabitants with diverse social behaviours, foraging strategies and antipredator adaptations. We find that several antipredator traits have evolved adaptively, dependent primarily on foraging strategy. We identify a previously unrecognised axis of diversity in butterflyfishes where species with robust morphological defences have riskier foraging strategies and lack sociality, while species with reduced morphological defences feed in familiar territories, have adaptations for quick escapes and benefit from the vigilance provided by sociality. Furthermore, we find evidence for the constrained evolution of fin spines among species that graze solely on corals, highlighting the importance of corals, as both prey and structural refuge, in shaping fish morphology.     

Shifting the balance between foraging and predator avoidance: the importance of food distribution for a schooling pelagic forager

It is widely held that when predator avoidance conflicts with other activities, such as feeding, avoidance of predators often takes precedence. In this study, we examine how predation risk and food distribution interact to influence the schooling behavior and swimming speed of foraging juvenile walleye pollock, Theragra chalcogramma. Fish were acclimated to either spatially and temporally clumped, or spatially and temporally dispersed food for 3 weeks. Fish were then monitored while feeding in the absence and presence of predatory sablefish, Anoplopoma fimbria. Fish foraging for clumped food swam rapidly in a loose school when predators were absent, but swam more slowly and adopted more cohesive schooling in the presence of predators, trading-off foraging opportunity for decreased vulnerability to predators. Fish foraging for dispersed food swam about slowly and did not engage in cohesive schooling in either the absence or presence of predators. These fish accepted greater predation risk in order to continue foraging, suggesting that the cost of schooling, in terms of decreased foraging opportunity, was greater when food was dispersed than when it was clumped. This lower responsiveness to predators among fish receiving dispersed food demonstrates that predator avoidance does not always take precedence over other activities, but rather, that a balance is maintained between predator avoidance and feeding, which shifts as food distribution changes.