A test of the risk allocation hypothesis: tadpole responses to temporal change in predation risk

The risk allocation hypothesis predicts that temporal variationin predation risk can influence how animals allocate feedingbehavior among situations that differ in danger. We testedthe risk allocation model with tadpoles of the frog Rana lessonae,which satisfy the main assumptions of this model because theymust feed to reach metamorphosis within a single season, theirbehavioral defense against predators is costly, and they canrespond to changes in risk integrated over time. Our experiment switched tadpoles between artificial ponds with different numbersof caged dragonfly larvae and held them at high and low riskfor different portions of their lives. Tadpoles responded stronglyto predators, but they did not obey the risk allocation hypothesis:as the high-risk environment became more dangerous, there wasno tendency for tadpoles to allocate more feeding to the low-riskenvironment, and as tadpoles spent more time at risk, they didnot increase feeding in both environments. Our results suggestthat the model might be more applicable when the time spentunder high predation risk is large relative to the time requiredto collect resources.     

Biogeographic variation in behavioral and morphological responses to predation risk

The expression of prey antipredator defenses is often related to ambient consumer pressure, and prey express greater defenses under intense consumer pressure. Predation is generally greater at lower latitudes, and antipredator defenses often display a biogeographic pattern. Predation pressure may also vary significantly between habitats within latitudes, making biogeographic patterns difficult to distinguish. Furthermore, invasive predators may also influence the expression of prey defenses in ecological time. The purpose of this study was to determine how these factors influence the strength of antipredator responses. To assess patterns in prey antipredator defenses based upon geographic range (north vs. south), habitat type (wave-protected vs. wave-exposed shores), and invasive predators, we examined how native rock (Cancer irroratus) and invasive green (Carcinus maenas) crab predators influence the behavioral and morphological defenses of dogwhelk (Nucella lapillus) prey from habitats that differ in wave exposure across an ~230 km range within the Gulf of Maine. The expression of behavioral and morphological antipredatory responses varied according to wave exposure, geographic location, and predator species. Dogwhelks from areas with an established history with green crabs exhibited the largest behavioral and morphological antipredator responses to green crabs. Dogwhelk behavioral responses to rock crabs did not vary between habitats or geographic regions, although morphological responses were greater further south where predation pressure was greatest. These findings suggest that dogwhelk responses to invasive and native predators vary according to geographic location and habitat, and are strongly affected by ambient predation pressure due to the invasion history of an exotic predator.     

Seasonal variation of tadpole spatial niches in permanent streams: The roles of predation risk and microhabitat availability

Phenotypic plasticity can improve fitness in unstable environments and can be expressed in many traits, such as life history attributes, growth and behavioural features. Microhabitat choice can have important consequences for development and survival of aquatic organisms and is expected to vary in response to stimuli, such as predation risk, food availability and temperature. At seasonal sites, microhabitat availability and associated benefits may change from season to season, which might lead to altered patterns of microhabitat use by tadpoles. We investigated this hypothesis in 17 streams from two localities in south‐eastern Brazil. We tested whether water level drops significantly during the dry season, whether lower water level results in altered microhabitat availability and whether predation risk changes between seasons, based on predator density. We then tested whether tadpoles change their pattern of microhabitat use, their spatial niche breadth (given by diversity of used microhabitats) and spatial niche overlap (in the case of co‐occurring species). We were able to include in our analyses tadpoles of four species of Hylidae, that occurred throughout both seasons. Stream depth decreased in the dry season, but microhabitat availability remained relatively stable in many streams, and predator density did not change significantly. Tadpoles of three out of the four species studied were more abundant during the dry season, which may be an adaptation to adjust time of metamorphosis to the rainy season. Tadpoles changed their patterns of microhabitat use between seasons, although the potential causing factors investigated did not seem to be responsible. Tadpole plasticity in microhabitat use may indicate the existence of selective pressures that vary through time and space and are still not well understood.     

Correlated geographic variation in predation risk and antipredator behaviour within a wide‐ranging snake species (Notechis scutatus,Elapidae)

Geographic variation in antipredator behaviour within wide‐ranging species may be driven by both genetic and environmental influences. We quantified antipredator responses in neonatal (laboratory born, n = 555) and adult (field caught, n = 346) tiger snakes (Notechis scutatus) from 11 mainland and island sites in southern Australia. We used these data to test predictions from Bonnet et al.'s hypothesis that the vigour of antipredator responses in this species reflects behavioural plasticity (in turn, driven by an individual snake's exposure to predators during its lifetime) rather than by genetic variation in this trait. We used the number of predator taxa in each area as an index of predator risk. As predicted, adult snakes from predator‐rich areas had more vigorous defensive responses when handled, whereas neonatal behaviour (although also variable among populations) was unrelated to predator species richness. Adult males bit more readily than adult females (as expected from the greater predation exposure of males during mate searching) but no such sex difference was evident in neonates. Although alternative models remain possible, our data are most consistent with the hypothesis that geographic divergence in antipredator tactics within this species primarily reflects developmentally plastic responses to local predation risk.     

Cooperation under predation risk: experiments on costs and benefits

Two fish that cooperatively inspect a predator may have negotiated the share of the risk that each takes. A test of both the costs of predator inspection dependent on the distance from which the predator is approached and the potential benefits of cooperation was carried out strictly experimentally. We made either singletons or pairs of dead sticklebacks, Gasterosteus aculeatus, approach hungry pike, Esox lucius, by remote control according to an algorithm that mimicked natural inspection. The predation risk of both single inspectors and parallel inspecting pairs increased with closer inspection distances. A member of an inspecting pair had only about half the risk of that of a single inspector. In pairs, a companion diluted the lead fish''s risk of being caught, depending on its distance behind the leader. The absolute risk difference between leader and follower was greatest for close inspection distances and decreased further away from the predator. The leader''s relative risk increased with its distance ahead of the laggard. However, for a given distance between leader and laggard, the relative risks of the two fish remained similar with distance from the predator. The cost side of the inequalities that define a ''Prisoner''s Dilemma'' has thus been measured for this system. In a second experiment the ''attack deterrence hypothesis'' of predator inspection (i.e. inspection decreases attack probability) was tested. The pike was offered a choice between two sticklebacks, one of which had carried out a predator inspection visit. There was no indication of attack deterrence through predator inspection.     

Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback

1. Adaptive maternal programming occurs when mothers alter their offspring's phenotype in response to environmental information such that it improves offspring fitness. When a mother's environment is predictive of the conditions her offspring are likely to encounter, such transgenerational plasticity enables offspring to be better-prepared for this particular environment. However, maternal effects can also have deleterious effects on fitness.2. Here, we test whether female threespined stickleback fish exposed to predation risk adaptively prepare their offspring to cope with predators. We either exposed gravid females to a model predator or not, and compared their offspring's antipredator behaviour and survival when alone with a live predator. Importantly, we measured offspring behaviour and survival in the face of the same type of predator that threatened their mothers (Northern pike).3. We did not find evidence for adaptive maternal programming; offspring of predator-exposed mothers were less likely to orient to the predator than offspring from unexposed mothers. In our predation assay, orienting to the predator was an effective antipredator behaviour and those that oriented, survived for longer.4. In addition, offspring from predator-exposed mothers were caught more quickly by the predator on average than offspring from unexposed mothers. The difference in antipredator behaviour between the maternal predator-exposure treatments offers a potential behavioural mechanism contributing to the difference in survival between maternal treatments.5. However, the strength and direction of the maternal effect on offspring survival depended on offspring size. Specifically, the larger the offspring from predator-exposed mothers, the more vulnerable they were to predation compared to offspring from unexposed mothers.6. Our results suggest that the predation risk perceived by mothers can have long-term behavioural and fitness consequences for offspring in response to the same predator. These stress-mediated maternal effects can have nonadaptive consequences for offspring when they find themselves alone with a predator. In addition, complex interactions between such maternal effects and offspring traits such as size can influence our conclusions about the adaptive nature of maternal effects.     

Temporal variation in site fidelity: scale-dependent effects of forage abundance and predation risk in a non-migratory large herbivore

Large herbivores are typically confronted by considerable spatial and temporal variation in forage abundance and predation risk. Although animals can employ a range of behaviours to balance these limiting factors, scale-dependent movement patterns are expected to be an effective strategy to reduce predation risk and optimise foraging opportunities. We tested this prediction by quantifying site fidelity of global positioning system-collared, non-migratory female elk (Cervus canadensis manitobensis) across multiple nested temporal scales using a long-established elk–wolf (Canis lupus) system in Manitoba, Canada. Using a hierarchical analytical approach, we determined the combined effect of forage abundance and predation risk on variation in site fidelity within four seasons across four nested temporal scales: monthly, biweekly, weekly, daily. Site fidelity of female elk was positively related to forage-rich habitat across all seasons and most temporal scales. At the biweekly, weekly and daily scales, elk became increasingly attached to low forage habitat when risk was high (e.g. when wolves were close or pack sizes were large), which supports the notion that predator-avoidance movements lead to a trade-off between energetic requirements and safety. Unexpectedly, predation risk at the monthly scale increased fidelity, which may indicate that elk use multiple behavioural responses (e.g. movement, vigilance, and aggregation) simultaneously to dilute predation risk, especially at longer temporal scales. Our study clearly shows that forage abundance and predation risk are important scale-dependent determinants of variation in site fidelity of non-migratory female elk and that their combined effect is most apparent at short temporal scales. Insight into the scale-dependent behavioural responses of ungulate populations to limiting factors such as predation risk and forage variability is essential to infer the fitness costs incurred.     

Population divergence in growth rate and antipredator defences in Rana arvalis

Growth and development rates often differ among populations of the same species, yet the factors maintaining this differentiation are not well understood. We investigated the antipredator defences and their efficiency in two moor frog Rana arvalis populations differing in growth and development rates by raising tadpoles in outdoor containers in the nonlethal presence and absence of three different predators (newt, fish, dragonfly larva), and by estimating tadpole survival in the presence of free-ranging predators in a laboratory experiment. Young tadpoles in both populations reduced activity in the presence of predators and increased hiding behaviour in the presence of newt and fish. Older tadpoles from the slow-growing Gotland population (G) had stronger hiding behaviour and lower activity in all treatments than tadpoles from the fast-growing Uppland population (U). However, both populations showed a plastic behavioural response in terms of reduced activity. The populations differed in induced morphological defences especially in response to fish. G tadpoles responded with relatively long and deep body, short tail and shallow tail muscle, whereas the responses in U tadpoles were often the opposite and closer to the responses induced by the other predators. U tadpoles metamorphosed earlier, but at a similar size to G tadpoles. There was no evidence that growth rate was affected by predator treatments, but tadpoles metamorphosed later and at larger size in the predator treatments. G tadpoles survived better in the presence of free-ranging predators than U tadpoles. These results suggest that in these two populations, low growth rate was linked with low activity and increased hiding, whereas high growth rate was linked with high activity and less hiding. The differences in behaviour may explain the difference in survival between the populations, but other mechanisms (i.e. differences in swimming speed) may also be involved. There appears to be considerable differentiation in antipredator responses between these two R. arvalis populations, as well as with respect to different predators.     

Temporal variation in nest predation risk along habitat edges between grassland and secondary forest in Central Europe

Habitat fragmentation alters many ecological processes, including trophic cascades. For example, increased predation pressure along habitat edges has often been observed in fragmented landscapes. Here, we studied how nest predation risk varies along the transition zone between grassland and mixed forest in Central Europe. Using artificial nests, we tested the two mechanisms that are expected to underlie higher predation rates along edges: (1) the matrix effect model that supposes predator penetration from a habitat type with higher predator density to one with lower predator density and (2) the ecotonal effect model that assumes specific predator preferences for habitat edges. Although our results do not fully support either of these scenarios, our data show high temporal instability in nest predation along forest–grassland edges. Predation was higher in habitat interiors compared to edges during the first year, whereas the opposite pattern was observed during the subsequent year. In addition, dramatic between-year differences in the species composition of nest predators were observed. Therefore, we hypothesise that the effect of edges on nest predation is difficult to predict in landscapes with high predator diversity. In addition, our data indicate that a high abundance of wild boar considerably increases the risk of predation for ground-nesting birds.     

Prey responses to fine‐scale variation in predation risk from combined predators

While it is well documented that organisms can express phenotypic plasticity in response to single gradients of environmental variation, our understanding of how organisms integrate information along multiple environmental gradients is limited in many systems. Using the freshwater snail Helisoma trivolvis and two common predators (water bugs Belostoma flumineum and crayfish Orconectes rusticus), we explored how prey integrate information along multiple predation risk gradients (i.e. caged predators fed increasing amounts of prey biomass) that induce opposing phenotypes. When exposed to single predators fed increasing amounts of prey biomass, we detected threshold responses; intermediate amounts of consumed biomass induced phenotypic responses, but higher amounts induced little additional induction. This suggests that additional increases in predator‐induced traits with greater predator risk offer minimal increases in fitness or that a limit in the response magnitude was reached. Additionally, the response thresholds were contingent on the predator and focal trait. For shell width, responses were generally detected at a lower amount of consumed biomass by water bugs compared to crayfish. Within the crayfish treatments, we found that the shell thickness response threshold was lower than the shell width response threshold. When we combined gradients of consumed biomass from both predators, we found that the magnitude of response to one predator was often reduced when the other predator was present. Interestingly, these effects were often detected at consumed biomass levels that were lower than the threshold concentration necessary to elicit a response in the single‐predator treatments. Moreover, our combined predator treatments revealed that snails shifted from discrete responses to more continuous (i.e. graded) responses. Together, our results reveal that organisms experiencing multiple environmental gradients can integrate this information to make phenotypic decisions and demonstrate the novel result that an exposure to multiple species of predators can lower the response threshold of prey.     

Effects of behavioral and morphological plasticity on risk of predation in a Neotropical tadpole

Predator-induced phenotypic plasticity is widespread among aquatic animals, however the relative contributions of behavioral and morphological shifts to reducing risk of predation remain uncertain. We tested the phenotypic plasticity of a Neotropical tadpole (Rana palmipes) in response to chemical cues from predatory Belostoma water bugs, and how phenotype affects risk of predation. Behavior, morphology, and pigmentation all were plastic, resulting in a predator-induced phenotype with lower activity, deeper tail fin and muscle, and darker pigmentation. Tadpoles in the predator cue treatment also grew more rapidly, possibly as a result of the nutrient subsidy from feeding the caged predator. For comparison to phenotypes induced in the experiment, we quantified the phenotype of tadpoles from a natural pool. Wild-caught tadpoles did not match either experimentally induced phenotype; their morphology was more similar to that produced in the control treatment, but their low swimming activity was similar to that induced by predator cues. Exposure of tadpoles from both experimental treatments and the natural pool to a free-ranging predator confirmed that predator-induced phenotypic plasticity reduces risk of predation. Risk of predation was comparable among wild-caught and predator-induced tadpoles, indicating that behavioral shifts can substantially alleviate risk in tadpoles that lack the typical suite of predator-induced morphological traits. The morphology observed in wild-caught tadpoles is associated with rapid growth and high competition in other tadpole species, suggesting that tadpoles may profitably combine a morphology suited to competition for food with behaviors that minimize risk of predation.     

Motility of zooplankton: fitness, foraging and predation

The relative fitness of planktonic organisms foraging underthe risk of predation is examined in terms of their swimmingspeed, path geometry and jump frequency. Fitness is quantifiedin terms of encounter and ingestion of prey, respiration andenergy cost associated with swimming and mortality due to encounterswith predators. It is shown that a convoluted swimming pathin the form of meanders, zigzags or spirals confers greaterfitness than swimming along a straight path. Optimal path configurationis such that the length-scale of the path-meanders is commensuratewith an organism's detection radius to prey, which in turn scaleswith the size of the organism. Optimal swimming speed for acruise-feeding organism decreases with increasing prey concentrationand increasing risk due to ambush predators. For ambush feedingon motile prey, a benefit is gained by periodically moving toa new location. The time spent swimming is largely a functionof energetic costs, whereas the time spent feeding is stronglycontrolled by prey concentration and the risk posed, in turn,by ambush predators. These predictions are supported by observationsdrawn from the literature.     

Interspecific variation in the escape responses of aphids: effect on risk of predation from foliar-foraging and ground-foraging predators

A series of laboratory experiments was conducted to determine the effect of interspecific differences on prey defensive behavior on the susceptibility of two aphid species (Acyrthosiphon pisum and A. kondoi) to a ground-foraging predator, Harpalus pennsylvanicus, and a foliar-foraging predator, Coccinella septempunctata. These organisms are representative of a biologically and economically important predator/prey system in alfalfa. The primary defensive behavior of both aphid species toward C. septempunctata was to “drop” from the plant. Both aphid species were significantly more likely to drop from the plant in the presence of C. septempunctata. However, when C. septempunctata was present, a significantly lower proportion of A. kondoi individuals dropped (0.42 ± 0.07) compared to A. pisum (0.73 ± 0.08). As a result of their lower propensity to drop from the plant A. kondoi individuals are significantly more likely to be consumed by C. septempunctata. Conversely, the higher propensity of A. pisum individuals to drop increased their susceptibility to ground-foraging predators. When A. pisum was the prey species, ground-foraging predators made a significant contribution to overall aphid suppression and there was a significant synergistic interaction between ground and foliar-foraging predators. When A. kondoi was the prey there was no interaction between the predator species. As either a cause or consequence of its higher propensity to drop, A. pisum seems to be more adapted for survival and dispersal off the plant. In comparison to A. kondoi individuals, A. pisum individuals relocate plants more quickly (63 ± 41 s vs. 164 ± 39 s), disperse farther (18 ± 1.7 cm vs. 13 ± 0.66 cm), and survive longer (37 ± 2.0 h vs. 25 ± 2.0) off the plant. This study demonstrates the importance of prey defensive behavior in determining the susceptibility of a prey species to a multiple-predator complex. Received: 24 February 1997 / Accepted:17 December 1997     

Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore

In the marine littoral, strong grazing pressure selects for macroalgal defenses such as the constitutive and inductive production of defense metabolites. Induced defenses are expected under spatiotemporally varying grazing pressure and should be triggered by a reliable cue from herbivory, thereby reducing grazing pressure via decreased herbivore preference and/or performance. Although induced resistance has frequently been demonstrated in brown macroalgae, it is yet to be investigated whether induced macroalgal resistance shows genetic variation, a prerequisite for evolutionary responses to selection. In addition, consequences of induced resistance on herbivore performance have rarely been tested while the role of brown algal phlorotannins as inducible defense metabolites remains ambiguous. Using preference bioassays, we tested various cues, e.g., natural grazing, waterborne cues or simulated grazing to induce resistance in the brown alga Fucus vesiculosus. Further, we investigated whether there are induced responses in phlorotannin content, genetic variation in induced resistance or incurred performance costs to the mesoherbivore isopod, Idotea baltica. We found that both direct grazing and waterborne grazing cues decreased the palatability of F. vesiculosus, while increasing the total phlorotannin content. Since the sole presence of the herbivore also increased the total soluble phlorotannins, yet failed to stimulate deterrence, we concluded that phlorotannins alone do not explain increased resistance. Induced resistance varied between algal genotypes and thus showed potential for evolutionary responses to variation in grazing pressure. Induced resistance also incurred performance costs for female I. baltica via reduced egg production. Our results show that the induced resistance of F. vesiculosus decreases grazing pressure by deterring herbivores as well as impairing their performance. Resistance may be induced in advance by waterborne cues and spread effectively throughout the F. vesiculosus belt. Through lowering herbivore performance, induced resistance may also reduce future grazing pressure by decreasing the population growth rate of I. baltica.     

Understanding predation risk and individual variation in risk avoidance for threatened boreal caribou

Predation risk is a driver of species’ distributions. Animals can increase risk avoidance in response to fluctuations in predation risk, but questions remain regarding individual variability and the capacity to respond to changes in spatial risk across human‐altered landscapes. In northeast British Columbia, Canada, boreal caribou populations declined as roads and seismic lines have increased, which are theorized to increase gray wolf predation. Our goal was to model risk and to evaluate individual variability and the development of risk perception by examining individual risk avoidance in response to reproductive status and age. We used locations from collared caribou and wolves to identify landscape features associated with the risk of a potential wolf‐caribou encounter and risk of being killed given an encounter. We built resource selection functions to estimate individual responses to risk. We used general linear regressions to evaluate individual risk and linear feature avoidance as a function of age and reproductive status (calf or no calf). Linear features increased the risk of encounter. Older caribou and caribou with calves demonstrated stronger avoidance of the risk of encounter and roads, but weaker avoidance in late summer to the risk of being killed relative to younger and calf‐less individuals. Mechanisms explaining the inverse relationships between the risk of encounter and risk of being killed are uncertain, but it is conceivable that caribou learn to avoid the risk of encounter and roads. Responses by females with vulnerable calves to the risk of encounter and risk of being killed might be explained by a trade‐off between these two risk types and a prioritization on the risk of encounter. Despite the capacity to alter their responses to risk, the global decline in Rangifer populations (caribou and wild reindeer) suggests these behaviors are insufficient to mitigate the impacts of anthropogenic disturbances.     

Age-dependent inbreeding risk and offspring fitness costs in female black grouse

Dispersal is an important mechanism used to avoid inbreeding. However, dispersal may only be effective for part of an individual's lifespan since, post-dispersal individuals that breed over multiple reproductive events may risk mating with kin of the philopatric sex as they age. We tested this hypothesis in black grouse Tetrao tetrix, and show that yearling females never mated with close relatives whereas older females did. However, matings were not with direct kin suggesting that short-distance dispersal to sites containing kin and subsequent overlap of reproductive lifespans between males and females were causing this pattern. Chick mass was lower when kinship was high, suggesting important fitness costs associated with inbred matings. This study shows that increased inbreeding risk might be a widespread yet rarely considered cost of ageing.