Tracy Langkilde

Why Did the Snake Cross the Road? Effects of Roads on Movement and Location of Mates by Garter Snakes (Thamnophis sirtalis parietalis)

If animals avoid road surfaces or are unable to follow conspecific trails across such surfaces, previously continuous populations may be fragmented. We gathered data on the effects of a small (4-m wide) gravel road on the behavior and trail-following abilities of garter snakes (Thamnophis sirtalis parietalis) in Manitoba, central Canada. As expected, the road surface had less vegetation cover, a more open canopy and, thus, higher incident radiation than did the surrounding grassland. Contrary to expectations, however, substrate temperatures were lower on the road than in its surrounds, because of the higher reflectivity of the roads surface. On a nearby asphalt road, substrate temperatures were relatively high on the road surface only in the evening, as surrounding areas cooled. Focal sampling showed that snakes avoided the gravel road, typically changing direction when they encountered it. If they crossed the road, they did so by the shortest possible route (straight across). Mate-searching male snakes were less able to follow substrate-deposited pheromonal trails left by females if those trails crossed a road than if the trails were entirely within the surrounding grassland. Thus, roads may significantly modify snake movement patterns, as well as the ability of males to locate reproductive females. Our study provides the first detailed information on the effects of roads on snake behavior.

Invasive fire ants alter behavior and morphology of native lizards

Nonnative species introductions are becoming more common, but long-term consequences of the novel pressures imposed by invaders on native species remain poorly known. The red imported fire ant, Solenopsis invicta, is an invasive species with potential global impact. Comparison of lizards across the invasive range within the United States reveals novel antipredator strategies and altered morphologies that mitigate potentially lethal attack by these ants, within 70 years of their introduction. The likelihood that adult lizards will behaviorally respond to fire ant attack increases with time since invasion, but hatchlings exhibit high levels of antipredator behavior irrespective of their site of origin. Adults and hatchlings from sites invaded longer ago also have relatively longer hind limbs. This trait increases the effectiveness of behavioral strategies for removing ants and is likely an adaptive response to minimize envenomation during attack. The observed changes are not correlated with habitat, exposure to fire ants, or latitude, arguing against phenotypic plasticity and learning as causal mechanisms, and museum specimens show that morphological differences were not evident prior to fire ant invasion. These data contribute to our growing awareness that ecological invasions can prompt adaptive responses, altering the nature of interactions between invaders and the natives they contact.

Competing for crevices: interspecific conflict influences retreat-site selection in montane lizards

Direct interference competition between sympatric taxa affects habitat use and shelter-site selection in species within most major vertebrate lineages. However, studies on interspecific social interference in reptiles largely have been confined to research on interactions between non-native (invasive) species and native fauna. Does interspecific interference also influence habitat use within natural assemblages of reptiles? We studied five broadly sympatric species of viviparous montane skinks within the genera Egernia and Eulamprus in southeastern Australia. Previous work has shown strong interspecific overlap in abiotic attributes of shelter-sites for these taxa, but no joint occupancy of retreats. Laboratory trials in which we manipulated the identity of co-occurring lizards revealed frequent displacement from “preferred” (hotter) shelters, with interspecific interactions more intense than intraspecific conflicts. The five species displayed a linear interspecific dominance hierarchy, with larger species displacing smaller taxa. Field manipulations confirmed that interspecific interactions between these species affect shelter-site use. We conclude that direct agonistic encounters between individuals of different species strongly influence habitat use by lizards within this assemblage.

The opportunistic serpent: Male garter snakes adjust courtship tactics to mating opportunities

Reproductive males encounter potential mates under a range of circumstances that influence the costs, benefits or feasibility of alternative courtship tactics. Thus, males may be under strong selection to flexibly modify their behaviour. Red-sided garter snakes (Thamnophis sirtalis parietalis) in Manitoba overwinter in communal dens, and court and mate in large aggregations in early spring. The number of males within a courting group varies considerably, as do the body sizes of both males and females. We manipulated these factors to set up replicated courtship groups in outdoor arenas, and analysed videotapes of 82 courtship trials to quantify courting behaviours of male snakes. Larger and more heavy-bodied males courted more vigorously than did their smaller, thinner-bodied rivals, and large females attracted more intense courtship. The major effect, however, involved the number of rival males competing for copulation. Males in large groups not only reduced their overall vigour of courtship, but also modified their tactics in such a way as to benefit from the courtship activities of rival males. That is, they devoted less energy to inducing female receptivity (which requires energy-expensive caudocephalic waving) and more effort to behaviour (tail-searching) that enhanced their own probability of mating if the female gaped her cloaca. This social parasitism reveals an unsuspected plasticity and complexity in the behavioural tactics of reproducing male snakes.

Cryptic forcible insemination: male snakes exploit female physiology, anatomy, and behavior to obtain coercive matings.

Whether males can inseminate uncooperative females is a central determinant of mating system evolution that profoundly affects the interpretation of phenomena such as multiple mating by females, mate choice, reproductive seasonality, and courtship tactics. Forcible insemination is usually inferred from direct physical battles between the sexes and has been dismissed on intuitive grounds for many kinds of animals. For example, snakes have elongate flexible bodies (making it difficult for a male to restrain a female physically), males are typically smaller than females, and copulation requires female cloacal gaping to enable intromission. Male garter snakes (Thamnophis sirtalis) do not display any overt aggression during courtship and simply lie over the female and exhibit rhythmic pulsating caudocephalic waves of muscular contraction; previous studies have interpreted this behavior as a mechanism for eliciting female receptivity. In contrast, we show that male garter snakes forcibly inseminate females. They do so by taking advantage of specific features of snake physiology, respiratory anatomy, and antipredator behavior. The snake lung extends along most of the body, with the large posterior section (the saccular lung) lacking any respiratory exchange surface. Rhythmic caudocephalic waves by courting male garter snakes push anoxic air from the saccular lung forward and across the respiratory surfaces such that females cannot obtain oxygen. Their stress response involves cloacal gaping, which functions in other contexts to repel predators by extruding feces and musk but in this situation permits male intromission. Thus, superficially benign courtship behaviors may involve cryptic coercion even in species for which intuition dismisses any possibility of forcible insemination.

Natural History Note The Physiological Basis of Geographic Variation in Rates of Embryonic Development within a Widespread Lizard Species

The duration of embryonic development (e.g., egg incubation period) is a critical life‐history variable because it affects both the amount of time that an embryo is exposed to conditions within the nest and the seasonal timing of hatching. Variation in incubation periods among oviparous reptiles might result from variation in either the amount of embryogenesis completed before laying or the subsequent developmental rates of embryos. Selection on incubation duration could change either of those traits. We examined embryonic development of fence lizards (Sceloporus undulatus) from three populations (Indiana, Mississippi, and Florida) that occur at different latitudes and therefore experience different temperatures and season lengths. These data reveal countergradient variation: at identical temperatures in the laboratory, incubation periods were shorter for lizards from cooler areas. This variation was not related to stage at oviposition; eggs of all populations were laid at similar developmental stages. Instead, embryonic development proceeded more rapidly in cooler‐climate populations, compensating for the delayed development caused by lower incubation temperatures in the field. The accelerated development appears to occur via an increase in heart mass (and, thus, stroke volume) in one population and an increase in heart rate in the other. Hence, superficially similar adaptations of embryonic developmental rate to local conditions may be generated by dissimilar proximate mechanisms.

Invader danger: lizards faced with novel predators exhibit an altered behavioral response to stress.

Animals respond to stressors by producing glucocorticoid stress hormones, such as corticosterone (CORT). CORT acts too slowly to trigger immediate behavioral responses to a threat, but can change longer-term behavior, facilitating an individuals survival to subsequent threats. To be adaptive, the nature of an animals behavior following elevated CORT levels should be matched to the predominant threats that they face. Seeking refuge following a stressful encounter could be beneficial if the predominant predator is a visual hunter, but may prove detrimental when the predominant predator is able to enter these refuge sites. As a result, an individuals behavior when their CORT levels are high may differ among populations of a single species. Invasive species impose novel pressures on native populations, which may select for a shift in their behavior when CORT levels are high. We tested whether the presence of predatory invasive fire ants (Solenopsis invicta) at a site affects the behavioral response of native eastern fence lizards (Sceloporus undulatus) to elevated CORT levels. Lizards from an uninvaded site were more likely to hide when their CORT levels were experimentally elevated; a response that likely provides a survival advantage for lizards faced with native predatory threats (e.g. birds and snakes). Lizards from a fire ant invaded site showed the opposite response; spending more time moving and up on the basking log when their CORT levels were elevated. Use of the basking log likely reflects a refuge-seeking behavior, rather than thermoregulatory activity, as selected body temperatures were not affected by CORT. Fleeing off the ground may prove more effective than hiding for lizards that regularly encounter small, terrestrially-foraging fire ant predators. This study suggests that invasive species may alter the relationship between the physiological and behavioral stress response of native species.

Traffic noise causes physiological stress and impairs breeding migration behaviour in frogs

Noise from human activities is increasing globally. We provide evidence that traffic noise increases glucocorticoid concentrations and impairs reproductive behavior in frogs. Since prolonged stress can compromise health, survival and reproduction, and because impaired reproductive behavior can reduce mating opportunities, these results suggest noise may contribute to amphibian declines.

The role of behaviour in the establishment of novel traits

It may seem as if behaviour is so plastic that it would not foster the establishment of a genetically determined trait, but under some circumstances, it can greatly influence whether a novel trait, such as a new morphology, spreads in a population. If the behaviours associated with the traits function already exist, a new variant finds a ready foothold, and selection can act accordingly. Behaviours that are particularly likely to foster novel traits include those that play a role in life history, such as antipredator behaviour, sexual signalling and foraging. Examples of behaviour facilitating novel trait establishment include the spread of a silent mutant in male Pacific field crickets, Teleogryllus oceanicus , and the propensity of juvenile fence lizards to show antipredator behaviours towards attacking fire ants, providing a selective opportunity for the evolution of longer limbs. The genetic or physiological mechanisms behind a behaviour can also influence its establishment; for example, learning may generate selection in favour of conspicuous novel traits faster, and for a wider range of traits, than genetically based sensory biases. Just as changes in behavioural traits over evolutionary time may expose populations of individuals to new adaptive zones, behavioural variation within a population may increase the diversity of environments to which individuals are exposed.

Consequences of envenomation: red imported fire ants have delayed effects on survival but not growth of native fence lizards

Context Aggressive encounters, including those with venomous species, impose selective pressure on native species. Immediate lethal outcomes of these encounters have been the primary focus of research in this field. However, not all aggressive interactions result in immediate mortality, and indirect consequences of aggressive interactions may be an equally important but under-considered selective force. The red imported fire ant is a globally important venomous invader that imposes novel selective pressure on native communities. Aims We examined indirect effects of fire ant envenomation on native fence lizard growth rates and subsequent survival. Methods Fence lizards are subject to fire ant envenomation in the field when they eat fire ants (they are stung inside the mouth) and through fire ant attack (they are stung on the body). We quantified body sizes of adult lizards from fire ant-invaded and uninvaded sites. We then experimentally exposed hatchling fence lizards to the two modes of fire ant envenomation, and quantified their growth and survival over 1 year. Key results Lizards from fire ant-invaded sites were smaller than those from an uninvaded site, even at similar latitudes. However, in contrast to studies on other native taxa, we found no effect of fire ant venom on growth rates of lizards from naive or fire ant-invaded populations. Lizards exposed to fire ant venom, through both eating and attack, experienced higher rates of delayed mortality, with 34% of lizards dying 1–11 weeks post-envenomation compared with 12% of lizards in the control treatment. These patterns were true for fire ant naive populations as well as those exposed to fire ants for ~35 generations. Conclusions These results suggest that the smaller body sizes observed in fence lizards from fire ant-invaded sites are not a consequence of exposure to fire ant venom. However, fence lizards from both sites suffer delayed survival costs of fire ant envenomation. Implications The present study highlights the importance of considering indirect fitness consequences of aggressive encounters if we are to fully understand the ecological and evolutionary consequences of these interactions, and adequately manage and predict the impacts of invasive species.