The non-consumptive effects of predators and personality on prey growth and mortality

Individual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade-offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade-offs mediated by personality.     

Feedback between size balance and consumption strongly affects the consequences of hatching phenology in size‐dependent predator–prey interactions

In many size‐dependent predator–prey systems, hatching phenology strongly affects predator–prey interaction outcomes. Early‐hatched predators can easily consume prey when they first interact because they encounter smaller prey. However, this process by itself may be insufficient to explain all predator–prey interaction outcomes over the whole interaction period because the predator–prey size balance changes dynamically throughout their ontogeny. We hypothesized that hatching phenology influences predator–prey interactions via a feedback mechanism between the predator–prey size balance and prey consumption by predators. We experimentally tested this hypothesis in an amphibian predator–prey model system. Frog tadpoles Rana pirica were exposed to a predatory salamander larva Hynobius retardatus that had hatched 5, 12, 19 or 26 days after the frog tadpoles hatched. We investigated how the salamander hatch timing affected the dynamics of prey mortality, size changes of both predator and prey, and their subsequent life history (larval period and size at metamorphosis). The predator–prey size balance favoured earlier hatched salamanders, which just after hatching could successfully consume more frog tadpoles than later hatched salamanders. The early‐hatched salamanders grew rapidly and their accelerated growth enabled them to maintain the predator‐superior size balance; thus, they continued to exert strong predation pressure on the frog tadpoles in the subsequent period. Furthermore, frog tadpoles exposed to the early‐hatched salamanders were larger at metamorphosis and had a longer larval period than other frog tadpoles. These results suggest that feedback between the predator‐superior size balance and prey consumption is a critical mechanism that strongly affects the impacts of early hatching of predators in the short‐term population dynamics and life history of the prey. Because consumption of large nutrient‐rich prey items supports the growth of predators, a similar feedback mechanism may be common and have strong impacts on phenological shifts in size‐dependent trophic relationships.     

Prey subsidy or predator cue? Direct and indirect effects of caged predators on aquatic consumers and resources

The non-consumptive effects of predators on prey can affect prey phenotypes, potentially having important consequences for communities due to trait-mediated indirect interactions. Predicting non-consumptive effects and their impacts on communities can be difficult because predators can affect resources directly through nutrient cycling and indirectly by altering prey resource use, which can lead to complex interactions among resources and consumers. In this study we examined the effects of caged dragonfly predators on aquatic resources in the presence and absence of two focal herbivores, the tadpoles of Neotropical tree frogs Agalychnis callidryas and Dendropsophus ebraccatus. We crossed the presence/absence of caged dragonflies with four tadpole treatments: no tadpoles, each tadpole species alone, and both species together to examine interactions among tadpole composition, predator presence, and time on tadpole growth, resources, and zooplankton abundances. Predator effects on growth changed through ontogeny and was species-dependent. Predators initially reduced then dramatically increased A. callidryas growth, but had no effect on D. ebraccatus. Predators also increased the abundances of both periphyton and phytoplankton. However, there was no evidence of a trait-mediated trophic cascade (i.e., tadpole by predator interaction). Instead, nutrients from prey carcass subsidies likely played an increasingly important role in facilitating resources, and shaping tadpole growth, competitive interactions, and zooplankton abundances through time. In nutrient-poor aquatic systems the release of nutrients via the consumption of terrestrially derived prey items by aquatic predators may have important impacts on food webs by facilitating resources independent of the role of trait-mediated trophic cascades.     

Keystone predators (eastern newts, Notophthalmus viridescens) reduce the impacts of an aquatic invasive species

Predation, competition, and their interaction are known to be important factors that influence the structure of ecological communities. In particular, in those cases where a competitive hierarchy exists among prey species, the presence of certain keystone predators can result in enhanced diversity in the prey community. However, little is known regarding the influence of keystone predator presence on invaded prey communities. Given the widespread occurrence of invasive species and substantial concern regarding their ecological impacts, studies on this topic are needed. In this study I used naturalistic replications of an experimental tadpole assemblage to assess the influence of predatory eastern newts, Notophthalmus viridescens, on the outcome of interspecific competition among native and nonindigenous tadpoles. When newts were absent, the presence of the tadpoles of one invasive species, the Cuban treefrog, Osteopilus septentrionalis, resulted in decreased survival and growth rate of the dominant native species, Bufo terrestris, and dominance of the tadpole assemblage by O. septentrionalis. However, the presence of one adult newt generally reduced or eliminated the negative impacts of O. septentrionalis tadpoles, resulting in comparable survival and performance of native species in invaded and noninvaded treatments. Differential mortality among the tadpole species suggests that newts preyed selectively on O. septentrionalis tadpoles, supporting the hypothesis that newts acted as keystone predators in the invaded assemblage. The presence of nonindigenous larval cane toads, Bufo marinus, did not significantly affect native species, and this species was not negatively affected by the presence of newts. Collectively, these results suggest that eastern newts significantly modified the competitive hierarchy of the invaded tadpole assemblage and reduced the impacts of a competitively superior invasive species. If general, these results suggest that the presence of certain species may be an essential factor regulating the ecological impacts of biological invasions.     

Chemical cues from multiple predator-prey interactions induce changes in behavior and growth of anuran larvae

Chemical signals are used as information by prey to assess predation risk in their environment. To evaluate the effects of multiple predators on prey growth, mediated by a change in prey activity, I exposed small and large bullfrog (Rana catesbeiana) larvae (tadpoles) to chemical cues from different combinations of bluegill sunfish (Lepomis macrochirus) and larval dragonfly (Anax junius) predators. Water was regularly transferred from predation trials (outdoor experiment) to aquaria (indoor experiment) in which activity and growth of tadpoles was measured. The highest predation mortality of small bullfrog larvae in the outdoor experiment was due to Anax, and it was slightly lower in the presence of both predators, probably resulting from interactions between predators. There was almost no mortality of prey with bluegill. The activity and growth of small bullfrog larvae was highest in the absence of predators and lowest in the presence of Anax. In the presence of bluegill only, or with both predators, the activity and growth of small bullfrog tadpoles was intermediate. Predators did not affect large tadpole activity and growth. Regressing mortality of small bullfrog tadpoles against activity and growth of bullfrog tadpoles revealed a significant effect for small bullfrog larvae but a non-significant effect for large bullfrog larvae. This shows that the response of bullfrog tadpoles to predators is related to their own body size. The experiment demonstrates that chemical cues are released both as predator odor and as alarm substances and both have the potential to strongly alter the activity and growth of prey. Different mechanisms by which chemical cues may be transmitted to species interactions in the food web are discussed. Received: 28 June 1999 / Accepted: 15 November 1999     

Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae

This study examined the effects of multiple predators on size‐specific behavior and mortality of two species of anuran larvae. Particularly, we focused on how trait changes in predators and prey may be transmitted to other species in the food web. In laboratory experiments, we examined the effects of bluegill sunfish, Lepomis macrochirus, and the odonate larva Anax junius on behavior and mortality of tadpoles of the bullfrog, Rana catesbeiana, and the green frog R. clamitans. Experiments were conducted with predators alone and together to assess effects on behavior and mortality of the tadpoles. The experiments were replicated on five size classes of the tadpoles to evaluate how responses varied with body size.
Predation rates by Anax were higher on bullfrogs than on green frogs, and both bullfrogs and green frogs suffered greater mortality from Anax than from bluegill. Bluegill only consumed green frogs. Predation rates by both predators decreased with increasing tadpole size and decreased in the non‐lethal (caged) presence of the other predator. Both anuran larvae decreased activity when exposed to predators. Bullfrogs, however, decreased activity more in the presence of Anax than in the presence of bluegill, whereas green frogs decreased activity similarly in the presence of both predators. The largest size class of green frogs, but not of bullfrogs, exhibited spatial avoidance of bluegill. These responses were directly related to the risk posed by the different predators to each anuran species. Anax activity (speed and move frequency) also was higher when alone than in the non‐lethal presence of bluegill. We observed decreased predation rate of each predator in the non‐lethal presence of the other, apparently caused by two different mechanisms. Bluegill decreased Anax mortality on tadpoles by restricting the Anax activity. In contrast, Anax decreased bluegill mortality on tadpoles by reducing tadpole activity. We discuss how the activity and spatial responses of the tadpoles interact with palatability and body size to create different mortality patterns in the prey species and the implications of these results to direct and indirect interactions in this system.     

Predator density and competition modify the benefits of group formation in a shoaling reef fish

Synthesis Predation risk experienced by individuals living in groups depends on the balance between predator dilution, competition for refuges, and predator interference or synergy. These interactions operate between prey species as well: the benefits of group living decline in the presence of an alternative prey species. We apply a novel model‐fitting approach to data from field experiments to distinguish among competing hypotheses about shifts in predator foraging behavior across a range of predator and prey densities. Our study provides novel analytical tools for analyzing predator foraging behavior and offers insight into the processes driving the dynamics of coral reef fish. Studies of predator foraging behavior typically focus on single prey species and fixed predator densities, ignoring the potential importance of complexities such as predator dilution; predator‐mediated effects of alternative prey; heterospecific competition; or predator–predator interactions. Neglecting the effects of prey density is particularly problematic for prey species that live in mixed species groups, where the beneficial effects of predator dilution may swamp the negative effects of heterospecific competition. Here we use field experiments to investigate how the mortality rates of a shoaling coral reef fish (a wrasse: Thalassoma amblycephalum), change as a result of variation in: 1) conspecific density, 2) density of a predator (a hawkfish: Paracirrhites arcatus), and 3) presence of an alternative prey species that competes for space (a damselfish: Pomacentrus pavo). We quantify changes in prey mortality rates from the predator's perspective, examining the effects of added predators or a second prey species on the predator's functional response. Our analysis highlights a model‐fitting approach that discriminates amongst multiple hypotheses about predator foraging in a community context. Wrasse mortality decreased with increasing conspecific density (i.e. mortality was inversely density‐dependent). The addition of a second predator doubled prey mortality rates, without significantly changing attack rate or handling time – i.e. there was no evidence for predator interference. The presence of a second prey species increased wrasse mortality by 95%; we attribute this increase either to short‐term apparent competition (predator aggregation) or to a decrease in handling time of the predator (e.g. through decreased wrasse vigilance). In this system, 1) prey benefit from intraspecific group living though a reduced predation risk, and 2) the benefit of group living is reduced in the presence of an alternative prey species.     

Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type

Many species alter their activity, microhabitat use, morphology and life history in response to predators. Predation risk is related to predator size and palatability of prey among others factors. We analyzed the predation risk of three species of tadpoles that occur in norwestern Patagonia, Argentina: Pleurodema thaul, Pleurodema bufoninum and Rhinella spinulosa. We sampled aquatic insect predators in 18 ponds to determine predator–tadpole assemblage in the study area. In laboratory conditions, we analysed the predation rate imposed by each predator on each tadpole species at different tadpole sizes. Finally, we tested whether tadpoles alter their activity in the presence of chemical and visual cues from predators. Small P. thaul and P. bufoninum tadpoles were the most vulnerable prey species, while small R. spinulosa tadpoles were only consumed by water bugs. Dragonflies and water bugs were the most dangerous tadpole predators. Small P. thaul tadpoles reduced their activity when they were exposed to all predators, while large tadpoles only reduced the activity in the presence of large predators (dragonfly larvae and water bugs). Small P. bufoninum tadpoles reduced the activity when they were exposed to beetle larvae and dragonfly larvae, while large tadpoles only reduced activity when they were exposed to larger predators (water bugs and dragonfly larvae). R. spinulosa tadpoles were the less sensitive to presence of predators, only larger tadpoles responded significantly to dragonfly larvae by reducing their activity. We conclude that behavioural responses of these anuran species were predator-specific and related to the risk imposed by each predator.     

An offensive predator phenotype selects for an amplified defensive phenotype in its prey

Inducible defenses of prey and inducible offenses of predators are examples of adaptive phenotypic plasticity. Although evolutionary ecologists have paid considerable attention to the adaptive significances of these strategies, they have rarely focused on their evolutionary impacts on the interacting species. Because the functional phenotypes of predator and prey determine strength of interactions between the species, the inducible plasticity can modify selective pressure on trait distribution and, ultimately, trait evolution in the interacting species. We experimentally tested this hypothesis in a predator–prey system composed of salamander larvae (Hynobius retardatus) and frog tadpoles (Rana pirica) capable of expressing antagonistic inducible offensive or defensive traits, an enlarged gape in the salamander larvae and a bulgy body in the tadpoles, when predator–prey interactions are strong. We examined selection strength on the tadpole’s defensive trait by comparing survival rates of tadpoles with different defensive levels under predation pressure from offensive or non-offensive salamander larvae. Survival rates of more-defensive tadpoles were greater than those of less-defensive tadpoles only when the tadpoles were exposed to offensive salamander larvae; thus, the predator’s offensive phenotype could select for an amplified defensive phenotype in their prey. As the expression of inducible offenses by H. retardatus larvae depends greatly on the composition of its ecological community, the inducible defensive bulgy morph of R. pirica tadpoles might have evolved in response to the variable expression of the H. retardatus offensive larval phenotype.     

Trait-mediated interactions: influence of prey size, density and experience

1. The role of non-consumptive predator effects in structuring ecological communities has become an important area of study for ecologists. Numerous studies have shown that adaptive changes in prey in response to a predator can improve survival in subsequent encounters with that predator. 2. Prey-mediated changes in the shapes of predators' functional response surfaces determine the qualitative predictions of theoretical models. However, few studies have quantified the effects of adaptive prey responses on the shape of predator functional responses. 3. This study explores how prey density, size and previous predator experience interact to change the functional response curves of different-sized predators. 4. We use a response surface design to determine how previous exposure to small or large odonate predators affected the short-term survival of squirrel tree frog (Hyla squirella) tadpoles across a range of sizes and densities (i.e. the shape of odonate functional response curves). 5. Predator-induced tadpoles in a given size class did not differ in shape, although induction changed tadpole behaviour significantly. Induced tadpoles survived better in lethal encounters with either predator than did similar-sized predator-naive tadpoles. 6. Induction by either predator resulted in increased survival with both predators at a given size. However, different mechanisms led to increased survival for induced tadpoles. Attack rate for the small predators, whereas handling time increased for the large predators.     

Inter‐specific differences in invader and native fish functional responses illustrate neutral effects on prey but superior invader competitive ability

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Vulnerability of an Australian anuran tadpole assemblage to the toxic eggs of the invasive cane toad (Bufo marinus)

The invasion of cane toads (Bufo marinus) across tropical Australia has fatally poisoned many native predators; the most frequent victims may be tadpoles of native frogs, which die when they consume the toxic eggs of the toads. Field studies have documented high and species‐specific mortality of tadpoles following toad spawning. To clarify the determinants of tadpole vulnerability, we conducted 1593 laboratory trials in which single tadpoles were exposed to 10 toad eggs, either with or without an alternative food source (lettuce). At least some tadpoles within all 15 species tested consumed toad eggs. Interspecific variance in survival rates (from 0 to >70%) was driven by feeding responses not by physiological tolerance to toxins: almost all native tadpoles that consumed eggs died rapidly. Tadpole mortality was decreased by the presence of an alternative food source in four species, increased in two species, and not affected in seven species. In three of four taxa where we tested both small (early‐stage) and large (late‐stage) tadpoles, both mean survival rates and the effects of alternative food on survival shifted with tadpole body size. Trials with one species (Limnodynastes convexiusculus) showed no significant inter‐clutch variation in feeding responses or tolerance to toxins. Overall, our data show that cane toad eggs are highly toxic to native anuran tadpoles, but that whether or not a tadpole is killed by encountering toad eggs depends upon a complex interaction between the native anuran's species, its body size, and whether or not alternative food was present. In nature, larval vulnerability also depends upon the seasonal timing and location of spawning events, and habitat selection and foraging patterns of the tadpoles. Our results highlight the complexity of vulnerability determinants, and identify ecological factors (rather than physiology or feeding behaviour) as the primary determinants of cane toad impact on native tadpoles.     

Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems

Many organisms undergo ontogenetic niche shifts due to considerable changes in size during their development. These ontogenetic shifts can alter the trophic position of individuals, the type and strength of ecological interactions across species, and allow for cannibalism within species. In this study we ask if and how the interaction of a size refuge and cannibalism in the prey alters the dynamics of intraguild predation (IGP) systems. By manipulating the composition of large cannibalistic (Aeshna umbrosa) and predatory (Anax junius) dragonfly larvae in mesocosms we show that the interaction of cannibals and predators was non-linear and increased the survival of prey. The structure of the final resource community shared by prey and predator differed between small and large dragonfly treatments but not within size classes across species. In general, the small prey stage showed similar shifts in microhabitat use and refuge use when exposed to either conspecific cannibals or predators, while large cannibals showed no clear anti-predator response. However, further behavioral experiments revealed that specific behavioral components, such as distances between individuals or number of movements, differed when individuals were exposed to either cannibals or predators. This indicates that individuals discriminated between conspecific or heterospecific predators. Furthermore, in similar experiments large cannibals and predators showed different behaviors when exposed to conspecifics rather than to each other. These changes in behavior are consistent with the observed increase in prey survival. In general, the results indicate that cannibalism and ontogenetic niche shifts can result in behavior-mediated indirect interactions that reduce the impact of the predator on the mortality of its prey and alter the interactions of IGP systems. However, they also indicate that size is not the sole determinant and that we also need to account for the species identity when predicting the dynamics of communities.     

Effects of cover and predator size on survival and development of Ranautricularia tadpoles

Size-limited predation is an important process during the development of many aquatic species, and mortality rates of early larval stages and small individuals can be particularly high. Structurally complex habitats can mediate predator-prey interactions and provide a potentially important mechanism for decreasing predation pressure on larvae. To determine whether structurally complex habitats mediate predation on tadpoles of the southern leopard frog (Ranautricularia), we designed a factorial experiment, crossing two levels of cover with three predator treatments (none, small, or large Trameacarolina naiads). Predator size had a larger effect on tadpole performance (survival, mass and age at metamorphosis) than did cover level, largely because small predators were ineffective. Within the large-predator treatment, however, tadpole survival was higher (78%) under high than under low cover (46%), suggesting that increased cover decreased predator foraging efficiency allowing more larvae to reach a size refuge. This study demonstrates that habitat structural complexity can play an important role in mediating predator-prey interactions, even when tadpoles start out at a size disadvantage relative to predators. Consideration of habitat structural complexity in future research should provide a more complete understanding of the role of size relationships in predator-prey systems. Received: 3 January 1997 / Accepted: 10 October 1997     

Further notes on the natural history of the South American pepper frog, Leptodactylus labyrinthicus (Spix, 1824) (Anura, Leptodactylidae)

Leptodactylus labyrinthicus tadpoles reach a large size in the nest through consumption of trophic eggs. We previously suggested that the trophic eggs are laid just after amplexus has finished, but our new data do not support this hypothesis. We also present further details on the natural history of the species with regard to breeding activity, spawning site, retreats and the ability of tadpoles in preying upon fully-growth heterospecific tadpoles. We also show that the tadpoles are mainly nocturnal and take diurnal refuges. We collected the data in Brazil in three localities within the Cerrado Biome. We examined burrows used by L. labyrinthicus males, verified if females still contained mature eggs just after released from amplexus, and tested the ability of tadpoles in preying fully-growth heterospecific tadpoles. Field observations and experiments were conducted on tadpole activity time, hiding behaviour and level of susceptibility to predation by the bird leaf-scrapers in four sheltering situations. Reproduction could start before the first rains; this may be advantageous by allowing the tadpoles to exploit eggs of other frogs. We found one floating nest built in a temporary pool. The nest of the species is normally circumscribed in an excavated basin beside the water body. Adult males were found during the day with their head-out of the entrance of underwater burrows, which were perforations through dense root mats beside calling/spawning sites. Probably, these burrows in permanently water-filled soil are actively excavated by males. Females released all their eggs during the amplexus, so trophic eggs are not produced by the currently-accepted mechanism. Fully-grown heterospecific tadpoles were not preyed upon by L. labyrinthicus tadpoles, which can prey only slow-moving newly hatched ones. Field tadpoles took shelter under mud/dead leaves during daylight and became exposed on the bottom at night. Free-ranging leaf-scrapers removed dead leaves from a pool with their beaks and preyed upon tadpoles. In the experiments, the tadpoles sheltered under gravel/leaves during daylight, but they were exposed at night. Leaf-scrapers ate all exposed tadpoles, but no tadpole of the gravel/leaves trays was consumed. Hence the nocturnal habits and use of diurnal refuges may protect the tadpoles from visual predators, such as the leaf-scrapers.     

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.     

Predator–prey interactions and metabolic rates are altered in stable and unstable groups in a social fish

Understanding the determinants and consequences of predation effort, success and prey responses is important since these factors affect the fitness of predators and prey. When predators are also invasive species, the impacts on prey can be particularly far-reaching with ultimate ecosystem-level consequences. However, predators are typically viewed as behaviourally fixed within this interaction and it is unclear how variation in predator social dynamics affects predator–prey interactions. Using the invasive eastern mosquitofish Gambusia holbrooki and a native glass shrimp Paratya australiensis in Australia, we investigated how varying levels of social conflict within predator groups influences predator–prey interactions. By experimentally manipulating group stability of G. holbrooki, we show that rates of social conflict were lower in groups with large size differences, but that routine metabolic rates were higher in groups with large size differences. Predation effort and success did not vary depending on group stability, but in stable groups predation effort by aggressive dominants was greater than subordinates. The anti-predator responses of prey to the stability of predator groups were mixed. While more prey utilized shelters when exposed to stable compared to unstable groups of predators, a greater proportion were sedentary when predator groups were unstable. Overall, this study demonstrates predator group stability is modulated by differences in body size and can influence prey responses. Further, it reveals a hidden metabolic cost of living in stable groups despite reduced overt social conflict. For invasive species management, it is therefore important to consider the behavioural and physiological plasticity of the invasive predators, whose complex social interactions and metabolic demands can modulate patterns of predator–prey interactions.     

Strong behavioural defensive responses of endemic Rana latastei tadpoles induced by a native predator's odour

Prey species must constantly acquire information on predator identity, abundance and dangerousness from the environment. In aquatic habitats, this information is mainly propagated by water-borne chemical signals, either predator-specific odours or prey alarm cues. Anuran larvae innately respond to conspecific alarm cues and are able to associate them to predator cues during their lifetime. In this study, we investigated the anti-predatory responses of endemic Italian agile frog (Rana latastei) tadpoles exposed to either conspecific or heterospecific alarm cues and a native predator's (Anax imperator larvae) odour. Pre-and post-stimulus behaviours of each tadpole were recorded by a digital camera and analysed by a source executable software for image-based tracking. We found that Italian agile frog tadpoles responded to fasted dragonfly odour by strongly reducing their activity, both in terms of the amount of time they spent active and path length covered in comparison to control groups. Contrary to previous studies, predators' diet had a negligible effect on tadpole response and our experiment did not bring any evidence of the phylogenetic-relatedness hypothesis. The innate or early-in-development recognition of dragonfly larvae is clearly adaptive and may increase tadpole survival with relatively low costs, but, at the same time, may increase the risk of ignoring novel potential threats.     

Interactions between the information content of different chemical cues affect induced defences in tadpoles

Animals often alter their behaviour, morphology and physiology in the presence of predators. These induced defences can be fine‐tuned by a variety of environmental factors such as predator species, acute predation risk or food availability. It has, however, remained unclear what cues influence the extent and quality of induced defences and how the information content of these cues interact to determine the development of antipredator defences. We performed an experiment to study the significance of direct chemical cues, originating from the predators themselves, and indirect cues, released by attacked or consumed prey, for phenotypic responses in Rana dalmatina tadpoles. We reared tadpoles in the presence of caged predators (Triturus vulgaris, Aeshna cyanea) fed either one or three tadpoles every other day outside the tadpole‐rearing tanks. Fifteen hours after food provisioning, predators were put back into the tanks containing focal tadpoles either after washing (direct + digestion‐released cues) or with the water containing remnants of the prey (direct + all types of indirect cues). Our results suggest that direct cues together with digestion‐released cues can be sufficient to induce strong antipredator responses. Induced defences depended on both direct cues, affecting predator‐specific responses, and the quantity of indirect cues, resulting in graded responses to differences in predation threat. Moreover, direct and indirect cues interacted in behaviour, resulting in predator‐specific graded responses. We also observed a decrease in the extent of predator‐induced responses in large tadpoles as compared to small ones. Our results, thus, suggest that prey integrate multiple cues about predators to optimize induced defences and that this process changes during ontogeny.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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