Predation Sequence Research Articles

Defensive Behaviour in Intertidal Crabs

ABSTRACTDespite a long roster of prey defences against predators now documented by biologists, any given species utilises only some of them, and we have few a priori predictions as to if, when or where they will be employed. In order to uncover general trends in the way in which crabs avoid predation attempts after they have been detected, we examined the antipredator behaviour of nine intertidal decapod species on three continents. We studied five different types of defensive behaviour and seven morphological and environmental factors which might affect such behaviours at different stages of the predatory sequence. In combination with other studies, we suggest that although intertidal crabs invest a great deal in crypticity to avoid detection, once discovered, they remain immobile, raise their chelae or flee but the extent to which these and other defences are exhibited differ markedly across species. We found that luminance contrast with the background, body size, chelae size and immediate habitat in which crabs were found affected antipredator behaviour whereas neither sex, nor chromatic contrast with the background were important. Our findings broaden understanding of defensive behaviour in several decapod species and highlight how species tailor the use of the same defences in different ways according to threat, morphology and local environment.

Ethogram of the predatory sequence of dogs (Canis familiaris)

Predatory behaviour is a relevant part of the behavioural repertoire of dogs, which often entails negative or desirable implications, depending on the context and target to which it is directed. It is also considered one of the most characterising aspects of breed-specific behaviour. Despite its relevance, there is surprisingly little scientific knowledge about the topic. In the present study we sought to develop an ethogram of the predatory sequence of dogs, with the aim of providing a sufficiently general structure to be applicable to dogs at large, without eluding peculiar aspects of the species’ specific behaviour. Sixty videos of dogs of different breeds expressing predatory acts, including both videos obtained from public internet repositories and videos made on purpose, were described in detail by two different observers. From descriptions, a general sequence was identified, consisting of four functional phases, i.e. search, approach, chase and bite. The descriptions of the behaviours included in each phase were organised into three levels, characterised by different levels of detail and focusing on different aspects of the behaviour. When appropriate, these descriptions highlighted differences in behaviour expressed by dogs belonging to different working groups. The ethogram proposed in the present paper could represent a useful starting point for improving knowledge about the predatory behaviour of dogs and answering relevant questions about both its evolution and ontogeny.

Highly defended nudibranchs "escape" to visually distinct background habitats.

The "escape and radiate" hypothesis predicts that once species have evolved aposematism, defended species can utilize more visually diverse visual backgrounds as they "escape" the need to be well camouflaged. This enables species to explore new ecological niches, resulting in increased diversification rates. To test this hypothesis "escape" component, we examined whether the background habitats of 12 nudibranch mollusk species differed among species depending on the presence and strength of chemical defenses. We obtained a rich array of color pattern statistics using quantitative color pattern analysis to analyze backgrounds viewed through the eyes of a potential predator (triggerfish, Rhinecanthus aculeatus). Color pattern analysis was done at viewing distances simulating an escalating predation sequence. We identified 4 latent factors comprising 17 noncorrelated color pattern parameters, which captured the among-species variability associated with differences in chemical defenses. We found that chemically defended species, indeed, were found on visually distinct backgrounds with increased color and luminance contrast, independent of viewing distance. However, we found no evidence for increased among-species background diversity coinciding with the presence and strength of chemical defenses. Our results agree with the "escape and radiate" hypothesis, suggesting that potent chemical defenses in Dorid nudibranchs coincide with spatiochromatic differences of visual background habitats perceived by potential predators.

The environment to the rescue: can physics help predict predator-prey interactions?

Understanding the factors that determine the occurrence and strength of ecological interactions under specific abiotic and biotic conditions is fundamental since many aspects of ecological community stability and ecosystem functioning depend on patterns of interactions among species. Current approaches to mapping food webs are mostly based on traits, expert knowledge, experiments, and/or statistical inference. However, they do not offer clear mechanisms explaining how trophic interactions are affected by the interplay between organism characteristics and aspects of the physical environment, such as temperature, light intensity or viscosity. Hence, they cannot yet predict accurately how local food webs will respond to anthropogenic pressures, notably to climate change and species invasions. Herein, we propose a framework that synthesises recent developments in food-web theory, integrating body size and metabolism with the physical properties of ecosystems. We advocate for combination of the movement paradigm with a modular definition of the predation sequence, because movement is central to predator-prey interactions, and a generic, modular model is needed to describe all the possible variation in predator-prey interactions. Pending sufficient empirical and theoretical knowledge, our framework will help predict the food-web impacts of well-studied physical factors, such as temperature and oxygen availability, as well as less commonly considered variables such as wind, turbidity or electrical conductivity. An improved predictive capability will facilitate a better understanding of ecosystem responses to a changing world.

Outstanding issues in the study of antipredator defenses.

Protective defense mechanisms are well documented across the animal kingdom, but there are still examples of antipredator defenses that do not fit easily into the current conceptualization. They either fall within the intersection of multiple mechanisms or fail to fall neatly into pre-existing categories. Here, using Endler's predatory sequence as a framework, we identify problematic examples of antipredator defenses, separating them into protective mechanisms that are difficult to classify and those which act sequentially depending on context. We then discuss three ways of improving underlying terminological and definitional problems: (1) issues with English and polysemy, (2) overlapping aspects of similar mechanisms, and (3) unclear definitions. By scrutinizing the literature, we disentangle several opaque areas in the study of protective defense mechanisms and highlight questions that require further research. An unclear conceptual framework for protective defense mechanisms can lead to misconceptions in understanding the costs and benefits of defenses displayed by animals, while interchangeable terminologies and ambiguous definitions can hinder communication in antipredator studies.

Reactive response to predation risk affects foraging time of hares, yet not their phosphorus intake

Antipredator responses could affect nutrient intake, which could lead to nutritional deficits. However, little is known about the antipredator response of small herbivores because most are nocturnal or crepuscular and therefore very difficult to study in the field. Therefore, we experimentally assessed the effect of a reactive response to predation risk on the nutrient (i.e., phosphorous) intake of the European hare (Lepus europaeus) using three different playback sounds. Additionally, we studied the time spent being costly vigilant, the time spent foraging, and the vegetation height in which the hares were present using accelerometers and GPS. Our results showed that elevated predation risk from our playback experiment did not affect the (1) phosphorus intake, (2) time spent being costly vigilant, and (3) time spent in tall vegetation. However, elevated predation risk did increase the time spent foraging. Possibly hares spent more time foraging with an increased predation risk because hares cannot seek refuge from predators. Additionally, the effect on phosphorus intake could be weak because phosphorous intake does not benefit a flight escape, while the reactive response acts late in the predation sequence limiting the effect on hare ecology. Prey anti-predator responses seem strongly related to the escape tactics of prey species that can differ between different habitats and the time of the day. More detailed field studies are necessary to get a better insight into species’ anti-predator-food tactics.

Signal detectability and boldness are not the same: the function of defensive coloration in nudibranchs is distance-dependent.

Aposematic signals visually advertise underlying anti-predatory defences in many species. They should be detectable (e.g. contrasting against the background) and bold (e.g. using internal pattern contrast) to enhance predator recognition, learning and memorization. However, the signalling function of aposematic colour patterns may be distance-dependent: signals may be undetectable from a distance to reduce increased attacks from naïve predators but bold when viewed up close. Using quantitative colour pattern analysis, we quantified the chromatic and achromatic detectability and boldness of colour patterns in 13 nudibranch species with variable strength of chemical defences in terms of unpalatability and toxicity, approximating the visual perception of a triggerfish (Rhinecanthus aculeatus) across a predation sequence (detection to subjugation). When viewed from an ecologically relevant distance of 30 cm, there were no differences in detectability and boldness between well-defended and undefended species. However, when viewed at closer distances (less than 30 cm), well-defended species were more detectable and bolder than undefended species. As distance increased, detectability decreased more significantly than boldness for defended species. For undefended species, boldness and detectability remained comparatively consistent, regardless of viewing distance. We provide evidence for distance-dependent signalling in aposematic nudibranchs and highlight the importance of distinguishing signal detectability from boldness in studies of aposematism.

Why fake death? Environmental and genetic control of tonic immobility in larval lacewings (Neuroptera: Chrysopidae).

Tonic immobility is a passive antipredator strategy employed late in the predation sequence that may decrease individual mortality in prey animals. Here, we investigate how energetic state and genetic predisposition influence antipredator decision-making in green lacewing larvae, Chrysoperla plorabunda (Fitch), using simulated predatory encounters. We demonstrate that tonic immobility is a plastic response influenced by energetic resource limitation. Larvae exposed to 1 or 2 days of food deprivation initiate tonic immobility more often and with less physical provocation than individuals fed ad libitum. Recently molted individuals exposed to food deprivation, the individuals most energetically challenged, engage in tonic immobility at a higher rate than any other group. We also find that variation in antipredator strategy between individuals is partly the result of within-population genetic variation. We estimate the propensity to enter tonic immobility to have a broad-sense heritability of 0.502. Taken together our results suggest that larval lacewings under energetic stress are more likely to engage in tonic immobility. Yet, energetic state does not explain all within-population variation, as individuals can have a genetic predisposition for tonic immobility.

The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

Defence mitigation by predators of chemically defended prey integrated over the predation sequence and across biological levels with a focus on cardiotonic steroids.

Predator–prey interactions have long served as models for the investigation of adaptation and fitness in natural environments. Anti-predator defences such as mimicry and camouflage provide some of the best examples of evolution. Predators, in turn, have evolved sensory systems, cognitive abilities and physiological resistance to prey defences. In contrast to prey defences which have been reviewed extensively, the evolution of predator counter-strategies has received less attention. To gain a comprehensive view of how prey defences can influence the evolution of predator counter-strategies, it is essential to investigate how and when selection can operate. In this review we evaluate how predators overcome prey defences during (i) encounter, (ii) detection, (iii) identification, (iv) approach, (v) subjugation, and (vi) consumption. We focus on prey that are protected by cardiotonic steroids (CTS)—defensive compounds that are found in a wide range of taxa, and that have a specific physiological target. In this system, coevolution is well characterized between specialist insect herbivores and their host plants but evidence for coevolution between CTS-defended prey and their predators has received less attention. Using the predation sequence framework, we organize 574 studies reporting predators overcoming CTS defences, integrate these counter-strategies across biological levels of organization, and discuss the costs and benefits of attacking CTS-defended prey. We show that distinct lineages of predators have evolved dissecting behaviour, changes in perception of risk and of taste perception, and target-site insensitivity. We draw attention to biochemical, hormonal and microbiological strategies that have yet to be investigated as predator counter-adaptations to CTS defences. We show that the predation sequence framework will be useful for organizing future studies of chemically mediated systems and coevolution.

The Integral Nature of Encounter Rate in Predicting Livestock Depredation Risk

Carnivore depredation of livestock is one of the primary drivers of human-carnivore conflict globally, threatening the well-being of livestock owners, and fueling large carnivore population declines. Interventions designed to reduce carnivore depredation typically center around predictions of depredation risk. However, these spatial risk models tend to be informed by data depicting the number of livestock attacked by carnivores. Importantly, such models omit key stages in the predation sequence which are required to predict predation risk, or in this case depredation risk. Applying the classic predation risk model defined by Lima and Dill demonstrates that depredation risk is dependent upon quantifying the rates at which carnivores encounter livestock before attacking. However, encounter rate is challenging to estimate, necessitating novel data collection systems. We developed and applied such a system to quantify carnivore-livestock encounters at livestock corrals (i.e., bomas) across a 9-month period in Central Kenya. Concurrently, we monitored the number of livestock attacked by carnivores at these bomas. We calculated carnivore-livestock encounter rates, attack rates, and depredation risk at the boma. We detected 1,383 instances in which carnivores encountered livestock at the bomas. However, we only recorded seven attacks. We found that the encounter rate and attack rate for spotted hyenas were almost six and three times higher than that for any other species, respectively. Consequently, spotted hyenas posed the greatest depredation risk for livestock at the boma. We argue that better understanding of carnivore-livestock encounter rates is necessary for effective prediction and mitigation of carnivore depredation of livestock.

Beyond spatial overlap: harnessing new technologies to resolve the complexities of predator–prey interactions

Predation risk, the probability that a prey animal will be killed by a predator, is fundamental to theoretical and applied ecology. Predation risk varies with animal behavior and environmental conditions, yet attempts to understand predation risk in natural systems often ignore important ecological and environmental complexities, relying instead on proxies for actual risk such as predator–prey spatial overlap. Here we detail the ecological and environmental complexities driving disconnects between three stages of the predation sequence that are often assumed to be tightly linked: spatial overlap, encounters and prey capture. Our review highlights several major sources of variability in natural predator–prey systems that lead to the decoupling of spatial overlap estimates from actual encounter rates (e.g. temporal activity patterns, predator and prey movement capacity, resource limitations) and that affect the probability of prey capture given encounter (e.g. predator hunger levels, temporal, topographic and other environmental influences on capture success). Emerging technologies and statistical methods are facilitating a transition to a more spatiotemporally detailed, mechanistic understanding of predator–prey interactions, allowing for the concurrent examination of multiple stages of the predation sequence in mobile, free‐ranging animals. We describe crucial applications of this new understanding to fundamental and applied ecology, highlighting opportunities to better integrate ecological contingencies into dynamic predator–prey models and to harness a mechanistic understanding of predator–prey interactions to improve targeting and effectiveness of conservation interventions.

Social information use by predators: expanding the information ecology of prey defences

Social information use is well documented across the animal kingdom, but how it influences ecological and evolutionary processes is only just beginning to be investigated. Here we evaluate how social transmission may influence species interactions and potentially change or create novel selection pressures by focusing on predator–prey interactions, one of the best studied examples of species coevolution. There is extensive research into how prey can use social information to avoid predators, but little synthesis of how social transmission among predators can influence the outcome of different stages of predation. Here we review evidence that predators use social information during 1) encounter, 2) detection, 3) identification, 4) approach, 5) subjugation and 6) consumption. We use this predation sequence framework to evaluate the implications of social information use on current theoretical predictions about predator–prey dynamics, and find that social transmission has the potential to alter selection pressures for prey defences at each predation stage. This suggests that considering social interactions can help answer open questions about species coevolution, and also predict how populations and communities respond to rapid human‐induced changes in the environment.

Aposematism and mimicry in birds

We review the literature on warning coloration in birds starting from Alfred Russel Wallace's premise that aposematism may advertise difficulty in subduing prey rather than simply unpalatability. Across diverse taxa, there is a good deal of anecdotal information to suggest that signals, usually involving conspicuous coloration, are associated not only with distastefulness but with informing predators that prey will be difficult to catch. There are also examples of aposematism being associated with both Müllerian and Batesian mimicry. In Aves there are now several examples of competitive mimicry which involves resembling larger non‐predator species. We stress that broad‐sense aposematism dissuading predators from attack can operate throughout the predatory sequence in birds. Throughout, we suggest new avenues of research that are likely to be promising and which will reinvigorate rigorous research on warning coloration in birds.

Multimodal Aposematic Defenses Through the Predation Sequence

Aposematic organisms warn predators of their unprofitability using a combination of defenses, including visual warning signals, startling sounds, noxious odors, or aversive tastes. Using multiple lines of defense can help prey avoid predators by stimulating multiple senses and/or by acting at different stages of predation. We tested the efficacy of three lines of defense (color, smell, taste) during the predation sequence of aposematic wood tiger moths (Arctia plantaginis) using blue tit (Cyanistes caeruleus) predators. Moths with two hindwing phenotypes (genotypes: WW/Wy = white, yy = yellow) were manipulated to have defense fluid with aversive smell (methoxypyrazines), body tissues with aversive taste (pyrrolizidine alkaloids) or both. In early predation stages, moth color and smell had additive effects on bird approach latency and dropping the prey, with the strongest effect for moths of the white morph with defense fluids. Pyrrolizidine alkaloid sequestration was detrimental in early attack stages, suggesting a trade-off between pyrrolizidine alkaloid sequestration and investment in other defenses. In addition, pyrrolizidine alkaloid taste alone did not deter bird predators. Birds could only effectively discriminate toxic moths from non-toxic moths when neck fluids containing methoxypyrazines were present, at which point they abandoned attack at the consumption stage. As a result, moths of the white morph with an aversive methoxypyrazine smell and moths in the treatment with both chemical defenses had the greatest chance of survival. We suggest that methoxypyrazines act as context setting signals for warning colors and as attention alerting or “go-slow” signals for distasteful toxins, thereby mediating the relationship between warning signal and toxicity. Furthermore, we found that moths that were heterozygous for hindwing coloration had more effective defense fluids compared to other genotypes in terms of delaying approach and reducing the latency to drop the moth, suggesting a genetic link between coloration and defense that could help to explain the color polymorphism. Conclusively, these results indicate that color, smell, and taste constitute a multimodal warning signal that impedes predator attack and improves prey survival. This work highlights the importance of understanding the separate roles of color, smell and taste through the predation sequence and also within-species variation in chemical defenses.

Role of coloration in antipredator strategies of Pristidactylus achalensis (Squamata: Leiosauridae) related to sex and stages of predation

Abstract The interaction between behavioural and phenotypic traits, such as coloration, plays a specific role at different stages of the predatory sequence. Cryptic coloration involves a match to the background that reduces the risk of detection, and it is usually optimized by immobility behaviour. In lizards, sexual dichromatism and within-individual changes of colour can influence the level of their crypsis and thus influence antipredator behaviour and the decision to flee. Here, we examined variation in coloration and antipredator behaviour between the sexes of the Achala copper lizard (Pristidactylus achalensis). We measured sexual dichromatism and crypsis in accordance with avian vision. We also exposed lizards to a raptor dummy to assess the colour change and behaviour at the detection and approach stages of the predatory event. Finally, we tested escape behaviour in the natural habitat. We found that males were more conspicuous than females. Additionally, individuals showed distinct behaviours at different stages of the predation simulation, but there were no differences between the sexes. However, in their natural habitat males initiated flight at greater distances than females, which might be related to their more conspicuous coloration. In summary, this study shows how differences in crypsis between the sexes affect escape behaviour during the approach stage of predation.

Thermal dependence and individual variation in tonic immobility varies between sympatric amphibians

Tonic immobility (TI) is an important antipredator response employed by prey in the last stages of a predation sequence. Evolution by natural selection assumes consistent individual variation (repeatability) in this trait. In ectotherms, which experience variable body temperatures, TI should be repeatable over a thermal gradient to be targeted by natural selection; however, information on thermal repeatability of this trait is missing. We examined thermal repeatability of TI in juveniles of two sympatric amphibians, smooth (Lissotriton vulgaris) and alpine (Ichthyosaura alpestris) newts. Both species showed disparate TI responses to body temperature variation (13-28°C). While the proportion of TI response was repeatable in both taxa, it increased with body temperature in alpine newts but was temperature independent in smooth newts. Duration of TI decreased with body temperature in both taxa but was only repeatable in smooth newts. Our results suggest that a warming climate may affect population dynamics of sympatric ectotherms through asymmetry in thermal reaction norms for antipredator responses.

Changes in feeding behavior of longfin squid (Doryteuthis pealeii) during laboratory exposure to pile driving noise

Anthropogenic noise can cause diverse changes in animals' behaviors, but effects on feeding behaviors are understudied, especially for key invertebrate taxa. With the offshore wind industry expanding, concern exists regarding potential impacts of pile driving noise on squid and other commercially and ecologically vital taxa. We investigated changes in feeding and alarm (defense) behaviors of squid, Doryteuthis pealeii, predating on killifish, Fundulus heteroclitus, during playbacks of pile driving noise recorded from wind farm construction within squids' habitat. Fewer squid captured killifish during noise exposure compared to controls. Squid had more failed predation attempts when noise was started during predation sequences. Alarm responses to noise were similar whether or not squid were hunting killifish, indicating similar vigilance to threat stimuli in these contexts. Additionally, novel hearing measurements on F. heteroclitus confirmed they could detect the noise. These results indicate noise can disrupt feeding behaviors of a key invertebrate species, and will leverage future studies on how noise may disrupt squids’ vital ecological interactions.

Incorporating alternative interaction modes, forbidden links and trait‐based mechanisms increases the minimum trait dimensionality of ecological networks

Abstract Individual‐level traits mediate interaction outcomes and community structure. It is important, therefore, to identify the minimum number of traits that characterise ecological networks, that is, their ‘minimum dimensionality’. Existing methods for estimating minimum dimensionality often lack three features associated with increased trait numbers: alternative interaction modes (e.g. feeding strategies such as active vs. sit‐and‐wait feeding), trait‐mediated ‘forbidden links’ and a mechanistic description of interactions. Omitting these features can underestimate the trait numbers involved, and therefore, minimum dimensionality. We develop a ‘minimum mechanistic dimensionality’ measure, accounting for these three features. The only input our method requires is the network of interaction outcomes. We assume how traits are mechanistically involved in alternative interaction modes. These unidentified traits are contrasted using pairwise performance inequalities between interacting species. For example, if a predator feeds upon a prey species via a typical predation mode, in each step of the predation sequence, the predator's performance must be greater than the prey's. We construct a system of inequalities from all observed outcomes, which we attempt to solve with mixed integer linear programming. The number of traits required for a feasible system of inequalities provides our minimum dimensionality estimate. We applied our method to 658 published empirical ecological networks including primary consumption, predator–prey, parasitism, pollination, seed dispersal and animal dominance networks, to compare with minimum dimensionality estimates when the three focal features are missing. Minimum dimensionality was typically higher when including alternative interaction modes (54% of empirical networks), ‘forbidden interactions’ as trait‐mediated interaction outcomes (92%) or a mechanistic perspective (81%), compared to estimates missing these features. Additionally, we tested minimum dimensionality estimates on simulated networks with known dimensionality. Our method typically estimated a higher minimum dimensionality, closer to the actual dimensionality, while avoiding the overestimation associated with a previous method. Our method can reduce the risk of omitting traits involved in different interaction modes, in failure outcomes or mechanistically. More accurate estimates will allow us to parameterise models of theoretical networks with more realistic structure at the interaction outcome level. Thus, we hope our method can improve predictions of community structure and structure‐dependent dynamics.

Experimental assessment of trophic ecology in a generalist spider predator: Implications for biocontrol in Uruguayan crops

AbstractConservative biological control promotes the use of native natural enemies to limit the size and growth of pest populations. Although spiders constitute one of the most important groups of native predators in several crops, their trophic ecology remains largely unknown, especially for several generalist taxa. In laboratory, we assessed the predatory behaviour of a wandering spider (the wolf spider Lycosa thorelli (Keyserling, 1877) against several arthropods varying in size and trophic positions, all found in South American soybean and rice crops. As prey we used the bug Piezodorus guildinii (Westwood, 1837) as well as larvae and adults of the moth Spodoptera frugiperda (Smith, 1797), both being considered important pests in Uruguayan crops. We also used several non‐pest arthropods as prey, sarcophagid flies, carabid beetles and wolf spiders. All prey were attacked in more or less high, although not statistically differing, proportions. However, carabids were not consumed, and bugs were consumed in significantly lower proportions than flies. A negative correlation was found between prey size and acceptance rate. Immobilization times were longer against larvae when compared to moths and flies, while predatory sequences were longer for bugs when compared to flies, moths and spiders. In addition, we found a positive effect of prey size on predatory sequence length and complexity. Our results confirm the ability of spiders to attack and feed upon prey with different morphologies, included well‐defended arthropods, and their potential use as natural enemies of several pests in South American crops.