Valentín Pérez-Mellado

Ease and effectiveness of costly autotomy vary with predation intensity among lizard populations

Costly anti-predatory defences are used in ecological time and maintained in evolutionary time by natural selection favouring individuals that survive through their use. Autotomy of expendable body parts is a striking example of a defence having multiple substantial costs, including loss of ability to use the same defence, loss of energy, and decreased growth, reproductive success and survival following autotomy, plus the energetic cost of replacing the lost body part in species capable of regenerating them. Our study shows that autotomy in the lacertid lizard Podarcis lilfordi reduces sprint speed, indicating decreased capacity to escape as well as the loss of energy. Autotomy carries substantial cost, and thus should be avoided except as a last resort. Ease of autotomy and post-autotomic movements were studied in three populations of lacertid lizards. Two were islet populations of P. lilfordi from Aire (lowest predation pressure) and Colom (intermediate predation pressure) off Minorca. The third was a mainland population of Podarcis hispanica , a closely related species from the mainland of the Iberian Peninsula where predation pressure is higher than on the islets. As predicted, a suite of autotomic traits increases the effectiveness of autotomy as a defence as predation pressure increases. With increasing predation pressure, the frequency of voluntary autotomy increases, latency to autotomy decreases, pressure on the tail needed to induce autotomy decreases, vigour of post-autotomic tail movements increases, and distance moved by the shed tail increases. Additional changes that might be related to predation pressure, but could have other causes, are the presence of tail coloration contrasting with body coloration except under the lowest predation pressure (Aire) and longer tails in the mainland species P. hispanica . Correspondence between predation pressure and the suite of autotomic traits suggests that autotomy is an important defence that responds to natural selection. Comparative data are needed to establish the generality of relationships suggested in our study of only three populations.

Bayesian estimation of post-Messinian divergence times in Balearic island lizards

Phylogenetic relationships and timings of major cladogenesis events are investigated in the Balearic Island lizards Podarcislilfordi and P.pityusensis using 2675bp of mitochondrial and nuclear DNA sequences. Partitioned Bayesian and Maximum Parsimony analyses provided a well-resolved phylogeny with high node-support values. Bayesian MCMC estimation of node dates was investigated by comparing means of posterior distributions from different subsets of the sequence against the most robust analysis which used multiple partitions and allowed for rate heterogeneity among branches under a rate-drift model. Evolutionary rates were systematically underestimated and thus divergence times overestimated when sequences containing lower numbers of variable sites were used (based on ingroup node constraints). The following analyses allowed the best recovery of node times under the constant-rate (i.e., perfect clock) model: (i) all cytochrome b sequence (partitioned by codon position), (ii) cytochrome b (codon position 3 alone), (iii) NADH dehydrogenase (subunits 1 and 2; partitioned by codon position), (iv) cytochrome b and NADH dehydrogenase sequence together (six gene-codon partitions), (v) all unpartitioned sequence, (vi) a full multipartition analysis (nine partitions). Of these, only (iv) and (vi) performed well under the rate-drift model. These findings have significant implications for dating of recent divergence times in other taxa. The earliest P.lilfordi cladogenesis event (divergence of Menorcan populations), occurred before the end of the Pliocene, some 2.6Ma. Subsequent events led to a West Mallorcan lineage (2.0Ma ago), followed 1.2Ma ago by divergence of populations from the southern part of the Cabrera archipelago from a widely-distributed group from north Cabrera, northern and southern Mallorcan islets. Divergence within P.pityusensis is more recent with the main Ibiza and Formentera clades sharing a common ancestor at about 1.0Ma ago. Climatic and sea level changes are likely to have initiated cladogenesis, with lineages making secondary contact during periodic landbridge formation. This oscillating cross-archipelago pattern in which ancient divergence is followed by repeated contact resembles that seen between East-West refugia populations from mainland Europe.

TRADEOFFS BETWEEN ESCAPE BEHAVIOR AND FORAGING OPPORTUNITY BY THE BALEARIC LIZARD (PODARCIS LILFORDI)

Optimal escape theory predicts that prey permit closer approach by predators when fleeing is more costly, but does not predict other aspects of escape such as distance fled or the likelihood of returning to the initial site in the presence or absence of a resource such as food. Because a lizard preparing to feed may lose the feeding opportunity, optimal escape theory predicts that the lizard should allow a predator to approach closer before fleeing when a stationary food source is present than in its absence. In addition, we predicted that when a predator was nearby, lizards would flee a shorter distance and return more often when food was present than absent. We presented adult males of the omnivorous Balearic lizard, Podarcis lilfordi, with a tethered piece of pear or a pebble of similar size and shape. One of us approached a lizard in a standardized manner, stopping and remaining still when the lizard fled. The other investigator recorded escape and return behaviors. Lizards in the presence of food permitted closer approach before fleeing, fled a substantially shorter distance, and were far more likely to return to the site of stimulus presentation than when a pebble was presented. These findings suggest that prey may alter several aspects of escape behavior to reduce costs due to lost opportunities, and present a likelihood that interspecific variation exists in the combination of aspects of antipredatory behavior that are modified.

Population density in Podarcis lilfordi (Squamata, Lacertidae), a lizard species endemic to small islets in the Balearic Islands (Spain)

The Balearic lizard, Podarcis lilfordi , is present in 43 insular populations in the Cabrera archipelago and around the coasts of Mallorca and Menorca islands (Spain). We studied lizard densities over the entire range of distribution, analyzing observed differences of density in relation to island area, habitat diversity, availability of resources, presence of predators, competitors and human disturbances. The density of the Balearic lizard varies from less than 35 to almost 8000 lizards ha –1 , with an average of around 1500 lizards ha –1 . In some very small islets we detected no more than 10 individuals. Using a subsample of nine coastal islets (Menorca) we did not find any significant correlation between ground arthropod biomass and lizard density. The combination of island area and its maximal altitude, its so-called biotic capacity, was also uncorrelated with lizard density. In addition, neither degree of island accessibility nor presence/absence of seagull breeding colonies, were able to explain lizard densities. Islands without ship rats ( Rattus rattus ) showed a significantly higher lizard density, but islands in which rat eradication programs were launched during the study period, showed lower densities than those with rats but no eradication actions. Genetic variability was significantly higher on bigger lizard populations, lacking a correlation with lizard densities. No single independent variable can explain density differences among populations under study. Our results are discussed in the light of available hypotheses on factors affecting population densities.

Ecological Energetics and Food Acquisition in Dense Menorcan Islet Populations of the Lizard Podarcis lilfordi

1. Ecological energetics and water fluxes were compared between populations of the lacertid lizard Podarcis lilfordi from the Menorcan islets of Aire and Nitge (Balearic Islands, Spain) during a non-reproductive summer period using the doubly labelled water technique. 2. Lizards from Aire were larger than those from Nitge (9.6 ± 0.58 g vs 5.1 ± 0.38 g, respectively) and consequently had higher field metabolic rates (FMR) (1.739 ± 0.151 KJ day −1 vs 1.255 ± 0.977 kJ day −1 ). 3. FMR were lower in the Aire population, when the effects of the differing body masses were removed. 4. There were substantial differences in food availabilities between the two islets and this was reflected in strong dietary differences between the lizard populations

Change your diet or die: predator-induced shifts in insectivorous lizard feeding ecology

Animal feeding ecology and diet are influenced by the fear of predation. While the mechanistic bases for such changes are well understood, technical difficulties often prevent testing how these mechanisms interact to affect a mesopredator’s diet in natural environments. Here, we compared the insectivorous lizard Acanthodactylus beershebensis’ feeding ecology and diet between high- and low-risk environments, using focal observations, intensive trapping effort and fecal pellet analysis. To create spatial variation in predation risk, we planted “artificial trees” in a scrubland habitat that lacks natural perches, allowing avian predators to hunt for lizards in patches that were previously unavailable to them. Lizards in elevated-risk environments became less mobile but did not change their microhabitat use or temporal activity. These lizards changed their diet, consuming smaller prey and less plant material. We suggest that diet shifts were mainly because lizards from risky environments consumed prey items that required shorter handling time.

Islet tameness: escape behavior and refuge use in populations of the Balearic lizard (Podarcis lilfordi) exposed to differing predation pressure

Prey often exhibit reduced escape behavior on islands where predators are absent or scarce. Models of escape and refuge use predict that prey from populations having lower predation pressure have shortened flight initiation distance (FID; distance between a predator and a prey when escape begins), reduced distance fled and tendency to enter refuge, and shortened hiding time before emerging from refuge. By ourselves simulating approaching predators, we tested these predictions for two populations of the Balearic lizard, Podarcis lilfordi (Muller, 1927), on the islets of Rei (higher preda- tion pressure) and Aire (lower) adjacent to Menorca. FID, distance fled, and hiding time were shorter and probability of entering refuge was lower on Aire than on Rei, confirming all predictions. All effect sizes were large, indicating major dif- ferences in antipredatory behavior between islets. These findings are consistent with data for other lizards on FID and lim- ited data on distance fled and refuge entry. The effect of predation pressure on hiding time is a novel finding. Our results and those of previous studies suggest that relaxation of predation pressure leads to reduced natural selection for mainte- nance of antipredatory behavior at all stages of predator-prey interactions over a relatively short time span.

Effects of Predation Risk Factors on Escape Behavior by Balearic Lizards (Podarcis lilfordi) in Relation to Optimal Escape Theory

Escape theory predicts that flight initiation distance (FID = predator-prey distance when escape begins) increases as predation risk increases. We tested effects of variation of approach speed and directness, predator persistence, concealment, and weather conditions on FID in the Balearic lizard (Podarcis lilfordi) by ourselves simulating predators. We examined effects of directness of approach on probability of fleeing and of repeated approach on entering refuge and distance fled. As predicted, FID was greater for faster approach speed, more direct approach, during second than first approaches, and when lizards were exposed than partially concealed. Other effects of directness of approach and repeated approach also were as predicted by greater assessed risk by the lizards. The proportion of individuals that fled was greater for direct than indirect approaches. The proportion of lizards that entered refuges and distance fled were greater during the second of two successive approaches. Effects of weather on FID were complex. FID was shortest in the warmest conditions with no noticeable wind, when lizards were active. Lizards were inactive and basked in the other conditions. FID was longest at 20°C without wind, and intermediate FID occurred at 18°C in windy conditions. We present hypotheses for weather effects. Tests are needed to unravel effects of temperature and wind speed. All predictions of escape theory for simple risk factors, i.e., all except than weather conditions, were confirmed. Escape theory successfully predicts FID for these risks in P. lilfordi, other lacertids, and more broadly, in ecologically and taxonomically diverse lizards.

Using faecal samples in lizard dietary studies

While the use of faecal pellets is widely accepted as a primary methodological source of data for dietary studies, a recent paper advocated for the use of gut contents. This was due to the fact that faecal samples would give biased results of the diet of arthropod predators, due to a lower representation of soft-bodied prey in faecal pellets. To test this assumption, we compared the spring diet of several populations of two insular lizards from the Balearic Islands (Spain), Podarcis lilfordi and Podarcis pityusensis, using both faecal pellets and gut contents. Our results do not support the supposed bias of dietary analyses based on faecal pellets. Indeed, soft-bodied prey and particularly insect larvae are often equally represented in faecal pellets and gut contents. Alternatively, soft bodied prey are represented in different proportions in gut contents and faecal pellets, but in some cases with higher proportions being observed in the gut contents, and in other cases with higher proportions in faecal samples. We conclude that faecal pellets can be a reliable source of information for dietary studies.

Number, speeds, and approach paths of predators affect escape behavior by the balearic lizard, Podarcis lilfordi

Abstract The number of simultaneously attacking simulated predators and their approach speeds and angles affected escape trajectories and flight initiation distance in Balearic Lizards (Podarcis lilfordi). Our findings confirmed predictions prey flee in directions maximizing distance from predator(s). During slow approaches, escape angle was 45° when approached by two predators at right angles and 90° when approached from opposite directions. Escape at close to 45° by lizards approached at slower speed by a single predator supports the hypothesis that prey use escape trajectories allowing them to visually monitor predators. Flight angles were closer to being straight away from a predator during faster approaches, suggesting that distance maximization may be more important than monitoring predator position when risk is great. When predators approached from opposite directions, flight angle shifted away from the faster predator, suggesting that lizards may have equalized risk from both predators based on positions and speeds. Flight initiation distance was greater for approach by predators side by side than by one only during faster approaches, suggesting that risk is a joint function of predator number and speed. Flight initiation distance was greater when predators approached at right angles than side by side, perhaps because of difficulty of monitoring multiple predators in different locations. Distance fled did not differ among treatments and may have been affected by distance to refuge. Thus, Balearic Lizards adjusted flight initiation distance and escape trajectories in ways that enhanced their abilities to avoid predation during simultaneous approaches by two predators.