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Intrinsic and Extrinsic Factors Influence Expression of Defensive Behavior in Plains Hog-Nosed Snakes (Heterodon nasicus)

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Abstract

Animals failing to deter predation are eaten. Among the many deterrents to predation, antipredator behaviors are perhaps the most variable, ranging from active (fight or flight) to passive (immobility). We assessed variation in the expression of a passive defensive behavior, death-feigning, in Plains Hog-nosed Snakes (Heterodon nasicus) and predicted that intrinsic and extrinsic factors would influence the duration of this behavior and the latency to its onset. We simulated predatory attacks on 27 snakes encountered in the field, and analyzed the behavioral responses of snakes as a function of differences among individuals (sex and size) and environmental factors (temperature and microhabitat). Larger snakes death-feigned for longer durations than smaller ones; this relationship was stronger for female snakes than for males. Death feints were initiated sooner when snakes were encountered at higher temperatures. Extrinsic factors had a greater influence on latency to death-feigning behavior, whereas intrinsic factors more strongly influenced its duration. Because our results involved wild snakes, they provide an improved, highly relevant understanding of individual and environmental factors that regulate the expression of immobile defensive behavior. Furthermore, additional hypotheses can now be proposed that address the evolution of defensive behaviors that leave animals prone to attack.

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... We searched for snakes in the morning by walking 1.85km transects surveyed by 4 to 7 people, and all snakes were marked so that recaptures could be identified and pseudo-replication by individual avoided (details in Thol 2008;Durso and Mullin 2014). Sex was determined by probing, although we verified the sex of nine juveniles based on ratios of tail length to snout-vent length (SVL; Supplemental Fig. S1). ...
... In addition to an incomplete understanding of eDNA degradation rates, another challenge in using fecal eDNA for diet studies is collecting uncontaminated fecal samples in the field. Like many snakes, Heterodon tend to defecate when captured, and there might be some adaptive function to fecal retention beyond the point when additional water and nutrients can be absorbed (Lillywhite et al. 2002), especially when it is used as part of stereotyped defensive displays (Durso and Mullin 2014). More targeted collection of feces (e.g., holding each individual in a clean container until it defecated) would have increased sample size and decreased contamination, particularly with human DNA, but was incompatible with other study goals (Durso and Mullin 2014). ...
... Like many snakes, Heterodon tend to defecate when captured, and there might be some adaptive function to fecal retention beyond the point when additional water and nutrients can be absorbed (Lillywhite et al. 2002), especially when it is used as part of stereotyped defensive displays (Durso and Mullin 2014). More targeted collection of feces (e.g., holding each individual in a clean container until it defecated) would have increased sample size and decreased contamination, particularly with human DNA, but was incompatible with other study goals (Durso and Mullin 2014). In addition, these fecal samples were stored at À808C for several years before DNA was extracted, so this technique would likely have been more sensitive if DNA was extracted immediately (Barnes et al. 2014). ...
... When detected visually or physically disturbed by a predator or other antagonist, a wide range of vertebrates and invertebrates employ a complex behavioural tactic known as death feigning, or thanatosis (Rogers and Simpson, 2014;Humphreys and Ruxton, 2018;Cardoso and Mendonça, 2019), considered by some researchers to be a category of tonic immobility (Humphreys and Ruxton, 2018). In snakes, death feigning can be influenced by body size, sex, and temperature (Mutoh, 1983;Gerald, 2008;Gregory, 2008;Durso and Mullin, 2014). This antipredator mechanism appears to occur more often in snakes with small body sizes, such as hatchlings or juveniles (Gerald, 2008), in females than in males (Durso and Mullin, 2014), or when ambient temperature conditions are unfavourable for escape movements (Mutoh, 1983;Gregory, 2008). ...
... In snakes, death feigning can be influenced by body size, sex, and temperature (Mutoh, 1983;Gerald, 2008;Gregory, 2008;Durso and Mullin, 2014). This antipredator mechanism appears to occur more often in snakes with small body sizes, such as hatchlings or juveniles (Gerald, 2008), in females than in males (Durso and Mullin, 2014), or when ambient temperature conditions are unfavourable for escape movements (Mutoh, 1983;Gregory, 2008). The execution and duration of this antipredator mechanism are also determined by the snake species' ability to visually and chemically receive and interpret various signals, such as type of predator, escape opportunities, and distance and direction of the predator (Burghardt and Greene, 1988;Durso and Mullin, 2014). ...
... This antipredator mechanism appears to occur more often in snakes with small body sizes, such as hatchlings or juveniles (Gerald, 2008), in females than in males (Durso and Mullin, 2014), or when ambient temperature conditions are unfavourable for escape movements (Mutoh, 1983;Gregory, 2008). The execution and duration of this antipredator mechanism are also determined by the snake species' ability to visually and chemically receive and interpret various signals, such as type of predator, escape opportunities, and distance and direction of the predator (Burghardt and Greene, 1988;Durso and Mullin, 2014). ...
... Like many ectotherms, locomotion and defensive responses in S. dekayi are infl uenced by environmental temperatures (Keogh and DeSerto 1994;Gerald and Claussen 2007); sex, microhabitat, and a snake's prior activity may also be important factors infl uencing defensive responses in snakes (Shine et al. 2000). Due to the complex interaction between these, and possibly other variables, the majority of studies regarding defensive behaviors in snakes are carried out in the laboratory (Durso and Mullin 2014). ...
... Herzog and Burghardt (1986) demonstrated signifi cant differences among three species of Thamnophis in the defensive behaviors directed towards a threatening stimulus (i. e., a human fi nger), with T. melanogaster being the most reactive. Durso and Mullin (2014) demonstrated that both intrinsic (sex, size) and extrinsic (temperature) factors infl uenced the death-feigning behavior of Plains Hog-nosed Snakes (Heterodon nasicus), and it is likely that a combination of these factors infl uence the defensive behaviors of S. dekayi also. Snakes may also react differently to human interaction than they would when encountering one of their natural predators (Greene 1997). ...
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The defensive behaviors of free-ranging Dekay's Brownsnakes, Storeria dekayi, were studied at a site in Erie County, Pennsylvania, USA. Twenty-nine unique sequences of defensive behavior were documented. A total of 50 individual snakes (26 males and 24 females) provided 88 observations during the initial phase, of which 78% (n = 69) were of snakes that remained in place. Snakes were tapped with the investigator's hand to elicit defensive behaviors during the contact phase. Snakes were more than twice as likely to attempt to flee during the contact phase (46%) than during the initial phase (22%). During the contact phase, mean surface body temperatures were significantly higher in snakes attempting to flee (22.3 ± 1.3 °C) than those that remained in place (16.1 ± 2.2 °C). The most frequently observed response during the contact phase was dorso-ventral flattening of the head and body (n = 42). During capture, most snakes (94%) smeared their cloacal contents on themselves and the investigator's hand. Natural History Museum at the Tom Ridge
... Which defense is selected depends on the kind of threatening stimuli as well as a complex of external and internal factors, such as the substrate on which the snake is situated or the snake's body temperature. The flexibility and context-dependence of the anti-predator responses is supported by experimental research, such as experiments with Australian elapids (Llewelyn et al., 2010) and Hog-nosed Snakes (Durso and Mullin, 2014) and other studies of reptiles (Hertz et al., 1982;Shine et al., 2000;Burghardt, 2001, 2004). The relative infrequency in which (full blown) BBB has been observed, compared to other defensive strategies, suggest that it might only be used in particular combinations of a few conditions. ...
... Which defense is selected when threatened, depends on the kind of threatening stimuli as well as a complex of external and internal factors, such as the substrate on which the snake is situated or the snake's body temperature. The flexibility and context-dependence of the anti-predator responses is supported by experimental research, such as experiments with Australian elapids (Llewelyn et al., 2010) and Hognosed Snakes (Durso and Mullin, 2014) and other studies of reptiles (Hertz et al., 1982;Shine et al., 2000;Burghardt, 2001, 2004). The relative low frequency in which full blown BBB occurs upon a threat, suggests that it may only be displayed in particular combinations of a few conditions. ...
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Hitherto, body bending behavior (BBB) has been reported for less than a dozen of different snake species from tropical and subtropical America. Most authors assume that this rarely documented behavior is cryptic and antipredator, e.g., by taking the form of a liana the snake may avoid being attacked by a potential predator. We herein report the first records of this behavior in snakes in Asia and Europe. A dozen cases of body bending are documented for the colubrids Coelognathus radiatus (Boie, 1827), Ptyas carinata (Günther, 1858) and Oligodon joynsoni (Smith, 1917), and Malpolon monspessulanus (Hermann, 1804), and the natricids Fowlea piscator (Schneider, 1799) and Rhabdophis siamensis (Mell, 1931). In addition to the earlier reports from the New World, we suggest that BBB is widespread in snakes throughout the tropical and subtropical world. For a number of species that display it relatively frequently, such as C. radiatus in Thailand, BBB may have a significant adaptive value. We propose that this behavior is basically a kind of defensive immobility response that may develop swiftly or rather slowly and which is most often associated with diurnal activity, open spaces and an inclination to aggressive defenses. Our data suggest that its function is more often aposematic than cryptic.
... However, for species known to feign death, there is often intraspecific variation in the expression of death feigning as well as the duration of immobility. This variation has been shown to be genetically determined across disparate taxa (Prohammer and Wade 1981;Miyatake et al. 2004;Nakayama and Miyatake 2009;Nakayama et al. 2010;van den Brink et al. 2012), and can be correlated to body size (Hozumi and Miyatake 2005;Gerald 2008;Quadros et al. 2012;Durso and Mullin 2014), sex (Miyatake 2001a, b;Bilde et al. 2006;Miyatake et al. 2008;Kuriwada et al. 2009), age (Cassill et al. 2008;van den Brink et al. 2012), measures of physiological performance (King and Leaich 2006;Ohno and Miyatake 2007;Gerald 2008;Nakayama and Miyatake 2009;Kiyotake et al. 2014), or environmental variables such as temperature (Holmes 1902;Gerald 2008;Miyatake et al. 2008). However, despite a wealth of research, there is little consensus on the effects of most variables, with contrasting patterns shown for different taxa. ...
... All individuals are bright green and will contrast with the dirt, but smaller individuals might be more likely to escape detection by a ground foraging predator than larger individuals. While this strategy would seem to be plausible for disparate insect species, tests of age effects of the likelihood and duration of thanatosis typically demonstrate no patterns (Acheampong and Mitchell 1997;King and Leaich 2006; but see Cassill et al. 2008), and many relationships with body size show positive correlations with death feigning (Hozumi and Miyatake 2005; but see Quadros et al. 2012;Durso and Mullin 2014). A major difference between the present study and past studies of body size, however, is that T. cristinae exhibits incomplete metamorphosis, whereas other studies (e.g., Hozumi and Miyatake 2005) use insects with complete metamorphosis, so that these studies, while focusing on age and body size, are not focusing on ontogeny through developmental stages. ...
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Eco-evolutionary feedback loops, where rapid evolution influences the ecology of an organism and subsequently alters the evolutionary trajectory of the population, are intriguing possibilities, but evidence for or against them is scarce. Timema cristinae stick insects express variation within and among populations in the expression of death-feigning behaviour, but the causes of variation in this species is not known. Here, I test the hypothesis that variation in death feigning across populations stems from an eco-evolutionary feedback loop, whereby gene flow causes poor camouflage, which increases the strength of bird predation, and ultimately drives the evolution of increased death-feigning. By conducting behavioural trials on eight T. cristinae populations that differ in the degree of maladaptive gene flow incurred, I falsify the eco-evolutionary feedback hypothesis for the evolution of death-feigning. Instead, I show that smaller individuals are more likely to feign death than larger individuals. By rearing individuals in the lab, I offer suggestive evidence that the body size effect is explained by the age of wild-caught individuals: younger individuals feign death more than older individuals. These findings add an example to the literature where no eco-evolutionary feedback exists in a system for which other similar feedbacks have been found, and provide evidence that death-feigning behaviour depends on body size.
... Many species of bufophagous (i.e. toad-eating) snakes also death feign in response to an attack [64,[167][168][169]. The behaviour is not exclusive to bufophagous snakes, and at least one species of highly bufophagous snake (Causus rhombeatus) does not feign death [170]. ...
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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.
... In addition, Scudder and Burghardt (1983) found that male banded water snakes responded more aggressively to predator stimulation than females. Likewise, Durso and Mullin (2014) found that in plains hog-nosed snakes, larger snakes death-feigned for a longer period of time than smaller ones, and that this relationship was stronger in females. Thus, it seems plausible that sex and body size play an important role in predicting an individual's behaviour. ...
Article
Phenotypic traits are important to consider when examining behaviour because they can help explain behavioural trait variation. Behaviours such as exploration, boldness, and defense may vary between individuals because different intensities of a behaviour may be advantageous for males versus females, or at different body sizes. We tested the hypothesis that exploration, boldness, and defensive behaviours are related to body size, sex, and reproductive status in eastern garter snakes, Thamnophis sirtalis. We also tested whether the measured behavioural traits were consistent through time (i.e., whether eastern garter snakes could have personalities) and whether the measured behavioural traits were related to one another (i.e., whether behavioural syndromes could be present in eastern garter snakes). Males and non-gravid females were more likely to flee than gravid females when faced with an attack. Males and non-gravid females were also more active after the attack than before the attack, whereas gravid females were more active before the attack. Furthermore, longer females explored less than smaller females, with a more precipitous decline of exploration as a function of size in gravid females than in non-gravid females. In contrast, longer males explored more than smaller males. Although we did not detect behavioural syndromes, within individuals the measured behavioural traits were repeatable through time, suggesting that eastern garter snakes could have personalities.
... An alteration in tissue-specific expression of this nature would likely compromise muscle performance to some degree, because the natively expressed Na v 1.4 allows rapid, large amplitude changes in membrane potential compared with other channels (Geffeney and Rubin, 2006), allowing quick and intense muscular contractions. However, hog-nosed snakes are stout-bodied predators that rely on defensive displays rather than speed to avoid enemies (Durso and Mullin, 2014) and thus might tolerate some compromise in muscle function. Finally, an intriguing possibility is that H. platirhinos circumvent TTX not by possessing resistant sodium channels (targets of TTX) but by 'grabbing' TTX before the poison reaches sensitive tissues. ...
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Convergent evolution of tetrodotoxin (TTX) resistance, at both the phenotypic and genetic levels, characterizes coevolutionary arms races between amphibians and their snake predators around the world, and reveals remarkable predictability in the process of adaptation. Here we examine the repeatability of the evolution of TTX resistance in an undescribed predator–prey relationship between TTX-bearing Eastern Newts (Notophthalmus viridescens) and Eastern Hog-nosed Snakes (Heterodon platirhinos). We found that that local newts contain levels of TTX dangerous enough to dissuade most predators, and that Eastern Hog-nosed Snakes within newt range are highly resistant to TTX. In fact, these populations of Eastern Hog-nosed Snakes are so resistant to TTX that the potential for current reciprocal selection might be limited. Unlike all other cases of TTX resistance in vertebrates, H. platirhinos lacks the adaptive amino acid substitutions in the skeletal muscle sodium channel that reduce TTX binding, suggesting that physiological resistance in Eastern Hog-nosed Snakes is conferred by an alternate genetic mechanism. Thus, phenotypic convergence in this case is not due to parallel molecular evolution, indicating that there may be more than one way for this adaptation to arise, even among closely related species.
... Previous studies have also found that individual-level characteristics influence behavioral responses to both predation threats and actual predatory encounters (e.g., Bulova 1994). These characteristics may include the morphological or physiological condition of an individual, including color pattern (Brodie 1992), body size (Roth and Johnson 2004;Herrel et al. 2009), age (Cuadrado et al. 2001;Hopkins et al. 2011), sex (Durso and Mullin 2013), or reproductive condition (Goode and Duvall 1989). Among ectotherms, body temperature has a strong influence on defensive behaviors such as jumping performance or crawling speed (Hertz et al. 1982;Peterson et al. 1993;Gomes et al. 2002) because ectotherm physiological processes are closely coupled to body temperature (Lillywhite 1987). ...
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The ability to display multiple defensive behaviors may increase the chances of an individual avoiding predation. Morphological and physiological condition often influences the display of particular behaviors. Understanding the factors influencing the display of particular behaviors from a suite of potential behaviors can help understand the conditions under which displaying certain suites of defensive behaviors will confer the greatest advantage. Drymarchon couperi (Eastern Indigo Snake) is a large, non-venomous snake that exhibits multiple visual, auditory, olfactory, and physical defensive behaviors. We studied the responses of wild D. couperi to human capture and examined how the number and presence of individual behaviors were related to extrinsic and intrinsic variables using encounters from 84 snakes. Snakes were more likely to flee from the observer at warmer body temperatures and, once captured, exhibited wide variation in defensive behaviors with less costly (i.e., less aggressive) behaviors predominating. Individuals were more likely to display any type of defensive behavior earlier in the field season (i.e., November through January). However, our variables had relatively little influence on the presence of particular defensive behaviors although, for some behaviors, the probability of displaying a behavior increased as the number of other behaviors exhibited increased. Our study shows that D. couperi defensive behavior is quite variable and that the factors contributing variation are unclear. Environmental factors (e.g., distance to retreat site) or individual predispositions may contribute to some of this variation.
... Many factors might influence the choice and intensity of the elected antipredatory tactic, such as local conditions [i.e. environmental temperature, amount of light/period of day and vegetation cover/ terrain characteristics (Savino and Stein, 1989;Christensen and Persson, 1993;Brodie and Russell, 1999;Shine et al., 2000Shine et al., , 2003Schulte et al., 2004;Durso and Mullin, 2014)] or type and density of predators or their form of attack (Greene, 1988;Langkilde et al., 2004;Relyea, 2001;Seyfarth et al., 1980). The anti-predatory response is still dependent on the condition of the prey, for example, on its stage in the reproductive cycle, nutritional status (Brown and Shine, 2004;Burger et al., 1989;Shine et al., 2000) or its phenotypic characteristics. ...
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Anti-predatory behaviour evolves under strong action of natural selection because the success of individuals avoiding predation essentially defines their fitness. Choice of anti-predatory strategies is defined by prey characteristics as well as environmental temperature. An additional dimension often relegated in this multilevel equation is the ontogenetic component. In tegus Salvator merianae, adults run away from predators at high temperatures but prefer fighting when it is cold, while juveniles exhibit the same flight strategy within a wide thermal range. Here we integrate physiology and morphology to understand ontogenetic variation in the temperature-dependent shift of anti-predatory behaviour in these lizards. We compiled data for body shape and size and quantified enzyme activities in hindlimb and head muscles, testing the hypothesis that morpho-physiological models explain ontogenetic variation in behavioural associations. Our prediction is that juveniles exhibit body shape and muscle biochemistry that enhance flight strategies. We identified biochemical differences between muscles residing mostly on the LDH: CS ratio, being hindlimb muscles more glycolytic than jaw musculature. Juveniles, which often use evasive strategies to avoid predation, have more glycolytic hindlimb muscles and are much smaller when compared to adults being 1-2 years old. Ontogenetic differences in body shape were identified but marginally contributed for behavioural variation between juvenile and adult tegus, and variation in anti-predatory behaviour in these lizards reside mainly on associations integrating body size and muscle biochemistry. Our results are discussed in the ecological context of predator avoidance by individuals differing in body size living at temperature-variable environments, where restrictions imposed by the cold seem compensated in specific phenotypes.
... We also collected gut contents from the relatively few snakes that had them (N = 13; 13.5% of captures). Durso and Mullin (2014) reported additional sampling details. Table 1 Mean ± one standard error of morphometrics and stable isotope ratios for blood plasma, red blood cells and scale carbon (␦ 13 C) and nitrogen (␦ 15 N) of 54 plains hog-nosed snakes (Heterodon nasicus) from the Mean ± one standard error of stable isotope ratios of carbon (␦ 13 C) and nitrogen (␦ 15 N) of five tissue types collected from 186 prey items in seven categories from Thomson Sand Prairie (Carroll Co., Illinois) in 2010 and 2011. ...
... Malpolon monspessulanus is not included in this table because Sanolo et al. (2014) only mention that this snake remained flaccid and in an apparent death condition. Tabla 1: Comparación de la respuesta encontrada en C. girondica con otras especies de ofidios europeas (datos extraídos de Gregory et al., 2007;Gregory, 2008;Jelic & Vilaj, 2011;Iftime & Iftime, 2014) that influence the expression of defensive behaviour (Durso & Mullin, 2013) and to be able to extract the phylogenetic inertia that could be present in the evolution of the feigned death behaviour. ...
Article
Thanatosis or death feigning is a defence behaviour that has already been described previously in many species. This is the first record of thanatosis behaviour in the snake Coronella girondica. This case has been occurred in the Natural Park of the Sierras de Cazorla, Segura and Las Villas, in the southern Spain.
... An alteration in tissue-specific expression of this nature would likely compromise muscle performance to some degree, because the natively expressed Na v 1.4 allows rapid, large amplitude changes in membrane potential compared with other channels (Geffeney and Rubin, 2006), allowing quick and intense muscular contractions. However, hog-nosed snakes are stout-bodied predators that rely on defensive displays rather than speed to avoid enemies (Durso and Mullin, 2014) and thus might tolerate some compromise in muscle function. Finally, an intriguing possibility is that H. platirhinos circumvent TTX not by possessing resistant sodium channels (targets of TTX) but by 'grabbing' TTX before the poison reaches sensitive tissues. ...
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An official journal of the Genetics Society, Heredity publishes high-quality articles describing original research and theoretical insights in all areas of genetics. Research papers are complimented by News & Commentary articles and reviews, keeping researchers and students abreast of hot topics in the field.
... Regarding the other behaviours exhibited by Trilepida jani mentioned above, those are widespread among other scolecophidian snakes and terrestrial (mostly) alethinophidian species (Martins, 1996;Martins et al., 2008). Despite its importance for survival, effects of extrinsic and intrinsic factors on individual defensive behaviour have been neglected in most snakes and thus demand additional attention (Marques et al., 2013;Durso and Mullin, 2014). This study contributes by providing data on the biology of leptotyphlopid species, and further studies on other species of Leptotyphlopidae are recommended. ...
... When approached by a predator, animals use a variety of responses to avoid capture or evade detection. These include, but are not limited to, crypsis (Donnelly and Dill 1984;Broom and Ruxton 2005;Caro 2005; Barbosa et al. 2012), tonic immobility or death feigning (Hoagland 1928;Ewell et al. 1981;Arduino and Gould 1984;Miyatake et al. 2004;Gregory et al. 2007;Durso and Mullin 2013), flight (Hertz et al. 1982;Cooper and Frederick 2007), warning calls (Seyfarth et al. 1980;Magrath et al. 2007;Natale et al. 2010), defensive or distractive displays (Brodie and Gibson Communicated by C. R. Gabor 1969;Greene 1988;Caro 2005;Hossie and Sherratt 2013), discharge of foul or toxic compounds (Toledo and Jared 1995;Williams et al. 2000;Hopkins and Migabo 2010;Medill et al. 2011;Toledo et al. 2011;Mailho-Fontana et al. 2014) and combat (Caro 2005;Emlen 2008;Stankowich 2010). ...
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A potential prey item’s response to encountering a predator depends on aspects of the predator (e.g., its locomotor capacity), the local environment (e.g., proximity to shelter) and the physiological state of the prey item, but in addition, anti-predator tactics also vary geographically among different populations within wide-ranging species. Using standardised trials, we tested responses of cane toads (Rhinella marina) to being placed on a laboratory runway and encouraged to flee. Overall, the toads least capable of rapid locomotion were the ones most likely to respond to simulated predator attack by exuding toxins rather than attempting to escape. A toad’s willingness to move down the runway and its propensity to exude toxin from the parotoid glands rather than fleeing were repeatable in successive trials and influenced by the animal’s location of origin, morphology, previous experience, and parentage. We found that specimens from Australia were more willing to flee than were those from the native range (French Guiana) or Hawai’i; larger toads, and those with relatively longer legs, were more willing to flee; captive-raised toads were less willing to flee and more willing to exude toxin. Captive-raised offspring resembled their wild-caught parents both in propensity to run and in propensity to exude toxin. Thus, geographic divergence among cane toad populations in anti-predator responses reflects a complex combination of processes, including both developmental plasticity and heritability. Significance statement The process of colonising novel environments exposes an organism to a host of different predators that exert selection on morphology, behaviour and physiology. Over time, this can lead to the evolution of novel phenotypes that are adapted to local conditions. Anthropogenically facilitated biological invasions provide a unique opportunity to study how species respond to colonisation of new environments. Here, we studied geographic variation in cane toad (Rhinella marina) anti-predator behaviours from a range of locations (including invasive and native populations) using standardised trials. Our results suggest that invasive Australian cane toads have undergone a shift in their anti-predator response, becoming more willing to flee than are conspecifics from other areas. Location of origin, morphology, prior experience and parentage all played a role in shaping a toad’s anti-predator response, suggesting that the behaviour represents a combination of plastic and heritable variation.
... Thanatosis has been observed in a great diversity of snakes, including colubrids, natricids, dipsadids, and elapids (Gerald, 2008;Mirza et al., 2011;Bhosale and Thite, 2013;Marques et al., 2013;Sannolo at al., 2014). However, thanatosis is rarely reported among dipsadids (Marques et al., 2013;Durso and Mullin, 2014;Muscat et al., 2016). A number of different hypotheses have been suggested to explain the exact function of this behaviour, such as the loss of interest of predators specializing in live prey (Rovee et al., 1976) or enhanced escape opportunity (Ratner and Thompson, 1960;Rovee et al., 1976). ...
... However, thanatosis has been previously documented in other members of the genus (Muscat et al. 2016). Thanatosis may be used as a terminal defense or "last resort" by prey that have been detected or seized by a predator (Thompson et al. 1981;Miyatake et al. 2004;Gregory 2008) and may vary with sex, body size/age, or environmental factors (Gregory & Gregory 2006;Gerald 2008;Durso & Mullin 2014). ...
... This result is surprising at first sight, may be explained if we interpret handling aggression as an anti-predator response. When attacked by a predator, individuals can vary in their reactions towards predators, can show a fight, a flight or a freeze response (Lingle & Pellis 2002, Durso & Mullin 2014. Anti-predator responses depend on intrinsic and extrinsic factors (Lingle & Pellis 2002). ...
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Les environnements insulaires, discontinus et généralement plus simples que les systèmes océaniques ou continentaux, ont permis le développement et la mise en place de plusieurs théories en écologie. Ainsi, les études en biogéographie sont devenues de plus en plus précises quant à l'étude des dynamiques insulaires, multipliant les facteurs explicatifs, jusqu'à tenir compte des variations interindividuelles au sein des populations. L‘hypothèse du syndrome insulaire avance ainsi l‘idée que le phénotype des individus vivants sur les îles diffère de celui des individus continentaux, et ce à cause de plusieurs caractéristiques écologiques spécifiques aux îles. Cependant, les résultats des études empiriques ayant testées les prédictions du syndrome insulaire n‘offrent pas de consensus sur la validité ou non du syndrome. Cela est très probablement dû au fait que premièrement peu d‘études prennent en compte les différents niveaux d‘organisation biologiques de manière simultanée et ensuite parce que l‘hypothèse du syndrome insulaire est basée sur un modèle verbal déductif, offrant un pouvoir prédictif limité. Le but de ce doctorat est de mesurer les changements phénotypiques des individus vivant au sein d‘un paysage fragmenté et d‘étudier les causes de ces éventuels changements. Cela à partir de mesures phénotypiques effectuées sur deux espèces de petits mammifères : la souris sylvestre (Peromyscus maniculatus) et le campagnol à dos roux de Gapper (Myodes gapperi), ainsi que des relevés des caractéristiques du paysage, des communautés et des populations au sein d‘un milieu naturellement fragmenté. Chez les souris, nous avons montré que le phénotype des individus était largement affecté par la vie sur les îles, en comparaison des individus continentaux. Ainsi les individus vivant sur les îles étaient moins agressifs envers de potentiels prédateurs, ils étaient des explorateurs plus minutieux, les mâles étaient plus lourds et les juvéniles avaient des queues plus longues. En revanche les campagnols ne semblaient quasiment pas affectés par la vie insulaire. Nous avons également mis en évidence l‘impact de la surface, de l‘isolement et de la connectivité des parcelles sur ces traits phénotypiques chez la souris sylvestre. Dans un second temps nous avons mis en évidence chez la souris sylvestre que les individus disperseurs avaient un phénotype différent des individus résidents lorsqu‘il s‘agissait de jeunes adultes. Nous avons également montré que les parcelles d‘émigrations et d‘immigrations avaient des caractéristiques particulières. Enfin nous avons mis en évidence, pour les souris, que les caractéristiques du paysage (c.-à-d. surface et isolement des parcelles) avaient des impacts sur certaines dimensions des communautés, qui affectaient à leur tour les caractéristiques des populations. En revanche, les populations de campagnols étaient très peu affectées. Finalement nous avons démontré que ces changements liés à l‘insularité des parcelles étaient en partie responsables des modifications phénotypiques précédemment trouvées chez les souris sylvestre. Ce doctorat a permis de mettre en évidence la complexité des liens entre les différents niveaux d‘organisation biologique : du paysage jusqu‘au phénotype des individus. Il a également permis de valider certaines prédictions du syndrome insulaire mais d‘autres prédictions ont été infirmées dans notre aire d‘étude. Ce travail de doctorat a ainsi pu appréhender les causes écologiques responsables du maintien de la variabilité comportementale interindividuelle au sein d‘un paysage naturellement fragmenté.
... Death-feigning, death feint (Peters, 1964) or thanatosis is well-known in snakes with the North American Hognose Snakes being perhaps the best known example. Examples of deathfeigning in snakes elsewhere than in Africa are reported in several papers (e.g., Durso & Mullin, 2013;Fernández-Guiberteau & Carrero, 2016;Gehlbach, 1970;Gregory, 2008;Gregory, Isaac, & Griffiths. 2007;Iftime & Iftime, 2014;Jelic & Vilaj, 2011;Kreiner, 2007;Sannolo, et al. 2014). ...
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This short account details the first photographic evidence of death-feigning in a juvenile Naja mossambica Peters, 1854 (Naja (Afronaja) mossambica Peters, 1854) from KwaZulu-Natal, South Africa, accompanied by figures displaying threat posture and death-feigning. Records of this behaviour in other species, including photographs, are considered and referenced.
... Konrad meBert & Andrew M. durso Summary Predation and defense behavior in reptiles can take many forms (Vitt & Caldwell 2009) and its outcome depends on the interaction between predator and prey, as well as on intrinsic and extrinsic factors (Durso & Mullin 2013). These can include the arrival of secondary predators, which are sometimes attracted by the commotion caused by the initial predation event (e.g., Hödl & Gollman 1986, De Toledo et al. 2009). ...
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The ability of prey to escape predation often lies in the occurrence and efficacy of their predator avoidance and antipredator behaviors, which are often coupled with specialized morphology. How the use and efficacy of these behaviors change throughout ontogeny may be indicative of the vulnerability and ecological roles these animals experience throughout their lives. We examined the antipredator behavior of a large dragonfly nymph, Anax junius, from a historically fishless pond where these animals have traditionally been classified as top predators. These dragonfly nymphs displayed a series of distinct aggressive antipredator behaviors when grasped that involved stabbing with lateral and posterior spines and seizing with labial hooks. Larger (older) nymphs displayed these aggressive behaviors significantly more than smaller (younger) animals in simulated predation trials. During encounters with live larval salamander predators (Ambystoma tigrinum), all large nymphs, but only 12.5% of small nymphs successfully escaped predation attempts by the amphibians through the use of antipredator behavior. Large nymphs were also significantly more active than smaller nymphs in the presence of salamander larvae. Despite often being considered top predators in fishless ponds, our study demonstrates that their true role is more complex, depending on ontogeny and body size, and that effective antipredator behavior is likely necessary for survival in these systems.
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Species that sequester toxins from prey for their own defense against predators may exhibit population-level variation in their chemical arsenal that reflects the availability of chemically defended prey in their habitat. Rhabdophis tigrinus is an Asian snake that possesses defensive glands in the skin of its neck ('nuchal glands'), which typically contain toxic bufadienolide steroids that the snakes sequester from consumed toads. In this study, we compared the chemistry of the nuchal gland fluid of R. tigrinus from toad-rich and toad-free islands in Japan and determined the effect of diet on the nuchal gland constituents. Our findings demonstrate that captive-hatched juveniles from toad-rich Ishima Island that had not been fed toads possess defensive bufadienolides in their nuchal glands, presumably due to maternal provisioning of these sequestered compounds. Wild-caught juveniles from Ishima possess large quantities of bufadienolides, which could result from a combination of maternal provisioning and sequestration of these defensive compounds from consumed toads. Interestingly, juvenile females from Ishima possess larger quantities of bufadienolides than do juvenile males, whereas a small sample of field-collected snakes suggests that adult males contain larger quantities of bufadienolides than do adult females. Captive-born hatchlings from Kinkasan Island lack bufadienolides in their nuchal glands, reflecting the absence of toads on that island, but they can sequester bufadienolides by feeding on toads (Bufo japonicus) in captivity. The presence of large quantities of bufadienolides in the nuchal glands of R. tigrinus from Ishima may reduce the risk of predation by providing an effective chemical defense, whereas snakes on Kinkasan may experience increased predation due to the lack of defensive compounds in their nuchal glands.
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Chemical defenses are widespread among animals, and the compounds involved may be either synthesized from nontoxic precursors or sequestered from an environmental source. Defensive sequestration has been studied extensively among invertebrates, but relatively few examples have been documented among vertebrates. Nonetheless, the number of described cases of defensive sequestration in tetrapod vertebrates has increased recently and includes diverse lineages of amphibians and reptiles (including birds). The best-known examples involve poison frogs, but other examples include natricine snakes that sequester toxins from amphibians and two genera of insectivorous birds. Commonalities among these diverse taxa include the combination of consuming toxic prey and exhibiting some form of passive defense, such as aposematism, mimicry, or presumptive death-feigning. Some species exhibit passive sequestration, in which dietary toxins simply require an extended period of time to clear from the tissues, whereas other taxa exhibit morphological or physiological specializations that enhance the uptake, storage, and/or delivery of exogenous toxins. It remains uncertain whether any sequestered toxins of tetrapods bioaccumulate across multiple trophic levels, but multitrophic accumulation seems especially likely in cases involving consumption of phytophagous or mycophagous invertebrates and perhaps consumption of poison frogs by snakes. We predict that additional examples of defensive toxin sequestration in amphibians and reptiles will be revealed by collaborations between field biologists and natural product chemists. Candidates for future investigation include specialized predators on mites, social insects, slugs, and toxic amphibians. Comprehensive studies of the ecological, evolutionary, behavioral, and regulatory aspects of sequestration will require teams of ecologists, systematists, ethologists, physiologists, molecular biologists, and chemists. The widespread occurrence of sequestered defenses has important implications for the ecology, evolution, and conservation of amphibians and reptiles.
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Abstract Although the effects of temperature on insect behaviours are studied frequently, few studies report on the relationship between temperature and anti-predator behaviours. A negative relationship between ambient temperature and the intensity of death-feigning is found in adults of two seed beetle species, Callosobruchus maculatus (F.) and C. chinensis (L.) (Coleoptera: Bruchidae). Two traits representing the intensity of immobility, the frequency and the duration of death-feigning, are measured at different temperatures. Almost all adults feign death at 15 °C, but the frequency of death-feigning decreases at higher temperatures in C. maculatus, whereas all C. chinensis adults show this behaviour at 15 and 20 °C and almost all show it at 25 °C, but the frequency of death-feigning decreases at 30 and 35 °C. The difference between the two species might be due to the specific strain of each species used in the experiment. The duration of death-feigning is correlated negatively with the increase in ambient temperature in both species. The frequency at which adults feigned death is higher in females than in males in both species, but the duration of death-feigning is higher in females than in males only in C. maculatus. The relationships between temperature and death-feigning behaviours are discussed from physiological and ecological viewpoints.
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When studying animal behavior, it is often necessary to examine traits as a package, rather than as isolated units. Evidence suggests that individuals behave in a consistent manner across different contexts or over time; that is, behavioral syndromes. We compared locomotor activity levels and mating success between beetles derived from two regimes artificially selected for the duration of death-feigning behavior in the adzuki bean beetle, Callosobruchus chinensis. The two selection regimes comprised strains with higher (L) and lower (S) intensity (frequency and duration) of death-feigning behavior, respectively. We found that S strains had higher activity levels than L strains for both sexes, i.e., there is a negative genetic correlation between death feigning and activity. In addition, we found that S strains had higher mating success than L strains, presumably due to higher activity, in males but not in females. We thus demonstrate that death feigning is genetically correlated to mating behavior in males but not females in this species, suggesting that behavioral correlations may not always reflect in the same way in both sexes.
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Although there have been numerous studies on the effects of mating history on mating behaviour, few studies have reported the relationship between mating history and other contextual behaviours such as foraging and predator avoidance. We examined the effect of mating history on death-feigning behaviour (an antipredator behaviour) in the sweetpotato weevil. Because mating behaviour can be divided into phases, we examined the effects of encounters with the opposite sex, copulation and insemination success on death-feigning behaviour. For females after copulation and males after multiple copulations the duration of death-feigning behaviour was reduced, whereas encounters with the opposite sex had no effect. Insemination success did not affect the duration of death feigning in males, but inseminated females reduced the duration of death feigning. We discuss the implications of these results for the effect of mating history on this antipredator behaviour.
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Animals attacked by predators often enter a state of tonic immobility (TI) in which individuals appear to simulate death. Despite the fact that TI is often used as a proxy of fear in domesticated animals, quantitative data on individual variation is very scarce for wild vertebrates. As a consequence, we lack ecological interpretations for the variability in TI that may exist in wild populations. Here, we tested whether there are consistent differences among individuals in 2 components of TI within wild populations of 2 avian species, the Yellow-crowned bishop (Euplectes afer) and the Tree sparrow (Passer montanus). We next tested whether this variation reflects variation in boldness toward predators (measured as the response to 2 predator models) or is simply related to variation in general activity/restlessness (measured as baseline activity) in the bishop. We analyzed our data by means of Bayesian structural equation modeling (SEM), which has several general advantages and, moreover, allowed us to analyze censored (truncated) data. We found good support for relatively high repeatability within individuals of both components of TI. Measures of TI appeared to be uncorrelated with baseline activity. In contrast, our results suggest that individual variation in TI in a wild vertebrate can be interpreted in a context of boldness toward predators, making TI a meaningful and practical behavioral trait for studies involving personality and antipredation behavior in wild populations. In addition, we show that the Bayesian structural equation modeling approach to analyze censored data had greater statistical power than other approaches. Hence, this rarely implemented technique deserves to be more widely used.
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Usually, several traits in organisms are genetically linked with each other; thus, correlated responses to selection are generally observed. Anti-predator behaviors may be genetically correlated with other traits such as life-history. We compared the life-history traits of individuals derived from two regimes artificially selected for the duration of death feigning in the adzuki bean beetle, Callosobruchus chinensis. The two-way selected regimes include the L-lines with stronger intensity (longer duration and higher frequency) and the S-lines with weaker intensity (shorter duration and lower frequency) of death feigning. L-lines exhibited greater longevity, higher rates of emergence, laid bigger eggs and greater reproductive effort, and also had a tendency of faster development. Fecundity was not significantly different between L- and S-lines. These results provide the novel possibility that death feigning is a potentially advantageous anti-predator behavior that, through a positive genetic correlation with some life-history traits, can bring a higher fitness to an individual adopting this behavior. This novel aspect might explain why death-feigning behavior is prevalent in various taxonomic animal groups.
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In a two-choice experiment, cats (Felis domesticus) chose an active quail (Coturnix coturnix japonica) more often than a quail in tonic immobility (TI). In a second experiment, cats were individually presented with two active quail in an open field. Holding and biting by the cat, particularly about the neck, was necessary for inducing TI in a bird. Overall, the total time spent by a cat in stalking, attacking, and handling a bird was inversely related to the total time spent in TI by the bird. These results support the hypothesis that TI is a terminal defense mechanism elicited by predator contact. TI apparently eliminates the movement stimuli that sustain further attack.
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Death feigning is a potentially important behaviour used by a wide variety of animals to increase the probability of escape from a would-be predator. Few data are available on the influence of various factors on death feigning in vertebrates, especially ectotherms, because of difficulties in consistently stimulating the behaviour under controlled conditions. I examined the effects of temperature, body size and locomotor performance on death feigning in neonate brown snakes, Storeria dekayi, in the laboratory. Brown snakes consistently feigned death in water, and contrary to predictions, were more likely to feign death and to feign death longer as temperature increased. Q10 values for death-feigning durations (mean = 2.79) were greater than those for maximal swimming velocities (mean = 1.77) between 10°C and 20°C. However, no statistical difference was detected between Q10 values for feigning durations (mean = 1.11) and swimming velocities (mean = 1.28) between 20°C and 30°C. At 30°C, swimming velocity was negatively correlated with death-feigning duration. Moreover, body size was negatively related to death-feigning duration at 30°C. These results suggest that temperature probably plays a large role in the decision by ectotherms to death feign, and that an animal's locomotor abilities and body size potentially influence the likelihood and duration of death feigning at optimal temperatures. However, physiological constraints greatly reduce the use of death-feigning behaviours at suboptimal temperatures, regardless of locomotor abilities and body size. Therefore, other stationary defensive behaviours are probably more important at suboptimal temperatures.
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A prey animal has the alternative of fleeing or feigning death to survive when it encounters predators. We found that fleeing by an artificial threat, locomotion and feigning death are pleiotropically correlated with a genetic factor related to a biogenic amine in the red flour beetle, Tribolium castaneum. Walking distance of adults was significantly lower in strains artificially selected for longer (L strains) than shorter duration (S strains) of death-feigning. Crosses showed that S-strain adults were dominant in the frequency and duration of death-feigning and locomotor activity compared to those of L strains, suggesting that death-feigning and activity have the same genetic basis. S-strain adults fled, but L-strain adults feigned death, when they encounter artificial threat. Not only adults that were directly selected for the duration of death-feigning, but also the larvae of L strains frequently showed tonic immobility, when they were dropped onto the ground: the larvae of S strains showed this behaviour less often. This suggests that chemical modulators of behaviour present in these insects before and after metamorphosis control both general locomotor activity and death-feigning. Brain levels of the candidate neuromodulator dopamine were, in fact, found to be significantly higher in S strains compared to L strains in the two selection replications. Thus, we suggest that two alternative behaviours related to antipredator strategies, fleeing or feigning death, are associated with the pleiotropic effects of a neuroactive substance in T. castaneum.
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The adaptation of death-feigning (thanatosis), a subject that has been overlooked in evolutionary biology, was inferred in a model prey-and-predator system. We studied phenotypic variation among individuals, fitness differences, and the inheritance of death-feigning behaviour in the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Two-way artificial selections for the duration of death-feigning, over 10 generations, showed a clear direct response in the trait and a correlated response in the frequency of death-feigning, thus indicating variation and inheritance of death-feigning behaviour. A comparison of the two selected strains with divergent frequencies of death-feigning showed a significant difference in the fitness for survival when a model predator, a female Adanson jumper spider, Hasarius adansoni Audouin (Araneomophae: Salticidae), was presented to the beetles. The frequency of predation was lower among beetles from strains selected for long-duration than among those for short-duration death-feigning. The results indicate the possibility of the evolution of death-feigning under natural selection.
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Introduction, The scientific literature on foraging biology in lizards has tended to ignore intraspecific variation. Thus, the species is treated as the unit of analysis, under the implicit assumption that variation within a single species (and, to an even greater degree, within a single population) is trivial relative to variation among species. Many authors therefore talk of broad phylogenetic patterns in foraging mode, with all taxa within major lineages placed within the same major category (e.g. active or ambush). Such generalizations may have substantial value in pursuing broad issues, but at the population level they are simply wrong for many types of organism. Groups of related species certainly share many distinctive features of foraging biology, and there is a genuine validity to statements about lineage-wide patterns. None the less, a detailed analysis of almost any single population (let alone one species) is likely to reveal diversity in trophic biology. For example, juveniles may feed in different ways, in different places and on different kinds and sizes of prey than do adults within the same population. Similarly, males and females may differ in prey utilization. For several reasons, snakes offer more dramatic examples of such intraspecific niche divergence than do lizards. In this chapter, we review published evidence for size and sex effects on foraging biology in snakes, consider underlying biological factors that generate such diversity, and attempt to explain why snakes and lizards – two very closely related groups of organisms – differ so dramatically in the occurrence of intraspecific niche partitioning. é Cambridge University Press 2007.
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Predation by captive red foxes (Vulpes fulva) on approximately 50 ducks comprised of five species was observed in tests conducted at the Northern Prairie Wildlife Research Center, Jamestown, North Dakota. Most ducks were attacked from a rear or lateral position and seized in the cervical or thoracic region. All birds became immobile (death-feigned) immediately when seized and with few exceptions remained motionless during prey-handling and for varying lengths of time thereafter. Initial death feints lasted from 20 sec to 14 min. Recovery was delayed by tactile, visual and, possibly, auditory cues from the foxes. Death-feigning birds appeared alert and often took advantage of escape opportunities. Twenty-nine birds survived initial capture and handling by the foxes. Naive foxes were wary of ducks during initial confrontations, but experienced foxes showed little hesitation in attacking them. After capture, most ducks were taken alive to lay-down sites where they were mouthed and often killed. Then the ducks were usually cached or taken to dens or pups. Several birds were cached alive. Red foxes appear to have adapted to the escape of death-feigning ducks by learning to kill some birds soon after capture and by the evolution of an appendage-severing behavior. Death feigning appears to be a highly developed antipredator behavior of ducks that facilitates the escape of some birds after capture by red foxes.
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Toads are defended chemically by bufadienolides, a class of cardiotonic steroids lethal to most predators. Bufadienolides bind to Na+,K+-ATPases, inhibiting the ability of those cellular pumps to transport ions. In cardiocytes, this inhibition causes arrhythmia and increased contractile strength, which, if prolonged, lead to death. However, several snakes are resistant to bufadienolides and consume toads with no apparent ill effects. Adrenal glands produce hormones that function in the maintenance of Na+,K+-ATPases, and may therefore play an important role in countering the negative effects of bufadienolides. We hypothesized that bufophagous (toad-eating) snakes have enlarged adrenal glands that contribute to the snakes' resistance to bufadienolides, and that sexual dimorphism in adrenal gland size is a general characteristic of bufophagous snakes. We compared phylogenetically independent pairs of taxa to investigate differences in adrenal morphology between bufophagous and nonbufophagous species. We also compared adrenal masses between males and females of bufophagous and nonbufophagous species to test whether sexual dimorphism in adrenal size reported for one species of bufophagous snakes represents a more widespread phenomenon. Our results demonstrate for the first time that the allometric relationship between adrenal mass and body size is significantly different between several bufophagous species and related nonbufophagous species; adrenal size differs between males and females in those bufophagous species, with males having larger adrenal glands, but no such dimorphism exists in related nonbufophagous species. These results demonstrate that parallel morphological responses have occurred repeatedly in bufophagous snakes and suggest that the adrenal glands play a role in mediating the negative effects of bufadienolide ingestion in bufophagous snakes.
Article
Diet manipulation, an habituation test, and chemical analysis of urinary free amino acids were used to demonstrate that bullhead catfish (Ictalurus nebulosus) naturally detect the body odors of conspecifics and respond to them in a predictable fashion. These signals are used in dominance and territorial relationships and lead to increased aggression toward chemical "strangers." The results support the general notion that nonspecific metabolites, as well as specific pheromones, are important in chemical mediation of social behavior.
Article
The effects of physical environment, time in captivity, and distance between potential predator and prey on defensive behaviors were examined inAnolis carolinensis. When the experimenter was nearby, duration of immobility was significantly longer in the open than in areas with nearby foliage. However, this relationship between duration of immobility and the testing environment in the anole was reversed by Day 9 in captivity. Flight latency of anoles after termination of immobility was significantly shorter in anoles housed in terraria containing foliage, while greater incidence of freezing was shown by anoles housed in empty terraria. These results suggest that although the physical environment has strong effects on defense behaviors, the different defensive reactions are influenced in different ways.
Article
An immobility reflex may be induced in fish by a vigorous flow of water through the branchial chamber. The reflex was observed in 22 species representing bony and cartilaginous fishes from diverse habitats, and was invariably characterised by loss of caudal muscle tone and limp posture. The immobilised state may be maintained for many hours, and revival is instantaneous. The critical flow rate for induction increases with increasing body size in the snapper, Pagrus auratus, and heart rate falls below the resting rate. In addition, haematological parameters, and plasma lactate after 6 h were typical of resting fish. Although the mechanism is unclear, and the selective advantage for the fish unknown, pressure-sensitive receptors in the branchial chamber are likely to be involved. Application in live fish transport, and recovery from handling and exercise stressors is suggested.
Article
Predator-preference experiments and analyses of natural diets revealed that the caridean shrimp Tozeuma carolinense is underrepresented in the diet of pinfish Lagodon rhomboides, the dominant predatory fish in marine seagrass meadows in the SE USA. The behavioral response of moving around the grass blade, to which a shrimp was clinging, resulted in a significant increase in shrimp survival, and thus is strongly adaptive. Tozeuma also shifted microhabitats in response to predators; individuals that did not respond were often consumed. For the shrimp, predator-avoidance behaviors were far more important than cryptic coloration in eluding predatory fish.-from Author
Article
Individual variation in antipredator behavior may be influenced by ecological factors, such as ambient temperature and predation pressure, and by intrinsic factors, such as physiological condition. We tested the hypothesis that both types of factors interact to induce a specific antipredator response in the treefrog, Scinax hiemalis. When disturbed by the threat of predation, individuals of this species exhibit either a passive response by feigning death or immobility, or an active escape response by jumping away. We examined the responses of 24 adult male S. hiemalis to simulated predation in the laboratory at 10, 15, and 20 C. In addition, responses from a single stimulus were compared with those from a series of stimuli. We determined physiological condition from measures of body length and mass, jumping performance, aerobic metabolism, and estimated energy reserves. Temperature had the most influence on antipredator behavior, with more frogs exhibiting passive responses at 10 C than at higher temperatures. If stimulated more than once, the proportion of active responses increased at all three temperatures. Larger individuals were more likely to exhibit an active response, but no mass-independent physiological variables were related to response type. These results suggest that frogs respond to both extrinsic and intrinsic factors that may affect their behavioral performance.
Article
Because relative clutch mass (RMC) adversely affects locomotor performance, and therefore presumably survival rate of pregnant females, it is assumed to be constrained by natural selection. Changes in antipredator tactics during pregnancy can reduce females' dependence on locomotion, thereby alleviating selection acting on RCM. Comparisons of the locomotor performance and antipredator behaviors of pregnant female garter snakes Thamnophis ordinoides before and after parturition indicate that locomotor ability declines and that antipredator tactics change during gestation. Females tend more toward cryptic behavior during pregnancy than after. -from Author
Article
The idea that tonic immobility (TI) may be a reaction to predation has received increasing support in recent years. It follows, from this view, that distance between predator and prey and opportunity for escape should have predictable effects on immobility. Three experiments, using a total of 151 anoles ( Anolis carolinensis ), were conducted. Results of Exp I show that the presence of large bushes, as an explicit escape manipulation, reduced immobility durations in Ss in comparison to what occurred when they were immobilized in an open area, with the effect being most evident the closer the predator was to the prey. Exp II showed that close proximity between anoles and the E produced longer durations of immobility in an open area, while a 3rd experiment showed that with bushes nearby this relationship was reversed; that is, shorter durations of TI with anoles in close proximity to the E. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
The defensive behavior of 43 individually reared snakes of three sympatric species of water snakes (Nerodia cyclopion, N. fasciata, and N. rhombifera) was observed in a continuous 9-min trial involving baseline and 6 different human intruder conditions. Comparisons of the species were made using tongue-flick rates and the total number and proportions of defensive behaviors (coiling, body flattening, striking, thrashing) performed. Tongue-flick rates were similar for all three species in all conditions until the snakes were grasped, at which time the tongue-flick rate of all three species showed a large increase with N. cyclopion significantly higher than N. rhombifera and N. fasciata. Tongue-flicking generally fell off rapidly in each intruder condition after an initial increase, the major exception being the lack of change in behavior when the observer first became visible to the snakes. N. cyclopion responded with significantly more defensive behaviors than the other two species. Nerodia fasciata differed from the other species in performing more of the less aggressive behavior (flattening). Males differed significantly from females, tending to perform more aggressive behavior (strikes). Species and sex differences appear related to phylogenetic relationships as well as differences in microhabitat, activity rhythm and predator pressure. Das Verteidigungsverhalten dreier sympatrischer Wasserschlangen (Nerodia cyclopion, N. fasciata und N. rhombifera) wurde an 43 in völliger Isolation voneinander aufgezogenen Exemplaren der drei Arten in einem einheitlich durchlaufenden neunminütigen Versuch beobachtet. In dem Versuch, der von bestimmten Grundwerten ausging, wurden die Schlangen sechs verschiedenen Situationen menschlichen Eingreifens ausgesetzt. Verglichen wurden die Arten im Hinblick auf die Häufigkeit des Züngelns, die Gesamtanzahl der Abwehr-Verhaltensweisen (sich Zusammenrollen, Abflachen des Körpers, Schlagen, sich Hin- und Herwerfen) sowie die Prozentsätze, die auf jedes dieser Verhaltenselemente entfielen. Die Züngelhäufigkeit war bei alien drei Arten in alien Situationen ähnlich. Lediglich wenn die Schlangen von menschlicher Hand ergriffen wurden, stieg die Häufigkeit des Züngelns erheblich an, wobei N. cyclopion mit Abstand am häufigsten züngelte. Allgemein ging die Frequenz des Züngelns in jeder Versuchssituation nach anfänglicher Steigerung rapide zurück. Nur wenn der Beobachter für die Schlangen zum ersten Mal sichtbar wurde, blieb die Züngelrate während des ganzen Versuchs gleich. N. cyclopion wies eine erheblich höhere Summe von verteidigenden Verhaltensweisen auf als die beiden anderen Arten. Schlangen der Art N. fasciata unterschieden sich von den anderen Arten dadurch, daß ihre Reaktionen wesentlich weniger aggressiv waren (Körperabflachung). Männliche Tiere unterschieden sich von weiblichen generell dadurch, daß das von ihnen geäußerte Verhalten aggressiver war (Schlagen). Unterschiede zwischen Arten sowie Geschlechtern scheinen phylogenetisch bedingt, sowie auf Unterschiede im Mikrohabitat, Aktivitätsrhythmus und in der Feindbedrohung zurückzugehen.
Article
Tonic immobility is a common response of animals to capture by a predator; in some cases, the behaviour is elaborated into death-feigning. Death-feigning is usually interpreted as a last-resort anti-predator tactic that depends on the predator ceasing or slowing its attack when the prey is apparently dead, thus buying time for the prey to escape if the predator’s attention is directed elsewhere, even momentarily. I tested the effects of different handling regimes on the expression of death-feigning in the grass snake (Natrix natrix). In one test, degree of handling had a significant effect on frequency of death-feigning in small snakes, with snakes that received more handling feigning death more often. A second test showed that different initial handling regimes also affected the probability of death-feigning in large snakes, with snakes initially held by the tail feigning death least frequently and those initially held by the head most frequently. Thus, increased apparent threat to a vulnerable part of the body is more likely to result in death-feigning. It remains to be seen whether death-feigning can reduce the threat posed by real predators, but immobility is frequently carried over into the post-release period, during which the animal presumably weighs its chances and awaits an opportunity to escape. Regardless of cause, death-feigning snakes exhibited significantly more frequent and longer post-release immobility than did non-death-feigning snakes, which typically fled immediately upon release. Overall, small snakes feigned death less frequently than adults and were more likely to flee upon release, suggesting that immobility is a riskier anti-predator defence strategy for them.
Article
Contextual flexibility in prey restraint behaviour has been documented in advanced snakes (Colubroidea), but the degree of flexibility for earlier snake lineages has been largely unstudied. We document the prey restraint behaviour of five snake species belonging to three early macrostomate lineages: Loxocemidae, Erycinae and Boidae. Species from these lineages were chosen for this study because they utilize similar prey resources but exhibit different ecological habits that may have important consequences on prey restraint behaviour. Snakes (n = 27) were studied in a systematic experimental design assessing the effects of mouse size (small and large) and status (live and dead) across a total of 216 feeding trials. Loxocemus and Erycine snakes were highly flexible in their prey restraint behaviour patterns and these varied across prey category. Individuals of Boa constrictor exhibited very little contextual flexibility in feeding behaviour, confirming earlier reports. Flexibility in prey restraint behaviour corresponded with loop application pattern, whether the snake bent laterally or ventrally when forming a loop around prey. Our study is the first to show that early macrostomate snakes exhibit flexible prey restraint behaviours. Thus, our results suggest that flexibility in predatory behaviour may be more widespread across snake taxa than previously thought and we offer hypotheses for the observed interspecific differences in snake feeding behaviour.
Article
Differences in snake color pattern have been demonstrated to affect behaviors involved in antipredator defense. Snakes with blotched or banded color patterns are concealed when not moving, and tend to rely on concealment and aggression for defense. In contrast, snakes with uniform or striped color patterns are easily seen when stationary, but their speed and direction are difficult to track when moving. They tend to rely on flight for protection. Some snake taxa exhibit ontogenetic change in color pattern, but the behavioral consequences of this change have not been investigated. I present results of a behavioral study in the racer, Coluber constrictor, which has a blotched juvenile color pattern but is uniformly colored as an adult. Hatchling racers were significantly more likely than adults to show aggressive behavior when confronted with a model predator, whereas adults were more likely to flee. This supports the hypothesis that changes in behavior and color pattern are correlated in this species to provide effective antipredator defense at different stages of life history. I also examined sprint speed, which may be an important factor in antipredator defense. Juvenile and adult racers showed a similar relationship between length and speed, a pattern also seen in other species that lack color change. This result suggests that sprint speed is not a causal factor in the evolution of ontogenetic color change.
Article
Correlational selection favors combinations of traits and is a key element of many models of phenotypic and genetic evolution. Multiple regression techniques for measuring selection allow for the direct estimation of correlational selection gradients, yet few studies in natural populations have investigated this process. Color patterns and antipredator behaviors of snakes are thought to function interactively in predator escape and therefore may be subject to correlational selection. To investigate this hypothesis, I studied the survivorship of juvenile garter snakes, Thamnophis ordinoides, as a function of a suite of escape behaviors and color pattern. The only natural selection detected favored opposite combinations of stripedness of the color pattern and the tendency to perform during escape evasive behaviors called reversals. This selection presumably results from optical illusions created by moving patterns and their effects on visually foraging predators. Analysis of the bivariate selection surfa
Article
Many contextual factors affect the anti-predator behaviour of animals. In ectotherms, in which most physiological activities depend on body temperature, ambient temperature is one of the most important of these factors. We examined the effects of temperature on the anti-predator behaviour of an ectotherm, the Japanese grass snake (Rhabdophis tigrinus). This species has a large repertoire of anti-predator behavioural responses. Among these responses are several anti-predator displays that appear to be unique to this species and perhaps others in a small group of closely related species possessing nuchal glands containing toxic secretions that may be derived from their toxic toad diet. Snakes were tested at room temperatures of 14, 22 and 30°C with order of temperatures balanced. A long wand modified to simulate initial contact by a predator was used as the stimulus. Snakes exhibited rather passive responses (neck flatten, body flatten, neck arch and immobile) more frequently at low temperatures, and fled more frequently at high temperatures. The dorsal facing posture, a characteristic posture directed against the stimulus, was observed more frequently at low temperatures. Threatening, assertive responses such as strike were rarely observed. These results showed that R. tigrinus shifts its anti-predator behaviour from multiple passive responses to active flight responses with increasing temperature. This snake species thus appears to rely more on its nuchal glands as a predator deterrent at low ambient temperatures. Consistent individual variation was also observed, and its adaptive and causal bases are discussed.
Article
Data on over 950 natural matings of red-sided garter snakes,Thamnophissirtalisparietalis , in Manitoba revealed size-assortative pairing: large males tended to mate with large females, and small males with small females. Unlike previously reported cases of size-assortative mating, the causal mechanism in these snakes involved a size-related shift in active mate selection by males. In the field, courtship as well as mating was size assortative (albeit, with considerable scatter around the trend line). Staged trials in outdoor arenas showed that males of all sizes preferred to court large rather than small females, but this preference was stronger in large males. Males adjusted their courtship intensity in response to the numbers and sizes of females and competing males, but did not change their preferences with respect to female body size. Thus, size-assortative mating was not a direct consequence of large males excluding their smaller rivals from large females. Males may be selective courters in this species because they have a limited supply of sperm and mating plugs, and hence can copulate effectively only a few times within the mating season. Given intense competition from large males (which primarily court large females), small males may benefit from focusing on small females. Alternatively, small males may be less capable of inducing sexual receptivity from large females. Mark–recapture data confirmed that males grow rapidly from one year to the next. Thus, the size-related shift in male mate choice was due to an ontogenetic change rather than the existence of multiple male morphs differing in both body size and courtship preference.
Article
An experimenter induced tonic immobility (TI) in parentally naive chicks (G. gallusdomesticus). The chicks remained in TI longer when they were exposed to a conspecific adult fear squawk alarm call than when exposed to an equally novel attraction call or white noise. In a second experiment, both aerial-predator and ground-predator alarm calls enhanced TI similarly to the fear squawk call which is elicited by capture. These results support the hypotheses that TI is an antipredator defense mechanism and that alarm calls evolved through kin-selection.
Article
1. The durations of successive periods of induced tonic immobility in the lizard Anolis carolinensis was examined as a function of temperature. An automatic recording method was employed and observations were made of 12,000 to 15,000 immobilizations with six animals over a temperature range of 5 degrees to 35 degrees C. during 5 months. 2. The durations of the immobile periods were found to vary rhythmically in most cases. The reciprocal of the duration of the rhythm, i.e., the rate of change of the process underlying the rhythms, when plotted as a function of temperature according to the Arrhenius equation show distributions of points in two straight line groups. One of these groups or bands of points extends throughout the entire temperature range with a temperature characteristic of approximately micro = 31,000 calories, and the other covers the range of 20 degrees to 35 degrees C. with micro equal to approximately 9,000 calories. 3. The initial stimulus in a series of inductions of immobility appears to set off a mechanism which determines the duration of the state of quiescence. Succeeding forced recoveries seem to have no effect on the normal duration of the rhythm. 4. These results are interpreted by assuming the release, through reflex stimulation, of hormonal substances, one effective between 5 degrees and 35 degrees C. and the other effective between 20 degrees and 35 degrees C. These substances are assumed to act as selective inhibitors of impulses from so called "higher centers," allowing impulses from tonic centers to pass to the muscles. 5. In some experiments a progressive lengthening in successively induced periods of immobility was observed. The logarithm of the frequency of recovery when plotted against time in most of these cases (i.e., except for a few in which irregularities occurred) gave a linear function of negative slope which was substantially unaffected by temperature. In these cases it is assumed that a diffusion process is controlling the amount of available A substance. 6. The results are similar to those obtained by Crozier with Cylisticus convexus. The duration of tonic immobility seems to be maintained in both arthropod and vertebrate by the chemical activity of "hormonal" selective inhibitors. The details of the mechanisms differ, but there is basic similarity. 7. Injections of small amounts of adrenalin above a threshold value are found to prolong the durations of tonic immobility of Anolis, by an amount which is a logarithmic function of the "dose." It is possible that internally secreted adrenalin, above a threshold amount, may be involved in the maintenance of tonic immobility. 8. The production of tonic immobility reflexly is a problem distinct from that of the duration of immobility. It is suggested that the onset may be induced by "shock" to the centers of reflex tonus causing promiscuous discharge of these centers with accompanying inhibition of the higher centers. Such a condition may result when an animal is suddenly lifted from the substratum and overturned, or when, as in the case of Anolis, it struggles with dorsum down. This reaction of the "tonic centers" may at the same time lead to discharge of the adrenal glands by way of their spinal connections thus prolonging the state.
Article
Several authors have suggested that African antelope (family Bovidae) exemplify coadaptation of ecological, behavioral, and morphological traits. We tested four hypotheses related to the ecology and behavior of 75 species of African antelope using both conventional statistical techniques and techniques that account for the nonindependence of species by considering their phylogenetic relationships. Specifically, we tested the hypotheses that (1) dietary selectivity is correlated negatively with body mass, (2) dietary selectivity is correlated negatively with group size, (3) gregarious species either flee or counterattack when approached by predators, but solitary and pair-living species seek cover to hide, and (4) body mass and group size are correlated positively. Each of these hypotheses was examined for the global data set (family Bovidae) and, when possible, within the two antelope subfamilies (Antilopinae and Bovinae) and within 7 of the 10 antelope tribes. The results of our conventional and phylogenetically corrected analyses supported the hypotheses that group and body size vary predictably with feeding style and that antipredator behavior varies with group size. The hypothesis that body mass and group size are correlated positively was supported by conventional statistics, but these two traits were only weakly related using a phylogenetically corrected analysis. Moreover, qualitative and quantitative comparisons within each of the eight major African antelope tribes generally gave little support for the four hypotheses tested. Thus, although our analyses at the subfamily level provided results that were consistent with prior hypotheses, our analyses at the level of tribes were equivocal. We discuss several possible explanations for these differences.