Historical influence of predation pressure on escape by Podarcis lizards in the Balearic Islands

Island tameness (reduced escape behaviour on islands where prey have experienced prolonged relaxation of predation pressure) is known in several taxa, although the relationships between recent predation pressure and escape on islands are poorly known. We investigated escape by numerous populations exposed to differing predation pressure of two sister species of Podarcis lizards in the Balearic Islands. Our main findings are that flight initiation distance was greater in Podarcis pityusensis than Podarcis lilfordi and increased as predation pressure increased in P. pityusensis. Island tameness led to extinction of P. lilfordi on Menorca and Mallorca following anthropogenic introduction of predators; this species is extant only on nearby islets. The lack of relationship between recent predation pressure and flight initiation distance in P. lilfordi indicates that the historically acquired deficit in the ability to adjust escape behaviour to predation pressure still exists. Podarcis pityusensis, which was exposed to greater natural predation pressure before human introduction of predators, survives on Ibiza and Formentera, as well as on islets. Retention of the ability to respond to predation pressure is consistent with our finding that flight initiation distance increases as predation pressure increases among current populations. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Influence of incubation temperature on morphology, locomotor performance, and early growth of hatchling wall lizards (Podarcis muralis)

Eggs of wall lizards (Podarcis muralis) were incubated at three temperatures approaching the upper limit of viability for embryonic development in this species (26, 29, and 32 degrees C) to assess the influence of temperature on various aspects of hatchling phenotype likely affecting fitness. The thermal environment affected size and several morphometric characteristics of hatchling lizards. Hatchlings from eggs incubated at 32 degrees C were smaller (snout-vent length, SVL) than those from 26 and 29 degrees C and had smaller mass residuals (from the regression on SVL) as well as shorter tail, head, and femur relative to SVL. Variation in the level of fluctuating asymmetry in meristic and morphometric traits associated with incubation temperatures was quite high but not clearly consistent with the prediction that environmental stress associated with the highest incubation temperatures might produce the highest level of asymmetry. When tested for locomotor capacity in trials developed at body temperatures of 32 and 35 degrees C, hatchlings from the 32 degrees C incubation treatment exhibited the worst performance in any aspect considered (burst speed, maximal length, and number of stops in the complete run). Repeated measures ANCOVAs (with initial egg mass as covariate) of snout-vent length and mass of lizards at days 0 and 20 revealed significant effects of incubation temperature only for mass, being again the hatchlings from eggs incubated at 32 degrees C those exhibiting the smallest final size. All together, our results evidenced a pervasive effect of thermal regime during incubation (and hence of nest site selection) on hatchling phenotypes. However, incubation temperature does not affect hatchling phenotypes in a continuous way; for most of the analysed traits a critical threshold seems to exist between 29 and 32 degrees C, so that hatchlings incubated at 32 degrees C exhibited major detrimental effects. J. Exp. Zool. 286:422-433, 2000.     

The use of faecal counts for estimating populations of wall lizards (Podarcis muralis)

Measurements of the rates at which droppings of wall lizards ( Podarcis muralis ) on Jersey appeared in, and disappeared from, the environment made it possible to formulate a simple mathematical model for the dynamics of faecal pellet populations. The model shows how, for a given lizard population, the number of droppings changes with time according to weather conditions. It was used to estimate lizard densities at a number of sites from daily pellet counts. There were significant differences in the densities of lizards between sites; possible reasons for these are discussed.     

Lateralization in the predatory behaviour of the common wall lizard (Podarcis muralis)

Ectotherms have been shown being lateralized as well as mammals and birds. This is particularly evident in visual lateralization, i.e. the different use of the eyes, leading to use a specific eye to observe specific kind of stimuli and to process them with the correspondent contralateral hemisphere. Several lower vertebrates are facilitated in this from the lateral position of the eyes, enabling them to carry out more tasks simultaneously, controlled by different eyes and relative hemispheres. Predatory responses seem usually mediated by the right eye/left hemisphere in fishes, amphibians and some sauropsids, but there are no strong evidences of this in lizards. Eighteen wild males of the Common wall lizard Podarcis muralis were tested individually in captivity to ascertain whether they are lateralized to look at prey with a specific eye. The lizards were gently induced entering a 30-cm long central arm of a T-maze which led to a 44.5-cm long arm cross-arm at whose extremities there were two identical prey, Tenebrio molitor larvae, familiar to the lizards. We recorded what direction the lizards chose to reach the prey and the frequency and duration of head turning, indicative of looking either prey with the left or the right eye. We found that individuals show being lateralized at individual level. The preferred direction taken to reach the prey is the right for the majority of those (4 of 5) showing an evident preference, indicating also a possible form of laterality at population level. In addition, lizards maintained the same head side of the direction taken turned for more time towards the prey than the opposite head side, revealing an eye preference for observing this kind of cue. Our study demonstrates how males of Podarcis muralis have a visual lateralization to capture prey. Furthermore, it is another support to the hypothesis of vertebrate lateralization derivation from a common ancestor.     

Widespread primary,but geographically restricted secondary,human introductions of wall lizards,Podarcis muralis

Establishing the introduction pathways of alien species is a fundamental task in invasion biology. The common wall lizard, Podarcis muralis, has been widely introduced outside of its native range in both Europe and North America, primarily through escaped pets or deliberate release of animals from captive or wild populations. Here, we use Bayesian clustering, approximate Bayesian computation (ABC) methods and network analyses to reconstruct the origin and colonization history of 23 non‐native populations of wall lizards in England. Our analyses show that established populations in southern England originate from at least nine separate sources of animals from native populations in France and Italy. Secondary introductions from previously established non‐native populations were supported for eleven (47%) populations. In contrast to the primary introductions, secondary introductions were highly restricted geographically and appear to have occurred within a limited time frame rather than being increasingly common. Together, these data suggest that extant wall lizard populations in England are the result of isolated accidental and deliberate releases of imported animals since the 1970s, with only local translocation of animals from established non‐native populations. Given that populations introduced as recently as 25 years ago show evidence of having adapted to cool climate, discouraging further translocations may be important to prevent more extensive establishment on the south coast of England.     

Conspicuous blue tails,dorsal pattern morphs and escape behaviour in hatchling Iberian wall lizards (Podarcis hispanicus)

Predation has profound effects on the phenotypes of animal prey and, in lizards, the relationship between coloration and antipredatory behaviour has been studied in depth. However, studies that address the relationships between dorsal patterns and tail coloration with escape behaviour in polymorphic lizards are absent in the literature. We describe dorsal morphs and measured tail coloration and escape behaviour in hatchling Iberian wall lizards, Podarcis hispanicus, a species with a previously undescribed female‐restricted dorsal polymorphism (reticulated‐blotched males, and either striped or reticulated‐blotched females) and juvenile tails with conspicuous blue coloration, which is probably used to divert predator attacks towards the autotomizable tail. Overall we provide evidence for the existence of sexual dimorphism in tail ultraviolet reflectance between reticulated females and males, with striped females being intermediate. We identified sex/dorsal morph, body size and tail brightness as predictors of different aspects of escape behaviour and suggest the existence of two alternative escape strategies between striped and reticulated‐blotched females that may be dependent on dorsal morph differences, independently of sex. Reticulated‐blotched females, and also males (all reticulated‐blotched), ran faster and spent less time paused than striped females, which might reflect an escape behaviour strategy based on endurance in striped females. In addition, lowland males displayed tail waving as a ‘last resort’ antipredator strategy that may be related to fatigue. We concluded that hatchling antipredatory behaviour is influenced by both dorsal pattern and tail conspicuousness. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1094–1106.     

Metallothionein in the liver of the small lizard Podarcis muralis

A cysteine-rich protein presenting optical and biochemical features typical of metallothionein and a similar amino acid composition was found in the liver of the small lizard Podarcis muralis. Animals were given either CdCl2 (0.8 mg Cd2+/kg body wt) or saline (NaCl 0.9%) by i.p. injection for 3 days. A second group of animals were injected with a single dose of [35S]cysteine plus CdCl2 or saline. Lizard MT contained Zn and Cu when injected with saline and also Cd when injected with CdCl2. Metallothionein induction by cadmium was demonstrated by radioactive labelling.     

The effect of body armature on escape behaviour in cordylid lizards

The possession of armour may affect escape behaviour in two ways. On one hand, by decreasing vulnerability to predators, armour may permit individuals to use habitats and behaviours that are too risky for unarmoured individuals. Alternatively, the possession of armour may have negative trade-offs on other traits involved in antipredator behaviour, such as sprint speed, thus constraining antipredator options relative to those available to unarmoured individuals. To examine these contrasting predictions, we examined species in the lizard family Cordylidae, which contains remarkable morphological diversity, ranging from completely unarmoured to heavily defended species. Moreover, phylogenetic analysis indicates that armour has been an evolutionarily labile trait. We found support for the second prediction. Degree of body armature was inversely correlated with distance run from a predator: heavily armoured species always entered refuges after short distances, whereas many unarmoured lizards continued to flee and could not be induced to enter a refuge. Possession of armour was also negatively related to use of vertical surfaces during escape behavour. These results were unchanged when analysed in a phylogenetic context. Thus, we conclude that the morphological requirements for active flight and armoured defence are incompatible. Heavily armoured species are bulky, have short legs and run more slowly than less armoured species. Rather than constituting an alternative to behavioural antipredator tactics, we conclude that the possession of armour is part of an antipredator syndrome that includes habitat use and behaviour as well as morphology. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Magnitude of food reward affects escape behavior and acceptable risk in Balearic lizards, Podarcis lilfordi

During encounters with predators, prey must balance the degreeof risk against the loss of fitness-enhancing benefits suchas feeding and social activities. Most studies of tradeoffsbetween risk and cost of escaping have measured flight initiationdistance and time to emerge from refuge, for which theory providesrobustly supported predictions. Tradeoffs involving other aspectsof encounters, including distance fled and time between escapeand return to a food source, have received little theoreticalor empirical attention. By adapting models of flight initiationdistance and time between entry into refuge and emergence, wepredict effects of predation risk and cost on distance fledand time to return to a source of benefit after fleeing. Actingas simulated predators that approached at a fixed speed, weconducted an experimental field study to test the hypothesesthat flight initiation distance, distance fled, and time toreturn to food by Balearic lizards (Podarcis lilfordi) decreasewith the presence and amount of insect food. Predictions ofthe models were strongly supported, including those for distancefled and return time, but predictions for other cost factorsand predation risk factors remain to be tested.     

Morphological correlates of burst speed and field movement patterns: the behavioural adjustment of locomotion in wall lizards (Podarcis muralis)

Locomotion of lizards has clear morphological determinants and is important for developing activities such as feeding, social interaction and predator avoidance. Thus, morphological variation is believed to have fitness consequences through affecting locomotor performance. This paper firstly evaluates the dependence of burst speed on morphology, and secondly examines the movement patterns of free-ranging undisturbed wall lizards ( Podarcis muralis ) engaged in several kinds of activity. Body size was the most important correlate of burst speed as performed at the optimal temperature for running in the laboratory. After removing size effects from performance and morphological traits, the length of some particular limb segments had positive influence on burst speed, but these effects were weak, each trait explaining less than 16% of variance in burst speed. Free-ranging P. muralis exhibited intermittent locomotion, with movement sequences interrupted by frequent short pauses. Field movement patterns greatly differed depending upon the kind of activity and were in most aspects independent of the size and sex of the animal. P. muralis involved in thermoregulation performed short and low-speed displacements; exploratory activities were characterized by frequent, slow and short movements. On the contrary, lizards involved in intraspecific pursuits and predator escape developed comparatively high speeds, although only exceptionally did they attain the size-specific burst speed predicted from the laboratory trials. Speed of escape increased with distance to the refuge and the animals are able to assess predation risks to modulate approach distance, speed and pauses, so maximum exertion is seldom required. The evolution of locomotor capacities exceeding routine needs is discussed in the context of the principle of 'excessive construction'.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 135–146.     

Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure

We investigated the possible role of variation in predation pressure in the phenotypic divergence of two island populations of the Italian wall lizard, Podarcis sicula . In 1971, ten adult specimens from the island of Pod Kopište (Adriatic Sea, Croatia) were transported to the island of Pod Mrčaru, 3.5 km east, where they founded a new population. Although the two islands resemble each other in general physiognomy (size, elevation, microclimate) and in the absence of terrestrial predators, lizards from the newly established population are now on average larger and have shorter hind limbs. They also exhibit lower maximal sprint speed as measured on a racetrack, and fatigue faster when chased in a torus track. In the field, lizards from the original population of Pod Kopište respond to a simulated predatory attack by fleeing at larger approach distances and by running further from the predator than lizards from Pod Mrčaru. These changes in morphology, behaviour and performance may result from the relaxed predation intensity on the latter island. Our analysis of the structural features of the microhabitats suggests that the vegetation on Pod Mrčaru offers more protection to lizards. Also, plasticine models of lizards, laid out on the islands, less often exhibited signs of being attacked by birds on Pod Mrčaru than on Pod Kopište. Our findings provide an example of how changes in (possibly a single) environmental factor may simultaneously produce responses in behaviour, morphology and whole-animal physiology, and this on a surprisingly small spatial and temporal scale.     

The selective basis for increased egg retention: early incubation temperature determines hatchling phenotype in wall lizards (Podarcis muralis)

The thermal environment during development influences many aspects of the phenotype of hatchling reptiles. We hypothesized that temperature should differentially affect early incubation stages, in which differentiation dominates over growth, and late incubation stages, characterized by high growth rates. To test this idea, we incubated eggs of wall lizard ( Podarcis muralis ) under three regimes with the same mean temperature (29 °C), one constant and two variable with opposite sequences: first cold (25 °C) and then hot (32 °C), and vice versa. Hatchlings incubated at high temperature during the initial period had shorter hindlimbs and tails than those incubated under the other two temperature regimes and shorter heads than those incubated initially at low temperature. Thus, temperature experienced by embryos during the early external incubation period produced similar phenotypic responses compared to those reported in previous studies for the same constant temperature applied over the whole incubation period. Because female wall lizards select lower body temperatures during pregnancy, an increase of intrauterine retention would extend the time of exposure of developing embryos to suitable temperatures. Diminution of body temperature during pregnancy is contrary to the expected pattern under the hypothesis that egg retention has evolved to accelerate development, as proposed by the cold-climate model for evolution of viviparity in squamates, and the results of the present study support the alternative hypothesis of developmental optimization as a special case of the broader maternal manipulation view.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 441–447.     

Antipredatory behaviour in lizards: interactions between group size and predation risk

Group size effects on antipredatory behaviour are well documented in numerous animals, but little is known about how the level of predation risk influences this process. We tested the hypothesis that group size and level of risk interact to affect the levels of antipredatory behaviour in the group-living sun skink, Lampropholis delicata. We controlled the size of lizard groups (N=1, 2, 4, 8 or 12 females) and altered predation risk by providing either a basking tile covered with chemical cues from a predator (high risk) or one without scent (low risk). The time allocated to individual antipredatory behaviour decreased significantly with increasing group size. The relation between group size and time allocated to individual antipredatory behaviour was nonlinear and asymptotic, and did not change under low and high risks of predation. However, group size and predation risk interacted to affect significantly the time that lizards allocated to antipredatory behaviour. When the overall risk from predators was high, individual responsiveness decreased strongly as group size became larger. In contrast, when the overall risk from predators was low, individual responsiveness decreased weakly as group size became larger. Consequently, the time that lizards allocated to antipredatory behaviour under different risks of predation converged as group size increased.     

Immunocytochemical and electrophoretic distribution of cytokeratins in the regenerating epidermis of the lizard Podarcis muralis

Using immunocytochemistry at light- and electron-microscope levels, we studied the distribution of three monoclonal antibodies (AE1, AE2, AE3) specific for mammalian alpha-keratins in regenerating lizard epidermis. We also characterized the keratins expressed during this process by immunoblotting after electrophoretic separation. The AE1 antibody is localized in the basal and suprabasal layers of prescaling and scaling epidermis. During the first stages of scale neogenesis, the AE1 antibody also marks the differentiating oberhautchen and beta-layer, but it disappears from these layers as they mature. This antibody does not stain the prekeratinized and keratinized outermost layers in the hinge region. The AE2 antibody labels the superficial wound epidermis, prekeratinizing and keratinized beta- and alpha-layers, but not basal and suprabasal cells. The AE3 antibody labels all living and keratinized epidermal layers, although AE3 immunoreactivity decreases and disappears as the beta-layer matures. The ultrastructural study shows that the AE2 and AE3, but not the AE1, antibodies specifically label small electron-dense areas within the beta-layer, suggesting retention of alpha-keratins. In the stages of tail regeneration examined, immunoblotting with the three antibodies used for the immunolocalization gives a pattern similar to that of the normal epidermis, except distally, where the process of scale differentiation begins. In this region, in addition to the keratin forms discovered in the normal and in proximal regenerating epidermis, an intense low molecular weight band at 40-41 kDa, positive to all three antibodies, is clearly detectable. Furthermore, in the distal region AE1 and AE3 antibodies, but not the AE2, recognize a weak band at 77-78 kDa not present in the normal and proximal epidermis. The localization and the possible role of the different keratins in the regenerating epidermis is discussed.     

Chemical communication in the lacertid lizard Podarcis muralis: the functional significance of testosterone

Chemical signals are essential for intersexual communication in many animals, including lizards. While faeces have been suggested to contain socially relevant chemical stimuli, epidermal gland secretions are generally believed to be the leading source of chemosignals involved in lizard communication. Early research has shown that sex hormones affect epidermal gland activity, with androgens stimulating gland/pore size and/or gland productivity. However, the functional significance of hormone‐induced glandular activity in lizard chemical communication remains unclear. In this study, we manipulated testosterone (T) concentrations in male Podarcis muralis lizards. While T‐supplementation did not change pore size, it did increase secretion production substantially. Chemosensory tests showed that female conspecifics tongue‐flick at a higher rate and more quickly towards the secretion of males with experimentally increased T levels than towards the secretion of control males, suggesting that females can discriminate between males with dissimilar T levels based on chemical cues of secretion alone. Based on the scent of faeces, however, females were unable to discriminate between males with differential T levels. Also, females reacted more quickly when offered larger amounts of secretion – irrespective of whether secretions were obtained from control or T‐increased males. This result indicates that secretion quantity affects chemosignal detectability in Podarcis muralis.     

Influence of photoperiod and temperature on testicular recrudescence and body growth in the lizards, Lacerta sicula and Lacerta muralis

Annual testicular cycles in the lizards Lacerta sicula and L. muralis appear to be regulated by the interaction between seasonal changes in body temperature and an endogenous rhythmicity in thermal responsiveness. Photoperiodism does not appear to be an important factor; i.e. testicular activity does not appear to be regulated by daylength.
Following testicular regression in July, the lizards are refractory to sexual stimulation by high temperatures (i.e. normal preferred levels) for about five months. High temperatures accelerate gonadal regression and prevent recrudescence during late summer. Reduced temperatures stimulate testicular enlargement and spermatid formation during the autumn; this recrudescence can be blocked by treatment with testosterone. Very low temperatures suppress gonadal activity during mid-winter.
Maintenance of lizards at constant high temperatures (33°C) starting in July suppresses testicular recrudescence until December. Also, testicular collapse occurs in lizards transferred to high temperatures after recrudescence has started. The gonads are stimulated by exogenous gonadotropins at 33°C during the fall indicating that high temperatures reduce circulating levels of gonadotropins.
The refractoriness to high temperatures is "spontaneously" terminated during midwinter (December) under a wide range of photo-thermal conditions. Low temperatures may accelerate the termination of refractoriness. Thereafter, high temperatures stimulate, and are required for the final development of the testes and accessory sexual structures. Thus, the increase in body temperature following hibernation times the onset of breeding in the spring.
Temperature also has a marked influence on appetite and growth, independent of photo-period. Weight gains are greater at 33° than at 20°C. At 33° there is a tendency for abdominal fat bodies to enlarge but with little hepatic growth; whereas, the reverse occurs at 20°C.     

Evolutionary relationships of Podarcis lizards from Sicily and the Maltese Islands

The electrophoretic variation at 26 presumptive gene loci was investigated in populations of the closely related species Podarcis sicula, P. wagleriana, P. raffonei, and P. filfolensis. Low values of proportion of polymorphic loci (P) and mean observed heterozygosity (H_o) were found in P. sicula (P= 0.10; H_o= 0.016), P. wagleriana (P= 0.13; H_o= 0.029), and P. raffonei (P= 0.08; H_o= 0.017), while higher levels of genetic variability were observed in P. filfolensis (P= 0.17; H_o= 0.054). In the latter species, a multiple regression analysis was carried out in order to analyse the geographic correlates of P and H_o. The results of this analysis were consistent with the predictions of the time-divergence theory of variation, supporting the conclusion that directional selection is the main force eroding genetic variation on small islands. Intraspecific values of Nei 's (1972) standard genetic distance were relatively low in P. sicula (average D= 0.024), P. wagleriana (average D= 0.004), and P. filfolensis (average D= 0.012), while higher in P. raffonei (D= 0.040). The lizards from Pantellena Island, which were considered by BISCHOFF (1986) to be very similar to P. filfolensis from Malta on the basis of a superficial analysis of the coloration pattern, were shown to actually belong to P. sicula. This confirms that the range of P. filfolensis only includes the Maltese Archipelago, Linosa Island, and the islet of Lampione. Surprisingly, the samples of P. filfolensis from the Pelagie Islands (Linosa and Lampione) were very similar to those from the Maltese Archipelago (average D= 0.016). This could be explained by rafting or anthropogenic introduction of P. filfolensis on Linosa and Lampione. Podarcis wagleriana and P. raffonei were genetically related (average D= 0.152), confirming the results of previous electrophoretic investigations. Podarcis filfolensis, though showing some morphological affinity with P. wagleriana, was genetically highly differentiated from this latter species (average D= 0.526), while being more similar to P. sicula (average D= 0.306). This indicates a close relationship between P. sicula and P. filfolensis, suggesting that P. sicula and P. filfolensis probably diverged from a common ancestor, and that the apparent similarity between P. filfolensis and P. wagleriana could be merely due to morphological convergence.     

Sea lice escape predation on their host

Parasites seldom have predators but often fall victim to those of their hosts. How parasites respond to host predation can have important consequences for both hosts and parasites, though empirical investigations are rare. The exposure of wild juvenile salmon to sea lice (Lepeophtheirus salmonis) from salmon farms allowed us to study a novel ecological interaction: the response of sea lice to predation on their juvenile pink and chum salmon hosts by two salmonid predators-coho smolts and cut-throat trout. In approximately 70% of trials in which a predator consumed a parasitized prey, lice escaped predation by swimming or moving directly onto the predator. This trophic transmission is strongly male biased, probably because behaviour and morphology constrain female movement and transmission. These findings highlight the potential for sea lice to be transmitted up marine food webs in areas of intensive salmon aquaculture, with implications for louse population dynamics and predatory salmonid health.     

Characterization of microsatellite loci in the wall lizard Podarcis muralis (Sauria: Lacertidae)

In natural populations the mating success of males depends on different factors. By enhancing the intensity of secondary sexual characters, testosterone can play a role in mate choice. However, paradoxically, testosterone can also decrease immunocompetence and thus potentially diminish attractiveness. To estimate the influence of testosterone on male mating success in the wall lizard, Podarcis muralis, we characterized nine polymorphic microsatellite loci. There were three to 12 alleles per locus in the five to 16 individuals screened. These microsatellites will also be useful in determining population structure in this species.