Podarcis Lilfordi Research Articles

Predicting Spatial Patterns of Plant Recruitment Using Animal-Displacement Kernels

For plants dispersed by frugivores, spatial patterns of recruitment are primarily influenced by the spatial arrangement and characteristics of parent plants, the digestive characteristics, feeding behaviour and movement patterns of animal dispersers, and the structure of the habitat matrix. We used an individual-based, spatially-explicit framework to characterize seed dispersal and seedling fate in an endangered, insular plant-disperser system: the endemic shrub Daphne rodriguezii and its exclusive disperser, the endemic lizard Podarcis lilfordi. Plant recruitment kernels were chiefly determined by the disperser's patterns of space utilization (i.e. the lizard's displacement kernels), the position of the various plant individuals in relation to them, and habitat structure (vegetation cover vs. bare soil). In contrast to our expectations, seed gut-passage rate and its effects on germination, and lizard speed-of-movement, habitat choice and activity rhythm were of minor importance. Predicted plant recruitment kernels were strongly anisotropic and fine-grained, preventing their description using one-dimensional, frequency-distance curves. We found a general trade-off between recruitment probability and dispersal distance; however, optimal recruitment sites were not necessarily associated to sites of maximal adult-plant density. Conservation efforts aimed at enhancing the regeneration of endangered plant-disperser systems may gain in efficacy by manipulating the spatial distribution of dispersers (e.g. through the creation of refuges and feeding sites) to create areas favourable to plant recruitment.

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 po...

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

During encounters with predators, prey must balance the degree of risk against the loss of fitness-enhancing benefits such as feeding and social activities. Most studies of tradeoffs between risk and cost of escaping have measured flight initiation distance and time to emerge from refuge, for which theory provides robustly supported predictions. Tradeoffs involving other aspects of encounters, including distance fled and time between escape and return to a food source, have received little theoretical or empirical attention. By adapting models of flight initiation distance and time between entry into refuge and emergence, we predict effects of predation risk and cost on distance fled and time to return to a source of benefit after fleeing. Acting as simulated predators that approached at a fixed speed, we conducted an experimental field study to test the hypotheses that flight initiation distance, distance fled, and time to return to food by Balearic lizards (Podarcis lilfordi) decrease with the presence and amount of insect food. Predictions of the models were strongly supported, including those for distance fled and return time, but predictions for other cost factors and predation risk factors remain to be tested. Copyright 2006.

Disruption of a Plant‐Lizard Seed Dispersal System and Its Ecological Effects on a Threatened Endemic Plant in the Balearic Islands

Abstract: The introduction of exotic species to an island can have significant effects on the population density and distribution of native species and on the ecological and evolutionary interactions among them (e.g., plant‐animal mutualisms). The disruption of these interactions can be dramatic, significantly reducing the reproductive success of the species and even leading to their extinction. On Menorca Island (Balearic Islands, western Mediterranean), we examined the consequences of the disruption of the mutualism between two endemic species: a perennial shrub, ( Daphne rodriguezii [Texidor]) and a frugivorous lizard (Podarcis lilfordi [Günther]). The lizard became extinct from this island (as well as from Mallorca) as a result of the introduction of carnivorous mammals, which has continued since Roman times. The relict mutualism between D. rodriguezii and the lizard currently persists only in an islet (60 ha) where P. lilfordi is still abundant. We hypothesized that the absence of this lizard from most Menorcan populations is the factor causing the regression of this plant, currently considered at risk of extinction. Through observation and experimentation in the field and laboratory, we found strong evidence that a lack of seed dispersal in Menorca is the main cause of the low seedling recruitment. First, the population with greatest seedling recruitment was that in the islet where lizards were abundant. Second, lizards appeared to be the only dispersers of D. rodriguezii. Lizards consumed large amounts of fruits, without affecting either germination or seedling growth, and moved seeds to sites suitable for plant establishment. Seedlings in Menorca, in contrast, recruited almost exclusively under the parent plants. Third, the effect of other factors that may influence plant population growth (a low fruit set and a high postdispersal seed predation) was similar between the islet and the Menorcan populations. To our knowledge, our results are the first that quantitatively show that a biological invasion can cause a disruption of a specialized plant‐vertebrate mutualism that sets the plant partner on the road to extinction.

The lizard, Podarcis lilfordi (Squamata: Lacertidae) as a seed disperser of the Mediterranean plant, Phillyrea media (Oleaceae)

The phenomenon of saurochory (frugivory and seed dispersal by lizards) has been described from many island areas, such as the Caribbean Islands, Canary Islands, Balearic Islands, New Caledonia and New Zealand, as well as from some continental areas (South Africa and Central and South America, see review in Olesen and Valido, 2003).The knowledge of the interactions between frugivores and fruits is an important element for the conservation of endangered plants (Jordano, 2000; Kitamura et al., 2002), and the role of lizards as legitimate seed dispersers is well known in tropical habitats but few data exists as for temperate regions (Traveset, 1998). Herrera (1995) recognizes that seed dispersal by reptiles in Mediterranean ecosystems has not been extensively studied and that, according to the published literature, could be only relevant in insular habitats. Some data ara available for Lacerta lepida from Iberian Peninsula (Hernandez, 1990), Gallotia galloti and Gallotia atlantica from Canary Islands (Valido and Nogales, 1994) and Podarcis lilfordi from Balearic Islands (Saez and Traveset, 1995; Trav-

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 per...

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

AbstractCostly 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.

Cologne as a pungency control in tests of chemical discrimination: effects of concentration, brand, and simultaneous and sequential presentation

Cologne has been used extensively as a pungency control in experiments on chemosensory behavior to assess responses to an odorous, readily detectable stimulus that is irrelevant to the adaptive response being studied. However, undiluted cologne may be aversive, its effects might differ among brands, it might suppress responses to simultaneously presented chemical stimuli, and might affect subsequent responsiveness to other stimuli. We present experimental data showing that undiluted cologne can be aversive, but that aversion can be eliminated by dilution. We also show that the utility of cologne as a pungency control varies among brands, that cologne does not suppress responses to food chemicals in some species, but does in others, and that prior exposure to cologne does not affect later response to food chemicals. In 60 s swab trials with the Balearic lizard (Podarcis lilfordi), the main chemosensory responses were unaffected by cologne concentration. However, one-fourth of lizards exhibited slight to moderate aversion to undiluted cologne and 3:1 water:cologne, but not to a readily detected lower concentration (9:1). Two cologne brands did not affect responses, but a third brand induced increased tongue-flick rates. Colognes that stimulate increased tongue-flicking might mask real experimental effects. Cologne presented simultaneously with cricket chemicals did not affect tongue-flicking and biting responses in two species, but caused increased tongue-flicking in a third species and weaker response to cricket chemicals in a fourth. Prior testing with cologne did not affect responsiveness to cricket chemicals in a subsequent trial. Although cologne is a useful pungency control, pilot tests are needed to verify its utility for unstudied cologne types and animal species.

Behavioral responses to plant toxins by two omnivorous lizard species

An ability to detect plant toxins and thereby avoid eating chemically defended plants would be very beneficial for omnivorous and herbivorous lizards. We studied the ability of the omnivorous Podarcis lilfordi to detect compounds belonging to three classes of common plant toxins, as well as responses indicating aversion. Solutions of the alkaloid quinine, saponin, and the phenolic coumarin, as well as distilled water (odorless control), were presented to lizards on cotton swabs. The lizards detected all three toxins as indicated by significantly decreased tongue-flick rates and tongue-flick attack scores in comparison with distilled water. Several other variables revealed aversion to saponin, including a low number of individuals that bit swabs, avoidance of swabs after tongue-flicking, performance after tongue-flicking the swab of repeated short-excursion tongue-flicks that were directed away from the swab and did not contact any substrate, failure to respond at all in the next trial, and wiping the snout on the floor of the terrarium. Reasons for apparent differences in tongue-flicking behavior between P. lilfordi and two other omnivorous lizard species are discussed. We also showed experimentally that saponin depresses the tongue-flick rate in the omnivorous Bonaire whiptail lizard, Cnemidophorus murinus. Tongue-flicking enables at least one lizard species to detect specific chemicals representing three major classes of plant toxins. It is hypothesized that this ability is a widespread adaptation to reduce ingestion of plant toxins.

Responses by a generalist predator, the Balearic lizard Podarcis lilfordi , to chemical cues from taxonomically diverse prey

Specialist predators may respond strongly to sensory cues from preferred prey, but responses by generalist predators, although predicted to be less specific, are poorly known. Among squamate reptiles, diet and strength of response to chemical prey cues covary geographically in snakes that are specialist predators. There have been no previous studies of correspondence between diet and chemosensory response in lizards that are prey generalists. Actively foraging lizards discriminate between prey chemicals and control substances. It has been speculated that differential responses among prey species are unlikely in typical species that are dietary generalists. We examined this relationship in Podarcis lilfordi, an omnivorous lacertid that consumes a wide variety of animal prey. In experiments in which chemical stimuli were presented on cotton swabs, lizards responded more strongly to chemicals from a broad spectrum of prey types than to deionized water, an odorless control. These findings plus previous data showing that P. lilfordi is capable of prey chemical discrimination suggest that P. lilfordi can identify a wide range of potential prey using chemical cues. However, there was no evidence of differential response to stimuli among prey species, even in comparisons of prey included in the natural diet and potential prey not in the diet. The results, although limited to a single species, are consistent with the hypothesis that lizard species that are prey generalists do not exhibit the differential response strengths to chemical prey cues observed in snakes that have more specialized diets.

Responses to major categories of food chemicals by the lizard Podarcis lilfordi.

Many lizards are capable of identifying food using only chemical cues from food surfaces, but almost nothing is known about the types of compounds that are effective stimuli. We experimentally studied lingual and biting responses by a lacertid lizard, Podarcis lilfordi, to single representatives of three major categories of food chemicals, sucrose as a carbohydrate, pure pork fat as a mixture of lipids, and bovine gamma globulin as a protein. In 60-sec trials in which stimuli were presented on cotton swabs, the lizards detected all three stimuli, exhibiting more tongue-flicks, licks, or bites, or a greater tongue-flick attack score (TFAS; overall measure of response strength to prey stimuli) than to deionized water. The initial response to all stimuli was tongue-flicking, but the lizards discriminated among the types of chemical stimuli. After preliminary tongue-flicks, the lizards responded to sucrose solutions by licking at high rates, to pure pork fat by biting, and to protein by a combination of additional tongue-flicks and biting. Biting is a feeding response to prey or solid plant material. Licking is a feeding response to sugars in nectar or ripe fruit. Its frequency increased with sucrose concentration. Our data suggest that lizards can identify several types of chemicals associated with food and direct feeding attempts to sources of such chemicals in the absence of visual cues.

Lingual and biting responses to selected lipids by the lizard Podarcis lilfordi

Many lizards can identify food using chemical cues, but very little is known about the chemical constituents used for this purpose. We experimentally investigated responses to several lipid stimuli by the omnivorous lacertid lizard Podarcis lilfordi, which had been shown previously to be capable of identifying prey using only chemical cues and to respond to pork fat by tongue-flicking and biting. In 60-s trials in which stimuli were presented on cotton swabs, the lizards responded very strongly to pure pork fat and to oleic acid, but not to cholesterol or glycerol. Latency to bite swabs, the number of individuals that bit swabs, and the tongue-flick attack score, TFAS(R), which combines effects of tongue-flicks and bites, showed stronger responses to fat than to cholesterol, glycerol, and distilled water but did not differ significantly from responses to oleic acid. Several lines of evidence show that oleic acid elicited strong chemosensory and feeding responses. For individuals that did not bite, the number of tongue-flicks was significantly greater for oleic acid than for distilled water or glycerol, and nearly so for cholesterol. Latency to bite was significantly shorter for oleic acid than for distilled water, and TFAS(R) was significantly greater for oleic acid than for distilled water and glycerol. In combination with pilot data indicating no strong response to the waxy, saturated palmitic acid, these findings suggest that oleic acid in particular and probably other unsaturated fatty acids found in animal fat contribute strongly to the food-related responses to lipids.

Location of fruit using only airborne odor cues by a lizard

Although squamate reptiles are known to locate conspecifics by scent-trailing and to locate and identify prey by tongue-flicking substrates, an ability to locate food using only airborne cues has previously only been suspected based on observations that dead animals can be used as bait for Komodo dragons and that some nocturnal geckos aggregate on flowers. We conducted a simple field test of the ability of the omnivorous lizard Podarcis lilfordi to find fruit hidden under opaque cups. When a board having two identical cups spaced 1 m apart, one empty and the other hiding a freshly cut piece of apricot, was placed in the habitat, lizards first contacted the cup hiding fruit at well above chance frequency. Upon contact with a cup, lizards were significantly more likely to stay next to the cup, tongue-flick at high rates, climb the cup, and attempt to bite the cup if it hid a piece of apricot. The ability to follow a concentration gradient of airborne volatile chemicals to its source is very likely mediated by olfaction, but participation by or primacy of vomerolfaction cannot be excluded.

Insular interactions between lizards and flowers: flower visitation by an endemic Mauritian gecko

Lizards mainly eat arthropods, fruit, nectar, pollen and animal scats (Pérez-Mellado & Casas 1997, Whitaker 1987), using their sense of smell and good colour vision while foraging (Vinson & Vinson 1969). Although several papers have contributed to the knowledge on the relationship between lizards and floral resources, this topic is often still regarded as anecdotal. However, a few detailed ecological studies on lizard and flower interactions have been conducted, e.g. in New Zealand and the Balearic Isles (Eifler 1995, Sáez & Traveset 1995, Traveset & Sáez 1997,Whitaker 1987). Pollination by lizards was rendered likely by the following findings: first, Mediterranean lacertid lizards and New Zealand geckos have pollen adhering to their belly, throat and labium; second, they may carry pollen for several hours, and thus also transport pollen some distance away from a pollen donor plant. New Zealand geckos carry pollen up to 72 m away from donors. Good experimental evidence of lizard pollination was produced by Pérez-Mellado & Casas (1997). They showed that an umbellifer species produced less viable seeds if Podarcis lilfordi lizards were excluded from flowers.

Food chemical cues elicit general and population‐specific effects on lingual and biting behaviors in the lacertid lizard Podarcis lilfordi

Actively foraging lizards are capable of identifying prey using only chemical cues sampled by tongue-flicking, and the relatively few omnivorous and herbivorous lizards tested similarly can identify both animal and plant foods from chemical cues. Whether lizards that eat plants respond to cues specific to preferred plant types and whether there is geographic variability in responses to cues from various plants correlated with the importance of those plants in local diets is unknown. In three populations of an omnivorous lacertid, the Balearic lizard Podarcis lilfordi, we studied chemosensory sampling and feeding responses to chemical cues from plant and animal foods presented on cotton swabs. Each lizard population is endemic to one islet off the coast of Menorca, Balearic Islands, Spain. Lizards in all three populations discriminated chemical cues from plant and animal foods from control substances. Our results extend findings of prey chemical discrimination and plant chemical discrimination in omnivores, increasing confidence that correlated evolution has occurred between plant diet and chemosensory response to palatable plants. There were no consistent differences among populations in tongue-flicking and biting responses to stimuli from flowers of syntopic and allopatric plant species. The lizards may respond to cues indicative of palatability in a wide range of plant species rather than exhibiting strong responses only to locally available plant species. Nevertheless, tongue-flicking and biting frequencies varied among plant species, perhaps indicating food preferences. In addition, there were differences among populations in tongue-flick rates, latency to bite, and licking behavior. Licking was observed in only one lizard population as a response to floral chemicals from only one of the plants species tested, raising the possibility of a population-specific linkage between identification of a particular plant species and performance of an appropriate feeding response.

Reproductive Characteristics of the Island Lacertid Lizard Podarcis lilfordi

We report reproductive characteristics (clutch frequency, clutch size, egg and hatchling sizes) of the island lizard Podarcis lilfordi, studied in the laboratory. Individual females produced two or three consecutive clutches, composed of 2-4 eggs with an average mass of 0.63 g. Both clutch size and average egg mass were independent of female body length, and did not differ between the first and subsequent annual clutches. Among-clutch differences in egg mass were negatively correlated with clutch size, and this trade-off is independent of female size. Larger clutches were also composed of less elongated (i.e, rounder) eggs than are smaller clutches, suggesting that limitations posed by the females' body volume, rather than by restrictions of energy availability, induce the phenotypic trade-off between egg size and numbers. Egg shape was also related to female size: larger females laid shorter but wider eggs than smaller individuals, suggesting that egg width is constrained by the width of the female's pelvic girdle. Relative to other Eu- ropean lacertids with similar adult female body length, P lilfordi produces clutches that are composed of very few, but extremely large eggs. Comparative studies of life histories explore patterns of covariation among life history char- acteristics and search for relationships between trait complexes and ecological conditions. Many studies address these issues in reptiles, espe- cially lizards (e.g., Tinkle, 1969; Tinkle et al., 1970; Dunham and Miles, 1985; Dunham et al.,

Does passage time through the lizard Podarcis lilfordi’s guts affect germination performance in the plant Withania frutescens?

I tested predictions of the hypothesis that a longer seed passage time through the gut of the lizard Podarcis lilfordi enhances germination performance in the plant Withania frutescens. I compared germination success and germination time between seeds that were ingested by lizards and control seeds that were not. I also explored relationships between natural variation in seed passage time and germination performance. Germination success did not differ between ingested (63 %) and non-ingested seeds (56 %); there was no significant relationship between germinability and retention time. Germination time did not differ between ingested and non-ingested seeds, and was unrelated to retention time. Hence, I found no support for the hypothesis that prolonged retention times should improve germination performance. In addition, this is a pilot study stressing the importance of reptiles as seed dispersers, at least in certain habitats. © 2000 Editions scientifiques et medicales Elsevier SAS

POLLEN LOAD AND TRANSPORT BY THE INSULAR LIZARD, PODARCIS LILFORDI (SQUAMATA, LACERTIDAE) IN COASTAL ISLETS OF MENORCA (BALEARIC ISLANDS, SPAIN)

An analysis of pollen grains loaded and transported by the Balearic lizard, Podarcis lilfordi, at three coastal islets of Menorca (Balearic Islands, Spain) was performed. We studied 228 individual lizards from spring and summer, 1998, recording 323,986 pollen grains belonging to 35 different plant species. As a consequence of its foraging behavior, the Balearic lizard is able to load large quantities of pollen. In Aire Island pollen load was higher in adult females than males. P. lilfordi is an important pollen loader of some plant species such as Pistacia lentiscus, Crithmum maritimum, Allium ampeloprasum, Carlina corymbosa, and Pancratium maritimum. The role of P. lilfordi as the main pollinator has been previously demonstrated only for the sea fern, C. maritimum. However, results reported here indicate that the Balearic lizard can play an important role in the reproductive success of other plant species on coastal islets off the main island of Menorca.

Podarcis lilfordi from the Balearic islands as a potential disperser of the rare Mediterranean plant Withania frutescens

This study examines whether the lizard Podarcis lilfordi is a legitimate disperser of the rare Mediterranean plant Withania frutescens by using the biochemical test of triphenyl-2H-tetrazolium chloride for testing seed viability. This lizard eats the fresh fruits of the plants and defecates intact seeds which have been retained 1 to 3 d in their gut. Viability of seeds recovered from faeces was very high and comparable to the viability of fresh seeds. Seed dispersal by this lizard in the Balearic islands may facilitate population expansion of this rare plant in the Balearics.

Ontogenetic, Sexual, and Microgeographic Variation in Color Pattern within a Population of the Lizard Podarcis lilfordi

Ontogenetic, Sexual, and Microgeographic Variation in Color Pattern within a Population of the Lizard Podarcis lilfordi