Antipredator Research Articles

Evolutionary Drivers of Conspicuous Spots in Velvet Ants (Hymenoptera: Dasymutilla).

Predation plays an important role in animal evolution by selecting for antipredator adaptations. Antipredator color adaptations include conspicuous spots, which are believed to provide protection by deflecting attacks to harmful or peripheral body parts, deimatic signaling, or as conspicuous warning coloration. The utility of antipredator signals is context-dependent and may be influenced by the environment. In this study, we investigated the selective forces acting on the evolution of conspicuous spots on velvet ants (Mutillidae: Dasymutilla). We tested whether conspicuous spots in 80 species of velvet ants evolved in (i) forest-dwelling species, (ii) habitat-generalist species, or (iii) species predated by diverse birds and frogs. Results show that conspicuous spots are more likely to evolve in forest-dwelling species and in areas with more canopy cover, whereas species inhabiting open areas and deserts tend to lose them. Moreover, taxa with conspicuous spots transition between open and forested habitats less often. Spot presence was not associated with predator diversity. We suggest that spots in velvet ants require complex visual environments to be effective, which may limit their habitat occurrence. In simpler environments, carrying conspicuous spots could be costly due to increased exposure to visual predators.

Parrots live in smaller groups on islands.

Species living on islands are predictably different from their mainland counterparts in morphology and behaviour, but the source of these differences is still debated. Islands, in particular, are characterized by depauperate predator communities. Relaxed predation pressure might explain why living in groups, a common anti-predator adaptation in animals, is considered less likely on islands. However, the empirical evidence for this effect is scant and alternative explanations have been overlooked. For instance, smaller groups might be more common because island species are less studied, because a more stable food supply associated with benign climate on islands favours territoriality, or because the population density is too low to allow the formation of larger groups. I examined the determinants of foraging group size in parrots, a large worldwide avian order with many island populations. Using a multivariable phylogenetic framework, I found that foraging group size was smaller on islands than on the continents controlling for ecological variables known to influence group size such as diet and body size. In addition, the island effect persisted after controlling for research effort, climate variables and population density, suggesting that impoverished predator communities are an important driver of group size on islands.

A non‐monophyly of ‘crowned’ Daphnia (Ctenodaphnia) Dybowski et Grochowski, 1895 (Cladocera: Daphniidae): From genomes to morphology

AbstractDaphnia (Crustacea: Cladocera) has been frequently used as a model taxon for studying prey antipredator defences. Among numerous representatives of this genus, there are several taxa within the subgenus Daphnia (Ctenodaphnia) with a morphological innovation unique for these cladocerans, a head plate. In some populations, the margin of this anterior projection of carapace into the head shield is adorned with a remarkable ‘crown of thorns’, which has been shown to be an antipredator adaptation against tadpole shrimps (Notostraca). This structure is phenotypically plastic, dependent on the presence of these omnivorous crustaceans in the respective water bodies. We aimed to evaluate the monophyly of Eurasian ‘crowned’ Daphnia species (i.e., those forming the ‘crown of thorns’ under some circumstance) based on genomic phylogenies and morphology. For this study, we have individually sequenced the genomes of five daphniids, four representing taxa able to form ‘crowns’ (two specimens of different clades of the D. (C.) atkinsoni complex and two specimens of D. (C.) triquetra from distant populations), and D. (C.) mediterranea distantly related to D. (C.) atkinsoni that lacks the head plate. We analysed them along with genomes obtained from GenBank, focusing on either full mitochondrial or partial nuclear datasets (BUSCO). Our main hypothesis on a monophyly of all ‘crowned’ daphnids was rejected. Genomic analyses confirmed existence of two independent lineages able to express this phenotypic trait in the Palaearctic: (1) a monophyletic D. (C.) atkinsoni s. lat. and (2) D. (C.) triquetra, formally redescribed here. These lineages form a well‐supported clade together with several other species lacking a head plate (including D. (C.) mediterranea). Genomic analyses indicate that D. (C.) atkinsoni s. lat. is closely related to D. (C.) tibetana; mitochondrial markers also suggest a close relationship of D. (D.) triquetra with D. (C.) studeri, both D. (C.) tibetana and D. (C.) studeri, are lacking this morphological feature. Molecular clock estimated the time of the differentiation of the major clade containing both ‘crowned Daphnia’ to the Late Mesozoic, confirming an antiquity of the head plate as antipredator defence.

An ant-mimicking ant on an oceanic archipelago: Camponotus guanchus mimics Crematogaster alluaudi-An analogy with the situation of Camponotus lateralis (Hymenoptera: Formicidae).

Mimicry, that is, the imitation of any unpalatable or defensive species by another, has been of central interest to evolutionary research since Darwin's lifetime. Two ant species, Camponotus guanchus Santschi, 1908 and Crematogaster alluaudi Emery, 1893, endemic to the Canary Islands, occur in two color-morphs: While the head of workers is always reddish and the gaster blackish, the mesosoma (inclusive waist) is either fully reddish or fully blackish. In addition to the obvious morphological and coloration similarities, we provide evidence of mimicry: (i) Ca. guanchus was found only within the area of Cr. alluaudi. (ii) Color morphs are geographically non-randomly distributed: Workers of both species from 16 localities of syntopic occurrences shared in eight cases a blackish and in eight cases a reddish mesosoma. Hence, Ca. guanchus mimics both local color-morphs of Cr. alluaudi. We consider a fascinating analogy with the Mediterranean mimicry system in Camponotus lateralis (Olivier, 1792) and its model species of the Crematogaster scutellaris (Olivier, 1792) group on an island scale. Additionally, we present two endemic bug species, Perenotus stysi (Ribes etal., 2008) and P. malobae Roca-Cusachs & Goula, 2016, as mimics of those Cr. alluaudi workers having a reddish mesosoma. Our distribution, coloration, frequency, and behavioral data as well as the analogy with Ca. lateralis and the Cr. scutellaris group suggest a Batesian-mimicry system in which Ca. guanchus, Perenotus stysi, and P. malobae mimic the unpalatable and aggressive Cr. alluaudi as an antipredator adaptation.

Disguise or surprise: spider antipredator adaptations as a function of the architecture of their webs

Abstract Animals exhibit a variety of strategies to avoid predation; spiders are no exception. We explored whether web-building spiders that differ in the architecture of their webs exhibit morphologies or behaviors suggestive of antipredator strategies that trade-off with the degree of protection offered by their webs. Spiders build webs of 3 types: the more protected tangles and sheet-and-tangles, which are three-dimensional (3D), and the more exposed orbs, which are two-dimensional (2D), both with or without a refuge. We hypothesize that spiders whose webs offer greater protection—a 3D architecture or a refuge—will be less likely to be armored or brightly colored when compared to spiders without these protections. We collected data on 446 spiders and their webs in 2 lowland tropical rainforest sites. We show that 2D web builders with no refuges tended to be brightly colored (background contrasting) and spiny (spiky), whereas those with refuges tended to blend against the background of their refuges. 3D web builders, on the other hand, were neither cryptic nor brightly colored nor armored but were more likely to drop out of the web upon simulated predator contact. These results support the hypothesis that web-building spiders tend to be protected either through the architecture of their webs or their morphology and behavior, suggesting a trade-off between different types of antipredator strategies.

The divergence of mobility and activity associated with anti-predator adaptations in land snails

Abstract The extreme divergence of phenotypes between two closely related terrestrial gastropods, Karaftohelix editha and K. gainesi (Camaenidae, Stylommatophora), has been suggested as a result of anti-predator adaptations because K. editha and K. gainesi showed shy and bold anti-predator behaviours, respectively. In this study, we measured the crawling speeds in the laboratory and the exploration (the crawled distances during every 6 h) and the activity (the active/inactive statuses) in the field for each species. As a result, K. gainesi crawled faster under ordinary conditions and moreover upregulated its crawling speed 1.21–1.28 times after the stimulus. The activity pattern of K. editha was typical of nocturnal species, but K. gainesi remained active even under daylight. These results might suggest that K. editha and K. gainesi were deemed as shy/inactive and bold/active species, respectively, and that behavioural syndromes existed between shyness–boldness and activity personalities.

You are what your ancestors ate: retained bufadienolide resistance in the piscivorous water cobra Naja annulata (Serpentes: Elapidae)

Predators exploiting chemically defended prey are generally resistant to prey toxins. However, toxin resistance usually incurs a fitness cost and is therefore often lost when no longer needed. Bufonid toads are a frequently abundant food resource, but chemically defended by a group of cardiotonic steroids, bufadienolides. Bufophagous predators have evolved a specific and near-universal mechanism of resistance to these toxins, consisting of two amino acid substitutions in the Na+/K+-ATPase H1–H2 extracellular domain. The dynamics of loss or retention of this adaptation in secondarily non-bufophagous lineages remain inadequately understood. Here we explore this topic by showing that the piscivorous banded water cobra Naja annulata retains the bufadienolide-resistant genotype of the otherwise toad-eating cobra clade. This confirms a trend for secondarily non-toad-eating snakes to retain bufadienolide resistance. Keywords: Antipredator adaptation, cardiotonic steroid, cardiac glycoside, evolution, piscivory

Artificial light at night causes conflicting behavioural and morphological defence responses in a marine isopod.

Encroachment of artificial light at night (ALAN) into natural habitats is increasingly recognized as a major source of anthropogenic disturbance. Research focussed on variation in the intensity and spectrum of ALAN emissions has established physiological, behavioural and population-level effects across plants and animals. However, little attention has been paid to the structural aspect of this light, nor how combined morphological and behavioural anti-predator adaptations are affected. We investigated how lighting structure, background reflectance and the three-dimensional properties of the environment combined to affect anti-predator defences in the marine isopod Ligia oceanica. Experimental trials monitored behavioural responses including movement and background choice, and also colour change, a widespread morphological anti-predator mechanism little considered in relation to ALAN exposure. We found that behavioural responses of isopods to ALAN were consistent with classic risk-aversion strategies, being particularly exaggerated under diffuse lighting. However, this behaviour was disconnected from optimal morphological strategies, as diffuse light caused isopods to become lighter coloured while seeking out darker backgrounds. Our work highlights the potential for the structure of natural and artificial light to play a key role in behavioural and morphological processes likely to affect anti-predator adaptations, survival, and ultimately wider ecological effects.

How to Survive a (Juvenile) Piranha Attack: An Integrative Approach to Evaluating Predator Performance.

Cory cat panel figureDrawing of bite force measuring equipment and indentation rig Pygocentrus nattereri jaw muscle morphology and skull anatomyBox plot grid of number of Pygocentrus nattereri bites before puncture along different body regions of Corydoras trilineatus during feeding trials resultsDrawing of color-coded Corydoras trilineatus with attack frequencies and average bites until puncture by Pygocentrus nattereriBox plot of average voluntary juvenile Pygocentrus nattereri bite forces to standard lengthPanel of linear ordinary least-squares regressions of Pygocentrus nattereri bite force to adductor mandibulae mass, standard length, and body massOrdinary least-squares regressions of voluntary bites to restrained bites of Pygocentrus nattereriPanel of indentation tests for intact and removed Corydoras trilineatus scutesPanel of indentation tests for Corydoras trilineatus body region. There is an evolutionary arms race between predators and prey. In aquatic environments, predatory fishes often use sharp teeth, powerful bites, and/or streamlined bodies to help capture their prey quickly and efficiently. Conversely, prey are often equipped with antipredator adaptations including: scaly armor, sharp spines, and/or toxic secretions. This study focused on the predator-prey interactions between the armored threestripe cory catfish (Corydoras trilineatus) and juvenile red-bellied piranha (Pygocentrus nattereri). Specifically, we investigated how resistant cory catfish armor is to a range of natural and theoretical piranha bite forces and how often this protection translated to survival from predator attacks by Corydoras. We measured the bite force and jaw functional morphology of P. nattereri, the puncture resistance of defensive scutes in C. trilineatus, and the in situ predatory interactions between the two. The adductor mandibulae muscle in juvenile P. nattereri is robust and delivers an average bite force of 1.03 N and maximum bite force of 9.71 N, yet its prey, C. trilineatus, survived 37% of confirmed bites without any damage. The C. trilineatus armor withstood an average of nine bites before puncture by P. nattereri. Predation was successful only when piranhas bit unarmored areas of the body, at the opercular opening and at the caudal peduncle. This study used an integrative approach to understand the outcomes of predator-prey interactions by evaluating the link between morphology and feeding behavior. We found that juvenile P. nattereri rarely used a maximal bite force and displayed a net predation success rate on par with other adult vertebrates. Conversely, C. trilineatus successfully avoided predation by orienting predator attacks toward their resilient, axial armor and behavioral strategies that reduced the predator's ability to bite in less armored regions of the body.

Predator–prey ecological system with group defense and anti-predator traits of the preys: Synergies between two important ecological actions

During smart anti-predator adaptations, preys use their size, fleeing capability and herd in their evolutionary tug-of-war with the predators. Predator–prey ecology is teeming with such examples where predators can be defeated or even killed by the group of victims, that is, preys, banding together. In this paper, we focus on a stage-structured predator–prey model with herd behavior and anti-predator phenomenon that results in the lesser ecological opportunities for predation in the presence of the smart anti-predatory constraints. It is our purpose in this paper to illustrate the combined effects of the herd behavior and anti-predator strategy on the predator–prey ecology. By constructing the model equations, we present an analytical study of the system and the occurrence of Hopf and transcritical bifurcation for the anti-predator rate as a bifurcation parameter. Conditions for co-existence under global stable interior equilibrium as well as permanence region for the survival of all species is adequately discussed. Also, the extinction of predators is explored via numerical simulations, that is, the prey population survives successfully in the habitat due to their defense mechanism and anti-predator behavior. In order to better understand the role of anti-predator traits in predator–prey system with square root functional response, we compare the theoretical and numerical results of the proposed model with a similar predator–prey system having Holling type-I functional response. Our findings show that the predator–prey dynamics under prey’s herd behavior and anti-predator tactics can have large influence on shifting the paradigm of predator–prey relationship by turning the predator–prey dynamics into the prey dominant dynamics, which is indeed, due to the smart synergy between both ecological actions. When underdog, sticking together, fights back, that would be a headache to deal with, no matter how menacing the predator is.

Commentary: using prey naïveté to inform ecological management.

Commentary: using prey naïveté to inform ecological management.

Free-range domestic chickens can distinguish between different alarm calls of Japanese tits.

Heterospecific eavesdropping of alarm information is an anti-predator adaptation in the wild as it improves the monitoring of shared predators and hence provides opportunities to avoid predators. Our current understanding of heterospecific eavesdropping information is based primarily on studies of bird, primate, or ungulate populations in the wild, whereas little is known regarding the ability of domesticated species to respond to alarm signals from wild individuals. Using sound playback experiments, we assessed the behavioral responses of free-range domestic chickens (Gallus gallus domesticus) in Hainan to alarm calls (test playback) and songs (control playback) of wild Japanese tits (Parus minor). The results revealed that free-range domestic chickens showed greater vigilance to the alarm calls of Japanese tits than to the songs of Japanese tits, especially their alarm calls for Siberian chipmunks (Tamias sibiricus). Furthermore, individual-foraging single chickens were significantly more vigilant than those foraging collectively in groups. Our findings suggest that free-range domestic chickens are as capable as wild birds in responding to heterospecific alarm calls and are likely to be able to distinguish between different types of heterospecific alarm calls.

Predator responses to prey camouflage strategies: a meta-analysis.

Although numerous studies about camouflage have been conducted in the last few decades, there is still a significant gap in our knowledge about the magnitude of protective value of different camouflage strategies in prey detection and survival. Furthermore, the functional significance of several camouflage strategies remains controversial. Here we carried out a comprehensive meta-analysis including comparisons of different camouflage strategies as well as predator and prey types, considering two response variables: mean predator search time (ST) (63 studies) and predator attack rate (AR) of camouflaged prey (28 studies). Overall, camouflage increased the predator ST by 62.56% and decreased the AR of prey by 27.34%. Masquerade was the camouflage strategy that most increased predator ST (295.43%). Background matching and disruptive coloration did not differ from each other. Motion camouflage did not increase ST but decreases AR on prey. We found no evidence that eyespot increases ST and decreases AR by predators. The different types of predators did not differ from each other, but caterpillars were the type of prey that most influenced the magnitude of camouflage's effect. We highlight the potential evolutionary mechanisms that led camouflage to be a highly effective anti-predatory adaptation, as well as potential discrepancies or redundancies among strategies, predator and prey types.

The effect of spatial and temporal scale on camouflage in North African rodents

Abstract Background matching, a common form of camouflage, is a widespread anti-predator adaptation that hinders detection or recognition by increasing the resemblance of prey to its environment. However, the natural environment is complex and both spatially and temporally variable, which constrains effective background matching as an anti-predator strategy. Here, using remote sensing data (publicly available satellite imagery), we investigated how variation of habitat parameters predicts background matching in 16 Sahara–Sahel rodent species across spatial and temporal scales. All fur colour parameters (hue, saturation and brightness) strongly matched the respective habitats of the different species. Background matching in terms of hue was best at the microscale, whereas results for saturation and brightness showed more variation across spatial scales among species. Camouflage across the temporal scale (from 1 to 3 years before capture) was variable among species for all colour parameters. These complex interactions suggest that, in desert rodents, colour parameters are differentially sensitive to the respective scale of the habitat, plausibly reflecting the behaviour and life history of the species and the ecological properties determining their activity patterns. Consequently, the division between habitat (camouflage) generalists and specialists might become blurred in temporally changing and spatially variable environments.

Decrease in the rewarding value of spatial novelty due to the contamination of the stimulus field with light – Evidence from a free exploration test involving rats

It has been shown that rearranging the spatial properties of a familiar environment consistently elicits a positive response in rats directed toward the source of novelty. Previous studies have been conducted under red light or darkness. The purpose of this study was to test the effect of rearranging the spatial properties of a familiar environment in conjunction with a change in lighting conditions. The results have shown specific effects of the light presence and its intensity on different behavioral measures. We propose that this study provides a basis for hypothesizing a two-way mechanism of the behavioral response to light regulation in rats. The first is based on ON/OFF states. This level may be related to fundamental, evolutionarily early, emergent components of behavioral antipredator adaptations. Another level of behavioral regulation involves mechanisms sensitive to light intensity. These appear to be involved in the regulation of more advanced behavioral acts, such as exploratory responses. This may suggest that light intensity analysis may require the involvement of more advanced cognitive components in the behavioral regulation system.

Cognition contra camouflage: How the brain mediates predator-driven crypsis evolution.

While crypsis is a prominent antipredator adaptation, the role of the brain in predator-driven evolution remains controversial. Resolving this controversy requires contextualizing the brain with established antipredator traits and predation pressure. We hypothesize that the reduced predation risk through crypsis relaxes predation-driven selection on the brain and provide comparative evidence across 102 Chinese frog species for our hypothesis. Specifically, our phylogenetic path analysis reveals an indirect relationship between predation risk and crypsis that is mediated by brain size. This result suggests that at a low predation risk, frogs can afford to be conspicuous and use their large brain for cognitive predator evasion. This strategy may become less efficient or energetically costlier under higher predation pressure, favoring smaller brains and instead increasing crypsis.

Social information-mediated population dynamics in non-grouping prey

Inadvertent social information (ISI) use, i.e., the exploitation of social cues including the presence and behaviour of others, has been predicted to mediate population-level processes even in the absence of cohesive grouping. However, we know little about how such effects may arise when the prey population lacks social structure beyond the spatiotemporal autocorrelation originating from the random movement of individuals. In this study, we built an individual-based model where predator avoidance behaviour could spread among randomly moving prey through the network of nearby observers. We qualitatively assessed how ISI use may affect prey population size when cue detection was associated with different probabilities and fitness costs, and characterised the structural properties of the emerging detection networks that would provide pathways for information spread in prey. We found that ISI use was among the most influential model parameters affecting prey abundance and increased equilibrium population sizes in most examined scenarios. Moreover, it could substantially contribute to population survival under high predation pressure, but this effect strongly depended on the level of predator detection ability. When prey exploited social cues in the presence of high predation risk, the observed detection networks consisted of a large number of connected components with small sizes and small ego networks; this resulted in efficient information spread among connected individuals in the detection networks. Our study provides hypothetical mechanisms about how temporary local densities may allow information diffusion about predation threats among conspecifics and facilitate population stability and persistence in non-grouping animals.Significance statementThe exploitation of inadvertently produced social cues may not only modify individual behaviour but also fundamentally influence population dynamics and species interactions. Using an individual-based model, we investigated how the detection and spread of adaptive antipredator behaviour may cascade to changes in the demographic performance of randomly moving (i.e., non-grouping) prey. We found that social information use contributed to population stability and persistence by reducing predation-related per capita mortality and raising equilibrium population sizes when predator detection ability reached a sufficient level. We also showed that temporary detection networks had structural properties that allowed efficient information spread among prey under high predation pressure. Our work represents a general modelling approach that could be adapted to specific predator-prey systems and scrutinise how temporary local densities allow dynamic information diffusion about predation threats and facilitate population stability in non-grouping animals.

Lack of anti-predator recognition in a marine isopod under the threat of an invasive predatory crab

The prey naïveté hypothesis suggests that the failure of prey to recognize novel predators as a threat is caused by a lack of anti-predator adaptations. We tested this hypothesis in a unique natural setting, where the isopod Idotea balthica encountered the rapidly spreading invasive crab, Rhithropanopeus harrissii. Earlier research had indicated high mortality of the isopods during exposure to R. harrissii. The isopod exerted no co-evolutionary history with any littoral crabs and thus the strong impact could be caused by lack of pre-adaptations towards the new predator species. We tested this hypothesis by studying the anti-predator responses of the isopods with water-born cues of R. harrissii and of the native predatory fish Perca fluviatilis. Compared to control water, the isopods lowered their activity when exposed to the fish cue. Instead crab cue did not induce anti-predator behaviour. We also tested the hypothesis that mortality caused by novel predator, similar to predation by P. fluviatilis, would result in differential selection for the two sexes and contribute to the evolution of personalities. However, we found no differences in anti-predator behaviour nor in mortality between the sexes or personalities of the isopods. The outcomes reveal an interesting evolutionary scenario, where predation by a local predator induce soft selection on prey characteristics, but an invasive species cause hard selection without differentiating between prey individuals. Our study—conducted in the dawn of the population outbreak of R. harrissii—provides an excellent reference point for studies resolving the evolutionary impacts of invasive predators on naïve prey.

Diving behavior in a Neotropical spider (Trechalea extensa) as a potential antipredator tactic

AbstractThreat of predation often requires animals to seek refuge in unusual or suboptimal habitats. While aquatic refugia are thought to be used by many terrestrial animal species, there are challenges associated with aquatic refugia that could preclude their actual usefulness, particularly to air‐breathing ectotherms. Consequently, observations that can shed light on the evolution of antipredator strategies that cross the air–water interface are particularly valuable. “Semi‐aquatic” spiders in the family Trechaleidae have not been documented using diving as part of their antipredator behavior and, indeed, they are rarely known to submerge themselves at all, as their aquatic foraging occurs from a terrestrial location. The lack of diving behavior is hypothesized to be due to the high potential costs (e.g., thermal and respiratory) of submergence. Despite this, we document the prolonged underwater refuge use (>30 min) of Trechalea extensa following pursuit by a perceived threat (humans). We also identify some morphological adaptations that may potentially help counterbalance these costs and permit underwater antipredator behavior, specifically the ability of cuticular hairs to provide a hydrophobic surface, allowing the formation of a plastron that, in turn, may facilitate respiratory function and reduce heat loss. These observations expand our overall understanding of habitat use in this genus and, more generally, antipredator adaptations of spiders.

PREDATION ON ADULT LONG-TOED SALAMANDERS AND A NORTHERN RED-LEGGED FROG BY A BELTED KINGFISHER ON VANCOUVER ISLAND, BRITISH COLUMBIA: A REVIEW OF DEFENSIVE STRATEGY ADAPTATIONS

A case of predation by a Belted Kingfisher (Megaceryle alcyon) on adult Long-toed Salamanders (Ambystoma macrodactylum) and a Northern Red-legged Frog (Rana aurora) is reported. This general note provides a description of the predation events with photographs of the amphibians being devoured. Additional photographs showing scars in long-toed salamanders are presented and considered in review of types of predatory attacks and defensive strategies. A literature review was completed to identify reported cases of predation on these two amphibian species. We discuss what is known about their anti-predator defensive strategies and what species are involved in the ecological and evolutionary dynamics at play. Traits exhibited by these amphibians are discussed as anti-predator adaptations that include warning colorations, defensive postures, tail dropping, crypsis, and glandular skin secretions that can be adhesive, unpalatable, or toxic. A potentially significant role of avian predators is considered in light of the evidence presented.