Meal Size Effects on Antipredator Behavior of Hatchling Trinket Snakes, Elaphe helena

Current foraging models limit the decision‐making process of animals to the food searching and consuming phase. The post‐consummatory phase of feeding may influence optimal meal size for some species as a morphologic change often results from feeding. In snakes, a single prey item can lead to abrupt increases in body mass, thus influencing locomotor performance. Identifying factors affecting locomotor performance can help predict behaviors that should maximize an animal's chance of evading predators. Although many snakes ingest large percentages of their body mass, not much work has examined the post‐consummatory effects of ingesting bulky prey differing in relative mass. I examined the locomotor performance and antipredator tactics of hatchling trinket snakes (Elaphe helena) after subjecting snakes to mice prey varying by relative mass differences of 20–35%, 50–59% or 70–79% of an individual hatchling's body mass. Snakes in treatment groups were compared with snakes in a control group (0%). Meal size‐affected locomotor parameters such as burst speed, endurance, and endurance times for hatchlings that ingested 50–59% and 70–79% of their body mass (p < 0.001). Recent feeding also affected the types of antipredator modes employed. Hatchlings in the 0% and 20–35% treatments exhibited behaviors that were categorized as active and threatening, while hatchlings in the 50–59% and 70–79% treatments exhibited stationary, neutral, and cryptic behaviors. Although snakes may become more reclusive following a meal, this study demonstrates that relative prey mass affects the ability of hatchling trinket snakes to flee from a predator. In turn, these results suggest that the post‐consummatory effects of foraging should be considered in optimal foraging models for organisms that consume a substantial portion of their body mass during a single feeding.     

Short-Term Behavioural Responses of Impalas in Simulated Antipredator and Social Contexts

Prey animals often have to trade off foraging against vigilance. However, vigilance is costly and individuals are expected to adjust their vigilance and its cost in relation to social cues and their predation risk. To test this, we conducted playback experiments in the field to study how lions’ (Panthera leo) roars and male impalas’ (Aepyceros melampus) territorial vocalizations affected the vigilance and foraging behaviours as well as movements of female impalas. Our results show that impalas adjusted their activities in different ways depending on the vocalizations broadcast. After lions’ roars were played, female impalas increased their vigilance activity (in particular increasing their high-cost vigilance – vigilance without chewing), decreased their bite rates and increased their movements, whereas male impalas’ vocalizations caused females to decrease their vigilance (decreasing their low-cost vigilance – vigilance while chewing) and increase their movements without affecting their bite rates. Therefore, it appears that predators’ vocalizations stimulate anti-predator behaviours such as vigilance and movement at the expense of foraging, whereas males’ vocalizations increase individuals’ displacements at the expense of vigilance. Overall, this study shows that both predator and social cues have direct effects on the behaviour of gregarious prey and need to be considered in future studies.     

Antipredator Behavioral Responses of Native and Exotic Tadpoles to Novel Predator

Factors related to the invasion process, such as high abundance of invaders, residence time, and functional distinctiveness, are well documented, but less attention has been given to the effects of antipredator strategy of invasive species during colonization. In this study, we explored the antipredator strategy of an introduced species by comparing the predator avoidance behaviors of two native anuran species and one introduced(exotic) species in the presence of different predators. The two native anuran species used in the study were Black-spotted Pond Frog Rana nigromaculata and Terrestrial Frog Rana limnocharis. The introduced(invasive) species used was American bullfrog Lithobates catesbeianus. Chinese pond turtle Chinemys reevesii, Red-backed rat snake Elaphe rufodorsata, and Big-headed turtle Platysternon megacephalum were used as predator species. Chinese pond turtles and Red-backed rat snakes are native predators of Black-spotted Pond Frogs and Terrestrial Frogs, while Big-headed turtles are novel(unfamiliar) to the two frogs. All three predator species are novel(unfamiliar) to the American bullfrog. The results show that tadpoles of the two native species displayed behaviors of recognizing the two native predators, but did not display the capability of identifying the novel predator. Results from our study also suggest that American bullfrog tadpoles exhibited strong antipredator behavioral responses by displaying the capability of identifying unfamiliar predators without cohabitation history and prior exposure to them. Such antipredator behavioral responses could have resulted in more favorable outcomes for an invading species during the invasive introductory process.     

Comparison of Antipredator Responses of Two Related Water Striders to a Common Predator

This study compares the antipredator responses of two congeneric water striders that live in different habitats yet share a common predator. Aquarius nebularis and A. remigis are stream-dwelling species of water striders found in close association in central Kentucky. Aquarius nebularis typically inhabit third- and fourth-order streams that support diverse and complex fish communities; A. remigis inhabit adjacent first- and second-order tributaries that tend to have either no fish or relatively few fish patchily distributed. The ecological conditions for these two species are distinctly different, yet the green sunfish (Lepomis cyanellus) is a surface-feeding predator and a potential risk to both species. In experimental pools with sunfish, an initial fish strike caused A. remigis to move to the edge of the pool and become inactive. For the rest of the observation period, A. remigis reduced behaviour patterns that attract predators such as skating on open water, mating and male–male aggression. The proportion of A. remigis missing from sunfish pools was 5 times higher than in pools lacking fish, suggesting that 20% of water striders were killed by predation. In contrast, an initial fish strike caused A. nebularis to exhibit a burst of activity as individuals erratically skated over the open water. They then resumed the less active pre-attack behaviours a short time later. Aquarius nebularis showed none of the antipredator behaviours typical for A. remigis. Furthermore, the proportion of A. nebularis missing from sunfish pools did not differ from that in pools without fish. Although antipredator behaviour has been examined for relatively few species of water striders, this study suggests that the behaviour of the most commonly studied species, A. remigis, may not be indicative for water striders in general., Corresponding author: James J. Krupa, School of Biological Sciences, University of Kentucky, Lexington, KY 40506-0225, U.S.A. E-mail: bio149@pop.uky.edu bio149@pop.uky.edu     

Interspecific Responses of Ringtailed Lemurs to Playback of Antipredator Alarm Calls Given by Verreaux's Sifakas

The ringtailed lemur, Lemur catta, and Verreaux's sifaka, Propithecus verreauxi verreauxi, are diurnal prosimians living sympatrically in Madagascar. Species-specific alarm calls emitted by each of these two species in response to aerial and terrestrial predators differ acoustically. Behavioural responses of ringtailed lemurs evoked by playbacks of conspecific alarm calls differ when the vocalizations were produced in response to aerial predators as opposed to terrestrial predators. We conducted playback experiments on two populations of ringtailed lemurs, using two types of sifaka alarm calls. One population consisted of free-ranging groups which lived sympatrically with sifakas, the other was a colony group which had no contact with sifakas. The results illustrate that the former group of lemurs can perceive what type of predators the sifaka calls refer to, whereas the latter group was not able to recognize the difference in the calls.     

Effects of Sublethal Cadmium Exposure on Antipredator Behavioural and Antitoxic Responses in the Invasive Amphipod Dikerogammarus villosus

Amphipods are recognised as an important component of freshwater ecosystems and are frequently used as an ecotoxicological test species. Despite this double interest, there is still a lack of information concerning toxic impacts on ecologically relevant behaviours. The present study investigated the influence of cadmium (Cd), a non-essential heavy metal, on both antipredator behaviours and antitoxic responses in the invasive amphipod Dikerogammarus villosus under laboratory conditions. Amphipod behaviour (i.e. refuge use, aggregation with conspecifics, exploration and mobility) was recorded following a 4-min test-exposure to 500 μg Cd/L with or without a 24-h Cd pre-exposure and in the presence or absence of a high perceived risk of predation (i.e. water scented by fish predators and injured conspecifics). Following behavioural tests, malondialdehyde (MDA) levels, a biomarker for toxic effect, and energy reserves (i.e. lipid and glycogen contents) were assessed. Cd exposures induced (1) cell damage reflected by high MDA levels, (2) erratic behaviour quantified by decreasing refuge use and exploration, and increasing mobility, and (3) a depletion in energy reserves. No significant differences were observed between 4-min test-exposed and 24-h pre-exposed individuals. Gammarids exposed to Cd had a disturbed perception of the alarm stimuli, reflected by increased time spent outside of refuges and higher mobility compared to gammarids exposed to unpolluted water. Our results suggest that Cd exposure rapidly disrupts the normal behavioural responses of gammarids to alarm substances and alters predator-avoidance strategies, which could have potential impacts on aquatic communities.     

Antipredator deception in terrestrial vertebrates

Abstract Deceptive antipredator defense mechanisms fall into three categories： depriving predators of knowledge of prey＇s presence, providing cues that deceive predators about prey handling, and dishonest signaling. Deceptive defenses in terrestrial vertebrates include aspects of crypsis such as background matching and countershading, visual and acoustic Batesian mimicry, active defenses that make animals seem more difficult to handle such as increase in apparent size and threats, feigning injury and death, distractive behaviours, and aspects of flight. After reviewing these defenses, I attempt a preliminary evaluation of which aspects of antipredator deception are most widespread in amphibians, reptiles, mammals and birds     

Predatory Attacks to the Head vs. Body Modify Behavioral Responses of Garter Snakes

An animal's response to predatory attack may depend upon which part of its body is the focus of that attack, because of differential vulnerability to injury. Many avian and mammalian predators direct attacks preferentially toward the prey's head, so simulated attacks that do not have this focus may elicit non‐natural responses. We ‘pecked’ 152 free‐ranging adult male garter snakes (Thamnophis sirtalis parietalis) in Manitoba either on the head or the midbody, and recorded their responses. The snakes’ antipredator tactics were affected not only by body size (larger snakes performed threat displays more often) and body temperature (hotter snakes were more likely to flee), but also by location of the attack. Pecks to the head generally resulted in snakes coiling and hiding their heads, often simultaneously elevating and wriggling their tails in an apparent distraction display. In contrast, pecks to the midbody stimulated either escape responses, or (in snakes that did not flee) open‐mouthed threat displays. More generally, antipredator tactics may respond in flexible ways to details of the predator–prey encounter (including attributes of the habitat as well as the morphology and behavior of both participants) and hence, experimental studies need to carefully simulate such details. The part of the body under attack may be an important factor in this respect.     

Antipredator Behavior in Desmognathus ochrophaeus: Threat‐Specific Responses to Chemical Stimuli in a Foraging Context

Prey species may reduce the likelihood of injury or death by engaging in defensive behavior but often incur costs related to decreased foraging success or efficiency. To lessen these costs, prey may adjust the intensity or type of antipredator behavior according to the nature of the perceived threat. We evaluated the potential for threat‐sensitive responses by Allegheny Mountain dusky salamanders (Desmognathus ochrophaeus) exposed to chemical stimuli associated with predation by asking three questions: (1) Do individual D. ochrophaeus respond to chemical cues in a threat‐sensitive manner? (2) Do salamanders exhibit the same pattern of behavioral response while foraging? and (3) Is foraging efficiency reduced when focal individuals are exposed to stimuli from predators or predation events? In our first experiment, we evaluated salamander chemosensory movements (nose‐taps), locomotor activity (steps), and edge behavior in response to chemical stimuli from disturbed and injured conspecifics as well as predatory Gyrinophilus porphyriticus and found that individual D. ochrophaeus show a significant graded increase in nose‐taps when exposed to cues from conspecifics and a reduction in activity when exposed to the predator. In our second experiment, we again observed salamander responses to the same chemical stimuli but in this instance added five Drosophila prey to the test dishes. We found that salamanders exhibited a similar pattern of response to the chemical stimuli in the presence of prey, showing a graded increase in nose‐taps to cues from conspecifics and a reduction in activity when exposed to the predator. However, foraging efficiency (i.e. the proportion of successful strikes) did not vary significantly among treatments. Our data show that individual D. ochrophaeus detect and differentially respond to chemical stimuli associated with predation, but do not significantly reduce foraging efficiency. Overall, the type and relative intensity of these responses is largely unaffected by the presence of potential prey.     

Antipredator Responses by Native Mosquitofish to Non-Native Cichlids: An Examination of the Role of Prey Naiveté

The strong impact of non‐native predators in aquatic systems is thought to relate to the evolutionary naiveté of prey. Due to isolation and limited dispersal, this naiveté may be relatively high in freshwater systems. In this study, we tested this notion by examining the antipredator response of native mosquitofish, Gambusia holbrooki, to two non‐native predators found in the Everglades, the African jewelfish, Hemichromis letourneuxi, and the Mayan cichlid, Cichlasoma urophthalmus. We manipulated prey naiveté by using two mosquitofish populations that varied in their experience with the recent invader, the African jewelfish, but had similar levels of experience with the longer‐established Mayan cichlid. Specifically, we tested these predictions: (1) predator hunting modes differed between the two predators, (2) predation rates would be higher by the novel jewelfish predator, (3) particularly on the naive population living where jewelfish have not invaded yet, (4) antipredator responses would be stronger to Mayan cichlids due to greater experience and weaker and/or ineffective to jewelfish, and (5) especially weakest by the naive population. We assayed prey and predator behavior, and prey mortality in lab aquaria where both predators and prey were free‐ranging. Predator hunting modes and habitat domains differed, with jewelfish being more active search predators that used slightly higher parts of the water column and less of the habitat structure relative to Mayan cichlids. In disagreement with our predictions, predation rates were similar between the two predators, antipredator responses were stronger to African jewelfish (except for predator inspections), and there was no difference in response between jewelfish‐savvy and jewelfish‐naive populations. These results suggest that despite the novelty of introduced predators, prey may be able to respond appropriately if non‐native predator archetypes are similar enough to those of native predators, if prey rely on general antipredator responses or predation cues, and/or show neophobic responses.     

Evolutionary Patterns in Advanced Snakes

One prevalent view of phylogenetic events in advanced snakesholds that the fangs evolved along at least two pathways one(e.g. elapids) from ancestors with enlarged anterior and theother (e.g. viperids) from ancestors with enlarged posteriormaxillary teeth. Selective forces driving these changes arepresumed to arise from the increasing advantages of teeth andglands in venom injection. In this paper another plausible viewof these events is proposed. First fangs of both elapids and viperids likely evolved fromreal maxillary teeth. In non-venomous snakes, differences intooth morphology and function suggest that there may be somedivision of labor among anterior and posterior maxillary teeth.Anterior maxillary teeth, residing forward in the mouth likelyserve the biological role of snaring and impaling prey duringthe strike. They are also conical frequently recurved and lacka secretion groove. On the other hand posterior teeth becauseof their geometric position on the maxilla and mechanical advantages,tend to serve as aids in preingestion manipulation and swallowingof prey. They are often blade shaped and occasionally bear asecretion groove along their sides. Although both front andrear maxillary teeth of nonvenomous snakes may be elongatedthis is likely to serve these different functional roles andhence they evolved under different selective pressures. Whenfangs evolved they did so several times independently but fromrear maxillary teeth. In support one notes a) the similar positionpostorbital of venom and Duvernoy s glands b) similar embryonicdevelopment of fangs and rear maxillary teeth c) secretion groovewhen present, is found only on rear teeth and d) similar biologicalroles of some rear teeth and fangs. For ease in clearance ofthe prey during the strike the fangs are positioned forwardin the mouth accomplished in viperid snakes by forward rotationof the maxilla and elapids by rostral anatomical migration tothe front of the maxilla. Second, the adaptive advantage first favoring initial rear toothenlargement likely centered not on their role in venom injectionbut rather on their role in preingestion manipulation and swallowing.However once enlarged, teeth would be preadapted for later modificationinto fangs under selection pressures arising from advantagesof venom introduction. This has implications for the function and evolution of associatedstructures. Besides possibly subduring or even killing of preythe secretion of Duvernoy's gland may be involved in digestionor in neutralizing noxious or fouling products of the prey.The presence or absence of constriction need not be functionallytied to absence or presence of venom injection. The phylogeneticpathways outlined herein were likely traveled several timesindependently in advanced snakes.     

Antipredator behavior and the asset-protection principle

Many species of animals face the continual problem of balancingthe trade-off between reducing predation risks and maintainingor increasing their reproductive fitness. The terms of the trade-offare often asymmetric: each separate behavioral decision maylead to only a marginal increase in fitness, but may place theorganism's entire future reproduction in jeopardy. Consequently,the organism's reproductive value is an important componentof most antipredator decision problems. In this paper reproductivevalue is considered as an asset in need of protection. The "asset-protectionprinciple" states that the larger the current reproductive asset,the more important it becomes to protect it. Because reproductivevalue is usually age and condition dependent, optimal antipredatorbehavior also often depends on these variables. I use a uniformmodeling technique (dynamic programming) to address a varietyof issues related to antipredator behavior     

Scaling of Cardiovascular Physiology in Snakes

The elongate body form of snakes and the wide diversity of habitatsinto which they have radiated have affected the form and functionof the cardiovascular system. Heart position is strongly correlatedwith habitat. The heart is located 15–25% of the bodylength from the head in terrestrial and arboreal species, but25–45% in totally aquatic species. Semi-aquatic and fossorialspecies are intermediate. The viperids are exceptional, withgenerally more posterior hearts but arboreal species have heartscloser to the head. An anterior heartis favored when snakesclimb because it reduces the hydrostatic pressure of the bloodcolumn above the heart and tends to stabilize cephalic bloodpressure. In water, where hydrostatic bloodpressure is not aproblem, a more centrally located heart is favored because theheart does less work perfusing the body. In terrestrial species,head-heart distance increases linearly with body length andthe increased hydrostatic pressure is matched by higher restingarterial blood pressure in longer animals. Unlike mammals andbirds, snakes have blood pressures that increasewith body mass.The added stress on the ventricle wall in larger snakes is correlatedwith ventricles that are larger than predicted by other reptiles.Heart mass scales with body mass to the 0.95 power in snakesbut only 0.77–0.91 in other reptiles that are not as subjectto the hydrostatic effects of gravity. The spongy hearts ofreptiles do not conform well to the Principle of Laplace.     

Antipredator Responses to a Previously Neutral Sound by Free-living Adult Golden-mantled Ground Squirrels, Spermophilus lateralis (Sciuridae)

I investigated whether free-living adult golden-mantled ground squirrels ( Spermophilus lateralis ) could learn to associate a novel sound with the appearance of a predator. Using a classical conditioning protocol, I presented adult squirrels with a novel tone followed by the appearance of a model hawk. After repeated trials, I again measured the squirrels' behavioral responses to the tone and compared them with their pretraining responses. Individuals that experienced the tone paired with the hawk responded with antipredator behavior of longer duration after pairing than before and these responses were indistinguishable from responses to natural, conspecific alarm calls. By examining the process, rather than simply the pattern, of call recognition ontogeny, this study provides new evidence for a mechanism by which animals can develop the ability to respond to both conspecific and heterospecific calls.     

Antipredator behavior promotes diversification of feeding strategies

Animals often facultatively engage in less risky behavior when predators are present. Few studies, however, have investigated whether, or how, such predator-mediated behavior promotes diversification. Here, we ask whether tadpoles of the spadefoot toad Scaphiopus couchii have a diminished ability to utilize a potentially valuable resource--anostracan fairy shrimp--because of behavioral responses to predation risk imposed by carnivorous tadpoles of the genus Spea. Observations of a congener of Sc. couchii that occurs in allopatry with Spea, coupled with an ancestral character state reconstruction, revealed that Sc. couchii's ancestors likely consumed shrimp. By experimentally manipulating the presence of Spea carnivore-morph tadpoles in microcosms, we found that Sc. couchii reduce feeding and avoid areas where both Spea carnivores and shrimp occur. We hypothesize that the recurrent expression of such behaviors in sympatric populations of Sc. couchii led to the evolutionary fixation of a detritivorous feeding strategy, which is associated with a reduced risk of predation from Spea carnivores. Generally, predator-mediated behavior might play a key role in promoting diversification of feeding strategies.     

Heterochrony and Early Left-Right Asymmetry in the Development of the Cardiorespiratory System of Snakes

Snake lungs show a remarkable diversity of organ asymmetries. The right lung is always fully developed, while the left lung is either absent, vestigial, or well-developed (but smaller than the right). A ‘tracheal lung’ is present in some taxa. These asymmetries are reflected in the pulmonary arteries. Lung asymmetry is known to appear at early stages of development in Thamnophis radix and Natrix natrix. Unfortunately, there is no developmental data on snakes with a well-developed or absent left lung. We examine the adult and developmental morphology of the lung and pulmonary arteries in the snakes Python curtus breitensteini, Pantherophis guttata guttata, Elaphe obsoleta spiloides, Calloselasma rhodostoma and Causus rhombeatus using gross dissection, MicroCT scanning and 3D reconstruction. We find that the right and tracheal lung develop similarly in these species. By contrast, the left lung either: (1) fails to develop; (2) elongates more slowly and aborts early without (2a) or with (2b) subsequent development of faveoli; (3) or develops normally. A right pulmonary artery always develops, but the left develops only if the left lung develops. No pulmonary artery develops in relation to the tracheal lung. We conclude that heterochrony in lung bud development contributes to lung asymmetry in several snake taxa. Secondly, the development of the pulmonary arteries is asymmetric at early stages, possibly because the splanchnic plexus fails to develop when the left lung is reduced. Finally, some changes in the topography of the pulmonary arteries are consequent on ontogenetic displacement of the heart down the body. Our findings show that the left-right asymmetry in the cardiorespiratory system of snakes is expressed early in development and may become phenotypically expressed through heterochronic shifts in growth, and changes in axial relations of organs and vessels. We propose a step-wise model for reduction of the left lung during snake evolution.