Tonic immobility behaviour does not differ between fire salamander larvae from ponds and streams.

Tonic immobility is an antipredator defence in which the prey animal remains motionless after physical contact with the predator, pretending to be dead. This behaviour has been observed among a variety of taxa but has received only little attention in amphibian larvae. During our field studies with fire salamander larvae, we observed that larvae from different habitats display tonic immobility after handling. In our study site, we find larvae in pond and stream habitats, that differ in several aspects such as their stress response and their risk-taking behaviour, likely caused by the very different habitat conditions. We measured the time that the tonic immobility behaviour was displayed but found no difference between larvae from the two habitat types. Likewise, we also found no correlation between the size of the larvae and the duration of displaying the behaviour. In conclusion, we found that fire salamander larvae show tonic immobility, but found no evidence that the different habitat conditions influence the tonic immobility behaviour.

Drop dead! Female mate avoidance in an explosively breeding frog.

Males' and females' reproductive strategies may differ, potentially leading to sexual conflict. Increased efforts by males (harassment, forced copulation, intimidation) to gain access to females could even negatively affect female survival and thus lead to reproductive failure for both individuals. In anurans, a higher mortality risk of mating females has been reported in explosive breeding species. During these mating events, several males cling to a female, which are mostly unable to get rid of the unwanted males. This can lead to the female's death. From the literature, it seems that females of explosive breeding frogs have no means to reject unwanted males. Here we describe female mate avoidance behaviours in the European common frog. We observed three female avoidance behaviours, namely 'rotation', 'release call(s)' and tonic immobility (death feigning). These behaviours were significantly associated with smaller female body size, and smaller females were more successful in escaping amplexus. Tonic immobility as a tactic to avoid mating or male harassment has only been observed in a handful of species and only in one other amphibian. Our observations show that females in explosive breeding frogs may not be as passive and helpless as previously thought.

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.

Behavioural Repeatability and Behavioural Syndrome in the Dung Beetle Copris umbilicatus (Coleoptera, Scarabaeidae).

Although personality studies have primarily focused on vertebrates, the evidence showing invertebrates to be capable of displaying personalities has been steadily growing in recent years. In this study, we investigated the behavioural repeatability (repetition of a behaviour over time) and behavioural syndromes (a set of correlated behaviours) in Copris umbilicatus, which is a dung beetle species showing complex sub-social behaviour. We analysed three behaviours (activity, thanatosis and distress call emission) by measuring seven distinct behavioural traits (i.e., three activity-, one thanatosis- and three distress call-related traits). We found moderate to high levels of individual repeatability in all behavioural traits considered. The duration of thanatosis was inversely correlated with two activity traits, hinting a behavioural syndrome for thanatosis and activity, with bolder individuals exhibiting shorter thanatosis and higher locomotor activity in contrast with fearful individuals, which display longer thanatosis and poor locomotor activity. No relationships were found between the behavioural traits and body size or sex. Results of the principal component analysis (PCA) suggested personality differences among individuals. Dung beetles provide an impressive variety of ecosystem services. Since the provision of these services may depend on the personalities represented in local populations and communities, studies on the ecology of personality in dung beetles should be encouraged in future research.

Latitudinal cline of death-feigning behaviour in a beetle (Tribolium castaneum).

Death-feigning behaviour is a phenomenon in which a prey is rendered motionless due to stimulation or threat from a predator. This anti-predator defence mechanism has been observed across numerous animal taxa and is considered adaptive in nature. However, longer durations of death feigning can result in decreased opportunities for feeding and reproduction, and therefore is often associated with fitness costs as compared to environments without predators. Differences have also been observed in the frequencies and durations of death feigning within populations, and these differences are thought to be influenced by the balance between survival and other fitness costs. Furthermore, this balance is predicted to vary in response to changes in environmental conditions. In this study, we examined the death feigning in 38 populations of the red flour beetle (Tribolium castaneum). Our results demonstrate that frequencies and durations of the death feigning in T. castaneum show geographical variations and a latitude cline, indicating that this behaviour is influenced by location as well as latitude. This study is the first to demonstrate the existence of a latitudinal cline in death feigning and suggests that death-feigning behaviour might have evolved in response to environmental factors that vary with latitude.

Freezing or death feigning? Beetles selected for long death feigning showed different tactics against different predators.

Prey evolve antipredator strategies against multiple enemies in nature. We examined how a prey species adopts different predation avoidance tactics against pursuit or sit-and-wait predators. As prey, we used three strains of Tribolium beetles artificially selected for short (short strain) or long (long strain) duration of death feigning, and a stock culture (base population). Death feigning is known to be effective for evading a jumping spider in the case of the long strains, while the present study showed that the long-strain beetles used freezing against a sit-and-wait type predator, Amphibolus venator, in this study. The short- strain beetles were more easily oriented toward predators. The time to predation was also shorter in the short strains compared to the long strains. The results showed that, as prey, the short strains displayed the same behavior, escaping, against both types of predators. Traditionally, death feigning has been thought to be the last resort in a series of antipredator avoidance behaviors. However, our results showed that freezing and death feigning were not parts of a series of behaviors, but independent strategies against different predators, at least for long-strain beetles. We also examined the relationship between a predator's starvation level and its predatory behavior. In addition, the orientation behavior toward and predation rate on the prey were observed to determine how often the predatory insect attacked the beetles.

Morphology of immature stages, biology, and systematic position of the Violet seed weevil, Orobitiscyanea (Linnaeus, 1758) (Curculionidae, Conoderinae, Orobitiditae, Orobitidini).

The mature larva of the weevil species Orobitiscyanea (Linnaeus, 1758), one of only two Palaearctic members of the supertribe Orobitiditae, is re-described, while the pupa is described for the first time. The biology of this species was studied at two sites in Germany. It was reared from seed capsules of Violacanina L. (Violaceae), and feeding holes were observed on V.riviniana Rchb. Adults of Orobitiscyanea and O.nigrina Reitter, 1885, specialists of Viola, show a well-developed escape mechanism, to which contribute a smooth surface, a rounded, nearly spherical body shape, and a seed-imitating thanatosis behaviour. The molytine weevil Leiosomacribrum (Gyllenhal, 1834), the only other known weevil specialist of Viola in Europe, has a smooth surface, also, and is the most spherical species of the genus. The unique characters of the larva and pupa of Orobitiscyanea are discussed in regard to the systematic position of this taxon.

Death is common, so is understanding it: the concept of death in other species.

Comparative thanatologists study the responses to the dead and the dying in nonhuman animals. Despite the wide variety of thanatological behaviours that have been documented in several different species, comparative thanatologists assume that the concept of death (CoD) is very difficult to acquire and will be a rare cognitive feat once we move past the human species. In this paper, we argue that this assumption is based on two forms of anthropocentrism: (1) an intellectual anthropocentrism, which leads to an over-intellectualisation of the CoD, and (2) an emotional anthropocentrism, which yields an excessive focus on grief as a reaction to death. Contrary to what these two forms of anthropocentrism suggest, we argue that the CoD requires relatively little cognitive complexity and that it can emerge independently from mourning behaviour. Moreover, if we turn towards the natural world, we can see that the minimal cognitive requirements for a CoD are in fact met by many nonhuman species and there are multiple learning pathways and opportunities for animals in the wild to develop a CoD. This allows us to conclude that the CoD will be relatively easy to acquire and, so, we can expect it to be fairly common in nature.

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.

Hide-and-seek strategies and post-contact immobility.

To understand why an animal might gain by playing dead, or more precisely, exhibit post-contact immobility (PCI), we consider the context in which this behaviour occurs. Is it, for example, a method by which a potential victim encourages a predator to direct its attention elsewhere? We investigate this possibility by using the marginal value theorem to analyse predator behaviour in the context of this defence strategy by potential prey. We consider two models. In the first, (random revisiting) the predator may return to sites it has already depleted within the patch. In the second, (systematic search) the predator goes only to new sites within the patch. The results of the two models are qualitatively extremely similar. We show that when prey occur in patches, PCI favours prey survival. Indeed, certain antlion larvae have PCI durations characterized by very long half-lives. These appear to be of such long durations that further increases would convey no substantial benefits in redirecting potential predators to other antlions within the patch and subsequently to other patches.

Tonic Immobility Is Influenced by Starvation, Life Stage, and Body Mass in Ixodid Ticks.

The ability to escape predation modulates predator-prey interactions and represents a crucial aspect of organismal life history, influencing feeding, mating success, and survival. Thanatosis, also known as death feigning or tonic immobility (TI), is taxonomically widespread, but understudied in blood-feeding vectors. Hematophagous arthropods, such as ticks, are unique among animals as their predators (birds, mice, lizards, frogs, and other invertebrates) may also be their source of food. Therefore, the trade-off between predator avoidance and host-seeking may shift as the time since the last bloodmeal increases. Because ticks are slow-moving and unable to fly, or otherwise escape, we predicted that they may use TI to avoid predation, but that TI would be influenced by time since the last bloodmeal (starvation). We therefore aimed to quantify this relationship, examining the effect of starvation, body mass, and ontogeny on TI for two tick species: Dermacentor variabilis (Say) (Acari: Ixodidae) and Rhipicephalus sanguineus (Latreille) (Acari: Ixodidae). As we predicted, the duration and use of TI decreased with time since feeding and emergence across species and life stages. Therefore, ticks may become more aggressive in their search for a bloodmeal as they continue to starve, opting to treat potential predators as hosts, rather than avoiding predation by feigning death. Antipredator behaviors such as TI may influence the intensity and amount of time ticks spend searching for hosts, driving patterns of tick-borne pathogen transmission. This identification and quantification of a novel antipredation strategy add a new component to our understanding of tick life history.

Post-contact immobility and half-lives that save lives.

A wide variety of animals become completely immobile after initial contact with a potential predator. This behaviour is considered to be a last-ditch escape strategy. Here, we test the hypothesis that such immobility should have an extremely unpredictable duration. We find that it spans more than three orders of magnitude in antlion larvae. We also analyse the second period of immobility that follows the first bout of immobility, and consider the distributions of both first and second immobility periods within the context of the intermittence that characterizes the movement of most organisms. Both immobility durations were fitted best by exponential distributions. Therefore, both were characterized by high variability and hence, unpredictability. The immobility half-life, its mean duration and standard deviation were greater for the first than the second immobility. Furthermore, individual consistency was weak or absent in repeated measures of the first immobility and between the first and second immobilities. Our quantitative approach can be replicated across taxa and would help link an understanding of immobility after an initial predator contact in both vertebrates and invertebrates. To facilitate this, we contend that the terminology should be simplified, and we advocate the use of the term post-contact immobility (PCI).

Death feigning as an adaptive anti-predator behaviour: Further evidence for its evolution from artificial selection and natural populations.

Death feigning is considered to be an adaptive antipredator behaviour. Previous studies on Tribolium castaneum have shown that prey which death feign have a fitness advantage over those that do not when using a jumping spider as the predator. Whether these effects are repeatable across species or whether they can be seen in nature is, however, unknown. Therefore, the present study involved two experiments: (a) divergent artificial selection for the duration of death feigning using a related species T. freemani as prey and a predatory bug as predator, demonstrating that previous results are repeatable across both prey and predator species, and (b) comparison of the death-feigning duration of T. castaneum populations collected from field sites with and without predatory bugs. In the first experiment, T. freemani adults from established selection regimes with longer durations of death feigning had higher survival rates and longer latency to being preyed on when they were placed with predatory bugs than the adults from regimes selected for shorter durations of death feigning. As a result, the adaptive significance of death-feigning behaviour was demonstrated in another prey-predator system. In the second experiment, wild T. castaneum beetles from populations with predators feigned death longer than wild beetles from predator-free populations. Combining the results from these two experiments with those from previous studies provided strong evidence that predators drive the evolution of longer death feigning.

Food habits and substrate use by the South American xenodontine snake Erythrolamprus frenatus, with comments on its brightly-coloured venter

Erythrolamprus frenatus belongs to the Family Dipsadidae, is distributed mainly within Cerrado areas of southeastern South America and it is poorly known in your diet and use of the substrate. Information on substrate use and diet was obtained from unpublished data provided by other researchers and specimens deposited in the herpetological collections, respectively. Five specimens were observed in the water, while two others were found on the ground, but close to bodies of water. Four prey items were recorded, and all of them being swamp eels of the family Synbranchidae. Our results providing important information on substrate use and diet of this species, and suggests that E. frenatus is a fish-eatinger snake, which seems to have specialized on elongated fishes. The presence of brightly colored belly in E. frenatus, suggests that this pattern may be a defensive tactic against aquatic predators.

Sexual differences in weaponry and defensive behavior in a neotropical harvestman.

Sexual differences in morphology can evolve by sexual selection and/or natural selection. In some species, only males have morphological structures that are used as weapons. Since some weapons may also be used for defensive purposes, males and females may behave differently towards predators. In some species of harvestmen (Arachnida and Opiliones), males have sharp apophyses ("spines") on their 4th pair of legs whereas females lack them. Those apophyses are used in male-male fights and in antipredatory behaviors. The harvestmen antipredatory repertory also encompasses passive defenses such as thanatosis (death feigning), retaliation (attack on predators), and chemical defense. Due to the sexual differences on weaponry, we hypothesized that males and females of Mischonyx cuspidatus (Gonyleptidae) rely on different defensive strategies. We experimentally induced males and females to perform 3 defensive behaviors: thanatosis, pinching with legs, and chemical release. We predicted that females would engage more in passive and chemical defenses than males, whereas males would rely more on retaliation than females. As expected, females performed thanatosis more often than males. Likewise, males performed retaliation more often than females. We did not find differences in the rate of chemical defense use between the sexes. This study provides evidence that due to sexual dimorphism, alternative antipredatory behaviors may have been selected in the different sexes in M. cuspidatus.

Sound repetition rate controls the duration of tonic immobility in chicks (Gallus gallus).

Tonic Immobility (TI) functions as anti-predator defense. Its duration depends on cues signaling predator proximity. One such cue includes alarm calls from conspecifics and non-conspecifics. This study aimed to determine the cue within alarm calls that controls TI duration. We induced TI in chicks (Gallus gallus) and found that their TI durations increased in the presence of adult conspecific alarm calls, non-conspecific alarm calls, and synthetic sounds made of white noise set to the repetition rate found in natural alarm calls. Moreover, chicks did not increase their TI durations when exposed to conspecific attraction calls, synthetic sounds made of white noise set to the repetition rate found in natural attraction calls, and derived sounds made of a natural alarm call lacking an internote interval. We then created: 1) sounds with white noise set to the internote interval found in natural alarm calls and the note duration found in natural attraction calls, and 2) sounds with white noise set to the internote interval found in natural attraction calls and the note duration found in natural alarm calls. Neither affected TI duration. We conclude that repetition rate acts as a salient cue that lengthens TI duration.

Arousal from Tonic Immobility by Vibration Stimulus.

Tonic immobility (TI) is an effective anti-predator strategy. However, long immobility status on the ground increases the risk of being eaten by predators, and thus insects must rouse themselves when appropriate stimulation is provided. Here, the strength of vibration causing arousal from the state of TI was examined in strains artificially selected for longer duration of TI (L-strains: long sleeper) in a beetle. We provided different strengths of vibration stimuli to the long sleepers in Tribolium castaneum. Although immobilized beetles were never awakened by the stimuli from 0.01 to 0.12 mm in amplitude, almost of the beetles were aroused from immobilized status by the stimulus at 0.21 mm. There was a difference in sensitivity of individuals when the stimuli of 0.14 mm and 0.18 mm were provided. F2 individuals were also bred by crossing experiments of the strains selected for shorter and longer duration of TI. The arousal sensitivity to vibration was well separated in the F2 individuals. A positive relationship was observed between the duration of TI and the vibration amplitude, suggesting that immobilized beetles are difficult to arouse from a deep sleep, while light sleepers are easily aroused by even small vibrations. The results indicate a genetic basis for sensitivity to arousal from TI.

Death-feigning behaviour in Iphisa elegans: the second reported case in the Family Gymnophthalmidae (Reptilia: Squamata) / Comportamento de tanatose em Iphisa elegans: o segundo caso na Família Gymnophthalmidae (Reptilia: Squamata)

Death-feigning behaviour occurs when the animal simulates a state of immobility. This behaviour is described for some lizard families, among them the family Gymnophthalmidae with only one record. Iphisa elegans is a diurnal and terrestrial Amazonian gymnophtalmid lizard. It has cryptic behavior and moves rapidly on the ground, hindering observations of its behavior. We report a case at the Comodoro Municipality, Mato Grosso State, Brazil. An adult male of I. elegans, when manipulated, turned its venter up and put itself in a death-feigning posture. This species is preyed upon by birds, snakes and other lizards¸ possibly behaving this way when the cryptic behaviour or escape attempt fails. More studies are necessary to evaluate the efficiency of this behaviour, as well as its frequency of occurrence, using individuals of both sexes. We also suggest to evaluate if the orange venter of males could have any antipredation advantage.

Fingir-se de morto é um comportamento no qual o animal simula um estado de imobilidade. Esse comportamento é descrito em algumas famílias de lagartos, dentre as quais, a família Gymnophthalmidae com apenas um registro. Iphisa elegans é um lagarto gymnoftalmídeo amazônico diurno e terrestre. Possui comportamento críptico e move-se rapidamente pelo solo, dificultando observações de seu comportamento. Reportamos um caso no município de Comodoro, Estado do Mato Grosso, Brasil: um macho adulto de I. elegans, quando manipulado, virou seu ventre para cima e fingiu-se de morto. Esta espécie é predada por pássaros, serpentes e outros lagartos, possivelmente portando-se dessa forma quando o comportamento críptico ou tentativa de fuga falham. São necessários mais estudos para observar a eficiência desse comportamento, assim como sua frequência de ocorrência, usando indivíduos de ambos os sexos. Também sugerimos que deve ser avaliado se a coloração alaranjada no ventre dos machos poderia fornecer alguma vantagem antipredação.

Aphids Playing Possum - Defensive or Mutualistic Response?

Paper presents the phenomenon of thanatosis or death-feigning in selected aphids species. This specific reaction was predominantly analysed on the example of aphid subfamily Lachninae. Individuals of this group were used in experiments, during which a thanatotic response was induced with various results. The response differed from prolonged thanatosis, lasting for several minutes (Eulachnus rileyi), through shrinking behaviour (e. g. in Stomaphis graffii) to non-responsive species such as Cinara (Schizolachnus) pineti. The large interspecies variation of observed responses can be linked to other defensive mechanisms existing in the studied species, as well as to their mutualistic relationship with ants. The behaviour of shrinking is hypothesized to be the mutualistic response, developed from thanatosis, and being adapted to transportation by ant workers.

A review of thanatosis (death feigning) as an anti-predator behaviour.

ABSTRACT: Thanatosis-also known as death-feigning and, we argue more appropriately, tonic immobility (TI)-is an under-reported but fascinating anti-predator strategy adopted by diverse prey late on in the predation sequence, and frequently following physical contact by the predator. TI is thought to inhibit further attack by predators and reduce the perceived need of the predator to subdue prey further. The behaviour is probably present in more taxa than is currently described, but even within well-studied groups the precise taxonomic distribution is unclear for a number of practical and ethical reasons. Here we synthesise the key studies investigating the form, function, evolutionary and ecological costs and benefits of TI. This review also considers the potential evolutionary influence of certain predator types in the development of the strategy in prey, and the other non-defensive contexts in which TI has been suggested to occur. We believe that there is a need for TI to be better appreciated in the scientific literature and outline potentially profitable avenues for investigation. Future use of technology in the wild should yield useful developments for this field of study. SIGNIFICANCE STATEMENT: Anti-predatory defences are crucial to many aspects of behavioural ecology. Thanatosis (often called death-feigning) has long been an under-appreciated defence, despite being taxonomically and ecologically widespread. We begin by providing much-needed clarification on both terminology and definition. We demonstrate how apparently disparate observations in the recent literature can be synthesised through placing the behaviour within a cost-benefit framework in comparison to alternative behavioural choices, and how aspects of the ecology differentially affect costs and benefits. Extending this, we provide novel insights into why the evolution of thanatosis can be understood in terms of coevolution between predators and prey. We offer further novel hypotheses, and discuss how these can be tested, focussing on how emerging technologies can be of great use in developing our understanding of thanatosis in free-living animals.