Andrea Gazzola

Urbanization affects refuge use and habituation to predators in a polymorphic lizard

Prey–predator interactions are plastic behaviours shown by both players, which constantly modify their decisions depending on physiological conditions and ecological context. We investigated whether the behavioural response to repeated simulated predatory attacks varied between adult males of the common wall lizard, Podarcis muralis, inhabiting environments characterized by different degrees of human presence. Our aim was to detect possible effects of urbanization on antipredator responses, in terms of activity, time spent hidden in refuges and habituation. Moreover, since this lizard species exhibits intrapopulation colour polymorphism, we looked for the occurrence of possible correlations between antipredator strategy and individual ventral coloration. We found that urban lizards spent less time in their refuge after predatory attacks and decreased successive hiding times faster than rural lizards, suggesting different wariness towards a potential predator. Irrespective of population, yellow lizards gradually spent less time in the refuge before appearing and emerging outside than the other two morphs. Conversely, red lizards showed progressively longer appearance and emergence times after successive tests, suggesting a growing sensitization to the potential threat of a predatory attack. In conclusion, our study showed the occurrence of different levels of behavioural plasticity in common wall lizards antipredator response: the population level, depending on ecological context, here different degrees of exposure to human disturbance, and the individual level, which suggests the occurrence of morph-specific antipredator strategies. Thus, using a lizard species as a model, we shed light on two key points of evolutionary ecology concerning both the antipredator response and the factors driving the maintenance of intraspecific polymorphism.

Dynamics and population structure of native Echinogammarus stammeri (Karaman, 1931) (Crustacea: Amphipoda) and non-native Gammarus roeselii Gervais, 1835 (Crustacea: Amphipoda) occurring in sympatry in Northern Italy

Abstract Gammarids are one of the most successful invaders in freshwater ecosystems due to both their diet plasticity and high reproductive capability. The Balkanic amphipod, Gammarus roeselii Gervais, 1835, has colonised a small canal in the southern part of the sub-lacustrine Ticino River basin (Northern Italy), where it lives in sympatry and shares the same habitat with the native species Echinogammarus stammeri (Karaman, 1931). We surveyed the populations of the two species over 12 months (from July 2014 to June 2015) to investigate their structure and dynamics. The overall densities of the two populations were similar in the study area, but we observed marked differences in the population structure: G. roeselii was in fact more successful than the native gammarid in achieving the adult stage, and E. stammeri exhibited a rather limited reproductive period, which does not justify the stable occurrence of juvenile individuals. We hypothesise that the population of the native gammarid in this small habitat is supported by a continuous upstream immigration of individuals from the Ticino River, while G. roeselii exhibits a well-structured and self-reproducing population.

Fear is the mother of invention: anuran embryos exposed to predator cues alter life-history traits, post-hatching behaviour, and neuronal activity patterns

ABSTRACT Neurophysiological modifications associated to phenotypic plasticity in response to predators are largely unexplored, and there is a gap of knowledge on how the information encoded in predator cues is processed by prey sensory systems. To explore these issues, we exposed Rana dalmatina embryos to dragonfly chemical cues (kairomones) up to hatching. At different times after hatching (up to 40 days), we recorded morphology and anti-predator behaviour of tadpoles from control and kairomone-treated embryo groups as well as their neural olfactory responses, by recording the activity of their mitral neurons before and after exposure to a kairomone solution. Treated embryos hatched later and hatchlings were smaller than control siblings. In addition, the tadpoles from the treated group showed a stronger anti-predator response than controls at 10 days (but not at 30 days) post-hatching, though the intensity of the contextual response to the kairomone stimulus did not differ between the two groups. Baseline neuronal activity at 30 days post-hatching, as assessed by the frequency of spontaneous excitatory postsynaptic events and by the firing rate of mitral cells, was higher among tadpoles from the treated versus the control embryo groups. At the same time, neuronal activity showed a stronger increase among tadpoles from the treated versus the control group after a local kairomone perfusion. Hence, a different contextual plasticity between treatments at the neuronal level was not mirrored by the anti-predator behavioural response. In conclusion, our experiments demonstrate ontogenetic plasticity in tadpole neuronal activity after embryonic exposure to predator cues, corroborating the evidence that early-life experience contributes to shaping the phenotype at later life stages. Summary: Predator kairomones perceived by anuran embryos induce life-history and behavioural changes in tadpoles, and result in a long-term increase in neuronal activity and response to predator cues.

Context-dependent behavioural lateralization in the European pond turtle Emys orbicularis (Testudines, Emydidae)

ABSTRACT Lateralization presents clear advantages in ecological contexts as the dominance of one brain side prevents the simultaneous activation of contrasting responses in organisms with laterally located eyes. This is crucial in selecting a safe refuge during a predatory attack and may strongly affect predator–prey interactions. We explored the possible presence of lateralization in the anti-predatory behaviour of European pond turtles, considering their escape facing a possible predatory attack. Thirty individuals (17 males, 13 females) were exposed to three different environmental situations of gradually increasing predatory threat: escape underwater from an unsafe shelter, diving into the water from a basking site and righting after being overturned. All turtles were tested 20 times for each of the three experiments (60 trials per individual; 1800 overall trials). We recorded multiple behavioural responses in the general context of predation risk. This was done in order to assess both the existence of lateralization and possible correlations among different behaviours as function of lateralization. The number of significant responses to the left side was always prevalent in each of the three simulated anti-predatory situations, suggesting the existence of a lateralized behaviour in this species. At the individual level, the differences we found in the three experiments could be related to different ecological contexts and consequent risk of predation. Our findings, among the few on chelonians, support the possible involvement of right hemisphere activity and, most importantly, reveal how the complexity of a general predatory context can affect the laterality of escape behaviour. Summary: Laterality for escape behaviour is modulated by environmental context, leading to possible unexplored relationships for behavioural responses, above all in reptiles, in which brain lateralization is still poorly investigated.

The effect of thinning and cue:density ratio on risk perception by Rana dalmatina tadpoles

The “risk assessment hypothesis” considers prey density as an important variable to properly assess the actual level of risk, and predicts that, when the ratio between predator cue concentration and prey density is constant, the level of risk perceived by prey is the same. All previous studies which tested this hypothesis with Anurans manipulated density by placing tadpoles into experimental tubs at fixed group sizes. As predation is a process that produces a progressive decrease in prey density, i.e. “thinning”, prey may respond to the rate of group size reduction rather than the absolute number of conspecifics in a given place at a given time. To test if Rana dalmatina tadpoles perceive the progressive decrease in population density due to predation and are able to use this information to fine-tune anti-predator responses, we combined thinning with a constant cue:density ratio and evaluated how these two types of information affected the level of activity of tadpoles. Our results showed no effect of density reduction on prey level of activity, and thinning did not interact with cue intensity to modify tadpoles’ behaviour. However, we observed no difference in tadpole behavioural responses between treatments with the same cue:density ratio.

Is It Worth the Risk? Food Deprivation Effects on Tadpole Anti-Predatory Responses

Predation risk affects foraging behavior and, particularly, the amount of time devoted to the search for food. When exposed to predation risk, food deprived animals should be risk prone and relax behavioral defenses to a wider extent than well fed individuals. To test for this prediction, we used a 2 × 2 factorial design experiment, manipulating both the energetic state (fed vs. fasted) and exposure to an attack-released cue (injured vs. uninjured conspecifics) of common water frog tadpoles (Pelophylax kl. esculentus). Contrary to expectations, food deprivation significantly lowered the activity level of predator-exposed tadpoles. As in this experiment no food resource was added to test containers, energy conserving behavior might have both delayed starvation and lowered the probability of encountering the potential predator. To test for the effect of food availability on behavioral responses, we performed a second experiment, using the same protocol and procedures, except for adding food to all test containers. All tadpoles showed similar levels of activity, while fed tadpoles exposed to alarm cues tended to swim farther from the cage containing the stimulus than in the first experiment. As many anuran larvae can feed on dead conspecifics, prey-borne cues may have been interpreted as the potential presence of both a food source and a predator, fed tadpoles possibly being more confident than fasted tadpoles in their ability to escape predation in case an actual attack occurs.

Freshwater turtles reveal personality traits in their antipredatory behaviour

Animals respond to predation risk with antipredatory behaviours that may disclose the presence of different personality traits among individuals in a population, and how populations may differ for the expression of those traits. Variation among individuals is a necessary condition for the evolution through natural selection and inter-individual behavioural differences may be selected in different environmental situations. We tested whether individuals of two freshwater turtle species, Emys orbicularis and Mauremys leprosa, show consistent risk-taking behaviour when exposed to the presence of a potential predator. In an outdoor experimental setting, we simulated a predatory attack by overturning a turtle onto its carapace and recording three different behavioural response variables. Our results showed clear differences between species. The appearance time was highly consistent over the trials for both species, but was shorter for E. orbicularis and very long for M. leprosa. Waiting time was consistent only for females of E. orbicularis while M. leprosa did not show repeatability and had significantly longer waiting times. The number of failed righting attempts, likely being partially dependent on turtle individual performance, was highly consistent during the experiment for both species. The hiding behaviour in both species of freshwater turtles was consistent over time and, therefore, could be regarded as a personality trait. However, the differences in waiting times consistency suggested possible differences in defensive strategies between sexes and species.

Male calling activity in syntopic populations of Rana latastei and Rana dalmatina (Amphibia: Anura)

Abstract Rana latastei and Rana dalmatina are two explosive breeder amphibians whose mating seasons last less than 1 month. The two species have very different repertoires of vocalisations, as Rana dalmatina uses only one advertisement call while Rana latastei uses two different vocalisations with opposite structural features. In our research, we continually recorded the calling activity of the two species during a whole breeding season in a pond where they breed in syntopy in order to assess the possible functions of their vocalisations. Males of both species increased their activity in coincidence with the peak of activity of females, but Rana latastei males reached the peak 2–3 days before the deposition peak. By contrast, males of Rana dalmatina reached the peak at the same time as the deposition peak, and called at high intensity long after the deposition peak. These different acoustic patterns led us to infer different prevailing functions for the vocalisations of these species. Male vocalisations of Rana latastei are addressed only to males in order to gain and confirm their position within male hierarchy. By contrast, Rana dalmatina males might vocalise also in order to attract females, rather than to deter rival males. Thus, vocalisation in this second species might also play an intersexual function. The two call types of Rana latastei were used since the beginning of the breeding season. No difference was found also in daily activity, and both vocalisations were used preferentially during night time.