Hereditary nature of death-feigning frequency in a parasitoid wasp Heterospilus prosopidis using sib analysis.

Death feigning, a state of immobility observed in many animals in response to external stimuli, is an anti-predator behaviour. Although previous studies showed that death-feigning behaviours are quantitative genetic traits, the knowledge of the heritable basis of death-feigning behaviour is lacking. To investigate the heritable basis of death-feigning behaviour, we used 3 laboratory strains of a braconid parasitoid wasp, Heterospilus prosopidis. The heritable basis using half-sib analysis, and the effects of different geographical backgrounds, rearing conditions in the laboratory, and host age were evaluated. The results of the half-sib analysis showed that the frequency of death feigning varied among sires, suggesting a certain extent of additive genetic variance. Also, the frequency of death feigning varied between geographical backgrounds and among strains. Death-feigning frequency was not affected by the age of the host. Our findings highlight the importance of genetic factors underlying the basis of the death-feigning behaviour and provide support for the genetic alterations of traits from the perspective of evolution in various animal species.

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.

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.

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.

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.

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.

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.

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.

The influence of mitonuclear genetic variation on personality in seed beetles.

There is a growing awareness of the influence of mitochondrial genetic variation on life-history phenotypes, particularly via epistatic interactions with nuclear genes. Owing to their direct effect on traits such as metabolic and growth rates, mitonuclear interactions may also affect variation in behavioural types or personalities (i.e. behavioural variation that is consistent within individuals, but differs among individuals). However, this possibility is largely unexplored. We used mitonuclear introgression lines, where three mitochondrial genomes were introgressed into three nuclear genetic backgrounds, to disentangle genetic effects on behavioural variation in a seed beetle. We found within-individual consistency in a suite of activity-related behaviours, providing evidence for variation in personality. Composite measures of overall activity of individuals in behavioural assays were influenced by both nuclear genetic variation and by the interaction between nuclear and mitochondrial genomes. More importantly, the degree of expression of behavioural and life-history phenotypes was correlated and mitonuclear genetic variation affected expression of these concerted phenotypes. These results show that mitonuclear genetic variation affects both behavioural and life-history traits, and they provide novel insights into the maintenance of genetic variation in behaviour and personality.

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.

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.

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.

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.

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.

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.

On the Adult Behavioral Repertoire of the Sawfly Perreyia flavipes Konow, 1899 (Hymenoptera: Pergidae): Movement, Mating, and Thanatosis.

Perreyia flavipes Konow, 1899 (Pergidae: Perreyinae) is a sawfly species with gregarious larvae commonly found in open areas in southern Brazil through Uruguay and northern Argentina. The combination of highly gregarious larvae with the production of a variety of toxins in P. flavipes has led to severe cases of intoxication in a variety of livestock species. Over the years, considerable information was discovered on the larval natural history of P. flavipes; however, virtually nothing is known about the adult behavior, particularly because of its short life-span. In this study, we report on the first extensive study on the adult behavior of P. flavipes, including movement, mating (with oviposition and maternal care), and thanatosis. Our results show some unusual behavioral adaptations presented by P. flavipes, such as irregular activity behavior (i.e., deficient gait pattern), thanatosis behavior-like display, and primitive maternal care. Individual behavioral acts are described and compared among sexes, and their potential functions are discussed.

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.