Adaptive variation in the development of extraembryonic membranes of gekkotan embryos: A meta-analytical approach.

Highly mineralized rigid-shelled eggs characterize one lineage of gekkotans. In contrast, poorly mineralized flexible-shelled eggs characterize basal lineages of gekkotans and all other squamates. Low oxygen permeability of rigid-shelled eggs is associated with small eggs and hatchlings, and long incubation lengths compared to flexible-shelled gekkotan eggs. These features represent a demographic cost for species with rigid-shelled eggs. This cost is offset, at least in part, because mortality due to desiccation and predation is reduced for rigid-shelled eggs relative to flexible-shelled eggs. Developmental traits may also compensate for the low oxygen permeability of rigid-shelled eggs. Oviposition, for example, occurs at earlier developmental stages for gekkotans with rigid- versus flexible-shelled eggs. Such early oviposition facilitates development because eggs move from the relatively hypoxic oviduct to the much better oxygenated nest environment. In this study, I tested the hypothesis that the growth of the yolk sac (YS) and chorioallantoic membrane (CAM) of gekkotans with rigid-shelled eggs is initiated and completed earlier than those of gekkotans with flexible-shelled eggs. I measured the surface area of eggs covered by the YS and CAM from oviposition to hatching and determined which of four nonlinear models provide the best fit for growth curves. I also compiled a data set on embryonic metabolism of gekkotans and other lizards in order to place growth of the YS and CAM in the context of energy utilization of lizard embryos overall. Growth of the YS and CAM of gekkotans with rigid-shelled eggs is accelerated relative to that of gekkotans with flexible-shelled eggs and may serve to separate the cost of YS and CAM development from that of the embryo itself. Adaptive variation in YS and CAM development may extend to birds, crocodilians, and turtles as they also exhibit life history variation that affects oxygen availability to embryos during development.

Agricultural land use creates evolutionary traps for nesting turtles and is exacerbated by mercury pollution.

The rate of anthropogenic habitat conversion often exceeds the rate of natural ecological and evolutionary processes, which sometimes creates mismatches between environmental cues and adaptive behaviors. In numerous species of aquatic turtles, nest site selection is primarily based on cues related to high solar exposure, which leads females to select sites where humans have disturbed habitat. These disturbed sites are often contaminated by pollutants, such as mercury. Despite the fact that anthropogenic disturbances often co-occur, few studies have examined the interactive influence of major global changes on animal development. Using Chelydra serpentina, we investigated the individual and interactive effects of crop agriculture and mercury pollution on hatch success and offspring phenotype. We hypothesized that following nesting, rapid crop growth would shade and cool nests in agricultural fields and subsequently negatively impact embryonic development. Agricultural and control nests were similar in temperature at the time of oviposition, but temperatures diverged as crops grew: agricultural nests averaged 2.5°C cooler than control nests over the course of incubation. In laboratory and field experiments, we found that turtles incubated under agricultural thermal regimens took longer to hatch, hatched at smaller body sizes, lost more mass, and had lower posthatching growth rates. Additionally, thermal conditions associated with agricultural land use interacted with mercury contamination to decrease hatching success. To our knowledge, this is the first documentation of negative interactive effects of mercury pollution and habitat quality on early vertebrate development and highlights the importance of examining the combined influence of anthropogenic global changes on organisms.

Developmental plasticity in reptiles: Insights into thermal and maternal effects on chameleon phenotypes.

Embryonic environments affect a range of phenotypic traits including sex and reproductive success. I determined (1) how the interaction between incubation temperature and egg size affects sex allocation of Chamaeleo calyptratus and (2) how incubation temperature and maternal parent (clutch) affect water uptake by eggs and body size, growth, and climbing speed of hatchlings and juveniles. Eggs from five clutches were exposed to five temperature treatments with clutches replicated within and among treatments. Temperature affected sex, but only when egg size was included as a factor in analyses. At intermediate (28°C) temperatures, daughters were more likely to be produced from large eggs and sons more likely to be produced from small eggs, while at 25 and 30°C, the pattern of sex allocation was reversed. Temperature and clutch affected water uptake and body size. Nonetheless, the direction of temperature and clutch effects on water uptake by eggs and on the size of hatchlings were not the same and the direction of temperature effects on body sizes of hatchlings and juveniles differed as well. Clutch affected hatchling size but not juvenile size and growth rate. Clutch, but not incubation temperature, affected climbing speed, but the fastest hatchlings were not from the same clutches as the fastest juveniles. The independent effects of incubation temperature and clutch indicate that hatchling phenotypes are influenced largely by conditions experienced during incubation, while juvenile phenotypes are influenced largely by conditions experienced in the rearing environment.

Developmental origin of limb size variation in lizards.

In many respects, reptile hatchlings are fully functional, albeit miniature, adults. This means that the adult morphology must emerge during embryonic development. This insight emphasizes the connection between the mechanisms that generate phenotypic variation during embryonic development and the action of selection on post-hatching individuals. To determine when species-specific differences in limb and tail lengths emerge during embryonic development, we compared allometric patterns of early limb growth of four distantly related species of lizards. The major questions addressed were whether early embryonic limb and tail growth is characterized by the gradual (continuous allometry) or by the abrupt emergence (transpositional allometry) of size differences among species. Our observations supported transpositional allometry of both limbs and tails. Species-specific differences in limb and tail length were exhibited when limb and tail buds first protruded from the body wall. Genes known to be associated with early limb development of tetrapods are obvious targets for studies on the genetic mechanisms that determine interspecific differences in relative limb length. Broadly comparative studies of gene regulation would facilitate understanding of the mechanisms underlying adaptive variation in limb size, including limb reduction and loss, of squamate reptiles.

Rigid shells enhance survival of gekkotan eggs.

The majority of lizards and snakes produce permeable parchment-shelled eggs that require high moisture conditions for successful embryonic development. One clade of gekkotan lizards is an exception; females produce relatively impermeable rigid-shelled eggs that normally incubate successfully under low moisture conditions. I tested the hypothesis that the rigid-shell increases egg survival during incubation, but only under low moisture conditions. To test this hypothesis, I incubated rigid-shelled eggs of Chondrodactylus turneri under low and under high moisture conditions. Eggs were incubated with parchment-shelled eggs of Eublepharis macularius to insure that incubation conditions were suitable for parchment-shelled eggs. Chondrodactylus turneri eggs had very high survival (>90%) when they were incubated under low moisture conditions. In contrast, eggs incubated under high moisture conditions had low survival overall, and lower survival than those of the parchment-shelled eggs of E. macularius. Mortality of C. turneri and E. macularius eggs incubated under high moisture conditions was the result of fungal infection, a common source of egg mortality for squamates under laboratory and field conditions. These observations document high survival of rigid-shelled eggs under low moisture conditions because eggs escape from fungal infection. Highly mineralized rigid shells also make egg survival independent of moisture availability and may also provide protection from small invertebrates in nature. Enhanced egg survival could thus compensate for the low reproductive output of gekkotans that produce rigid-shelled eggs.

Long-term data reveal a population decline of the tropical lizard Anolis apletophallus, and a negative affect of el nino years on population growth rate.

Climate change threatens biodiversity worldwide, however predicting how particular species will respond is difficult because climate varies spatially, complex factors regulate population abundance, and species vary in their susceptibility to climate change. Studies need to incorporate these factors with long-term data in order to link climate change to population abundance. We used 40 years of lizard abundance data and local climate data from Barro Colorado Island to ask how climate, total lizard abundance and cohort-specific abundance have changed over time, and how total and cohort-specific abundance relate to climate variables including those predicted to make the species vulnerable to climate change (i.e. temperatures exceeding preferred body temperature). We documented a decrease in lizard abundance over the last 40 years, and changes in the local climate. Population growth rate was related to the previous years' southern oscillation index; increasing following cooler-wetter, la niña years, decreasing following warmer-drier, el nino years. Within-year recruitment was negatively related to rainfall and minimum temperature. This study simultaneously identified climatic factors driving long-term population fluctuations and climate variables influencing short-term annual recruitment, both of which may be contributing to the population decline and influence the population's future persistence.

Developmental sequences of squamate reptiles are taxon specific.

Recent studies in comparative vertebrate embryology have focused on two related questions. One concerns the existence of a phylotypic period, or indeed any period, during development in which sequence variation among taxa is constrained. The second question concerns the degree to which developmental characters exhibit a phylogenetic signal. These questions are important because they underpin attempts to understand the evolution of developmental characters and their links to adult morphology. To address these questions, we compared the sequence of developmental events spanning the so-called phylotypic period of vertebrate development in squamate reptiles (lizards and snakes), from the formation of the primary optic placode to the first appearance of scale anlagen. We used Bayesian phylogenetic ancestral state reconstruction analyses and estimates of Bayesian posterior probabilities of the rank order of developmental events to determine the level of support for phylogenetically associated variation in development. We assessed the amount of variation in event sequences by plotting the proportions of reconstructed ranks (excluding unlikely events, PP < 0.05) associated with each event. Sequence variability was the lowest towards the middle of the phylotypic period and involved three events (allantois contacts chorion, maximum number of pharyngeal slits, and appearance of the apical epidermal ridge [AER]); these events each had only two reconstructed ranks. Squamate clades also differed in the rank order of developmental events. Of the 20 events in our analyses, 12 had strongly supported (PP ≥ 0.95) sequence ranks that differed at two or more internal nodes of the tree. For example, gekkotans are distinguished by the late appearance of the allantois bud compared to all other squamates (ranks 7 and 8 vs. rank 3, respectively) and Serpentes are distinguished by the earlier completion of torsion (rank 3) compared to acrodonts and pleurodonts (ranks 7 and 5, respectively). Clade specific sequences of developmental events mean that investigators should not extend observations on the development on particular squamate species to distantly related taxa for use in comparative studies.

Does low gas permeability of rigid-shelled gekkotan eggs affect embryonic development?

Parchment-shelled eggs are characteristic of most squamates, including the basal clades of gekkotan lizards. The majority of gekkotan lizards, however, produce rigid-shelled eggs that are highly impermeable to gas exchange; eggs are laid in dry sites and experience a net loss of water during incubation. We tested the hypothesis that the 1,000-fold lower rate of oxygen diffusion through the shells of rigid- compared to parchment-shelled eggs imposes a physiological cost on development. To do this, we contrasted species with rigid and with parchment shells with regards to (1) rates of embryonic metabolism and (2) rates and patterns of development of the yolk sac and chorioallantois, the vascularized extra-embryonic membranes that transport oxygen to embryonic tissues. Metabolic rates of embryos from the rigid-shelled eggs of Gehyra variegata did not differ from those of the parchment-shelled eggs of Oedura lesueurii. Moreover, maximum metabolic rates of gekkotans with rigid shells did not differ from those of gekkotan or scincid lizards with parchment shells. In contrast, the yolk sac covered more of the surface area of the egg at oviposition, and the chorioallantois reached its full extent earlier for the species with rigid shelled eggs (Chondrodactylus turneri, G. variegata) than for the species with parchment-shelled eggs (Eublepharis macularius, O. lesueurii). Differences in the temporal patterns of yolk sac and chorioallantois development would thus serve to compensate for low rates of oxygen diffusion through rigid shells of gekkotans.

Water vapor permeability of the rigid-shelled gecko egg.

The vast majority of squamate reptiles (lizards and snakes) produce parchment-shelled eggs that absorb water during incubation, and thus increase in mass, volume, and surface area. In contrast, females from a single monophyletic lineage of gekkotan lizards produce rigid-shelled eggs. These eggs are functionally comparable to those of birds, that is, at oviposition, eggs contain all the water needed for development, and their mass decreases during incubation via the diffusion of water vapor through the shell. I determined patterns of water loss and shell permeability to water vapor from oviposition to hatching for the rigid-shelled eggs of the gekkonid Chrondrodactylus turneri and compared permeability of C. turneri eggs to those of birds and other squamates. Chrondrodactylus turneri eggs incubated at 28.5°C and 40% relative humidity (RH) decreased in mass by 14% over the course of a 68-day incubation period. The rate of water loss varied during incubation; egg mass decreased rapidly during the first 8 days of incubation, declined at a low constant rate during the next 35 days, and then decreased rapidly during the final 25 days of incubation. Overall permeability was 0.17 mg/day/kPa/cm(2) . Percent water loss of rigid-shelled gecko eggs during incubation is similar to that exhibited by birds, but water vapor permeability is about one-third that of bird eggs and several orders of magnitude lower than that of parchment-shelled squamate eggs. In general, the water economy of their eggs may be associated with the adaptive radiation of the rigid-shelled sphaerodactylid, phyllodactylid, and gekkonid geckos.

Eggs under pressure: components of water potential of chameleon eggs during incubation.

Water exchange of squamate eggs is driven by the difference between the water potentials of eggs and of their nest environment. While osmotic potential is generally assumed to dominate the net water potential of eggs, resistance of the eggshell to stretching also affects egg water potential. We therefore determined osmotic potentials and pressure potentials (mechanical pressure) of eggs of the veiled chameleon Chamaeleo calyptratus over the course of incubation. Because embryos are diapausing gastrulae when eggs are laid and diapause persists several months, the water potential of eggs can be evaluated before it is influenced by the developing embryo. Water uptake during the first 2 wk of incubation was rapid as a result of the large difference between the total water potential of the egg (-848 kPa) and that of its incubation substrate. After about 2 wk, water potential of the egg stabilized at -460 kPa. By day 80 of incubation, the developing embryo and allantois affected water exchange of the egg. The allantoic fluid was initially very dilute, but its osmotic potential decreased to about -200 kPa by the end of incubation. Pressure potential of the egg averaged 25 kPa, with no systematic trend during incubation. The pressure potential exerted by the eggshell reduced the difference between the water potential of the egg and the water potential of the environment, that is, the ability of eggs to take up water. At the time of oviposition, this effect was relatively small, producing a 4%-6% reduction in water potential difference. Once the yolk osmotic potential stabilized, however, the reduction was 12% or more. This observation means that the dynamics of water uptake by squamate eggs cannot be fully understood without consideration of the pressure that is exerted on the contents of eggs by their shells.

Effects of incubation temperature on growth and performance of the veiled chameleon (Chamaeleo calyptratus).

I evaluated the effect of incubation temperature on phenotypes of the veiled chameleon, Chamaeleo calyptratus. I chose this species for study because its large clutch size (30-40 eggs or more) allows replication within clutches both within and among experimental treatments. The major research objectives were (1) to assess the effect of constant low, moderate, and high temperatures on embryonic development, (2) to determine whether the best incubation temperature for embryonic development also produced the "best" hatchlings, and (3) to determine how a change in incubation temperature during mid-development would affect phenotype. To meet these objectives, I established five experimental temperature regimes and determined egg survival and incubation length and measured body size and shape, selected body temperatures, and locomotory performance of lizards at regular intervals from hatching to 90 d, or just before sexual maturity. Incubation temperature affected the length of incubation, egg survival, and body mass, but did not affect sprint speed or selected body temperature although selected body temperature affected growth in mass independently of treatment and clutch. Incubation at moderate temperatures provided the best conditions for both embryonic and post-hatching development. The highest incubation temperatures were disruptive to development; eggs had high mortality, developmental rate was low, and hatchlings grew slowly. Changes in temperature during incubation increased the among-clutch variance in incubation length relative to that of constant temperature treatments.

Developmental arrest during embryonic development of the common chameleon (Chamaeleo chamaeleon) in Spain.

Embryonic development of the common chameleon, Chamaeleo chamaeleon, was monitored from oviposition to hatching at a field site in southwestern Spain and in the laboratory under five experimental temperature regimes. Embryos were diapausing gastrulae at the time of oviposition; developmental arrest in the field continued as cold torpor during winter. Postarrest development in the field commenced in April, and hatching occurred in August, for a total incubation period of 10.5 mo. In the laboratory, one group of eggs was incubated at a constant warm (26 degrees C) temperature. The remaining treatments simulated field conditions and consisted of initial periods of warm temperature of 0, 27, 46, and 71 d, a subsequent 4-mo period of cold winter (16 degrees C) temperature, and a final period of warm (26 degrees C) temperature. Embryos in the constant warm temperature treatment were in diapause an average of 3 mo, with clutch means ranging from 2 to 4 mo. Hatching among clutches occurred over 2 mo. In contrast, for field and experimental eggs that experienced cold winter conditions, hatching within treatments occurred over 2-14 d; "winter" conditions synchronized development. The length of time between the end of cold conditions and hatching did not differ among treatments; development thus resumed as soon as temperature was suitable regardless of the initial period of warm temperature. Diapause in nature thus insures that embryos remain gastrulae after oviposition despite nest temperatures that may be warm enough to support development.

Effects of temperature on embryonic development of the veiled chameleon, Chamaeleo calyptratus.

Temperature dependence of development of the chameleon, Chamaeleo calyptratus, was assessed from observations on eggs incubated at 25, 28 and 30 degrees C. Overall, differentiation, growth in mass, and growth of the yolk sac and chorioallantois were the slowest at 25 degrees C but did not differ between 28 and 30 degrees C. The relative area of the yolk sac (YS), chorioallantoic membrane (CAM), and their precursor, the area opaca vasculosa (AV) was used to characterize developmental phases. During Phase 1, only the AV was present; development was characterized by differentiation with little increase in the size of the embryo. During Phase 2, the vascularized YS and CAM grew from about 10 to 100% coverage of the surface of the shell during a period of about two weeks. Differentiation and growth of the embryo were accordingly rapid. During Phase 3, the YS and CAM were fixed in size and the remainder of development was relatively slow. Characterization of embryonic development with respect to the relative area of the AV-YS-CAM highlighted the functional linkage between development and the systems that provide nutrients to embryos.

Incubation temperature and phenotypic traits of Sceloporus undulatus: implications for the northern limits of distribution.

Cold environmental temperature is detrimental to reproduction by oviparous squamate reptiles by prolonging incubation period, negatively affecting embryonic developmental processes, and by killing embryos in eggs directly. Because low soil temperature may prevent successful development of embryos in eggs in nests, the geographic distributions of oviparous species may be influenced by the thermal requirements of embryos. In the present study, we tested the hypothesis that low incubation temperature determines the northern distributional limit of the oviparous lizard Sceloporus undulatus. To compare the effects of incubation temperature on incubation length, egg and hatchling survival, and hatchling phenotypic traits, we incubated eggs of S. undulatus under temperature treatments that simulated the thermal environment that eggs would experience if located in nests within their geographic range at 37 degrees N and north of the species' present geographic range at latitudes of 44 and 42 degrees N. After hatching, snout-vent length (SVL), mass, tail length, body condition (SVL relative to mass), locomotor performance, and growth rate were measured for each hatchling. Hatchlings were released at a field site to evaluate growth and survival under natural conditions. Incubation at temperatures simulating those of nests at 44 degrees N prolonged incubation and resulted in hatchlings with shorter SVL relative to mass, shorter tails, shorter hind limb span, slower growth, and lower survival than hatchlings from eggs incubated at temperatures simulating those of nests at 37 and 42 degrees N. We also evaluated the association between environmental temperature and the northern distribution of S. undulatus. We predicted that the northernmost distributional limit of S. undulatus would be associated with locations that provide the minimum heat sum (approximately 495 degree-days) required to complete embryonic development. Based on air and soil temperatures, the predicted northern latitudinal limit of S. undulatus would lie at approximately 40.5-41.5 degrees N. Our predicted value closely corresponds to the observed latitudinal limit in the eastern United States of approximately 40 degrees N. Our results suggest that soil temperatures at northern latitudes are not warm enough for a sufficient length of time to permit successful incubation of S. undulatus embryos. These results are consistent with the hypothesis that incubation temperature is an important factor limiting the geographic distributions of oviparous reptile species at high latitudes and elevations.

Evolution of viviparity in sceloporine lizards: in utero PO2 as a developmental constraint during egg retention.

Reptilian viviparity evolves through selection for increasingly prolonged egg retention within the oviduct. In the majority of sceloporine lizard species, however, egg retention past the normal time of oviposition results in retarded or arrested embryonic development. In this study, we tested the hypothesis that the amount of embryonic development normally attained in utero is directly related to in utero oxygen partial pressure (PO(2)). The three species of sceloporine lizards we used are characterized by developmental arrest (Urosaurus ornatus), retarded development (Sceloporus virgatus), and normal development (Sceloporus scalaris) when eggs are retained. We incubated eggs of these species for 10 d under conditions that simulated retention in the oviduct at a range of experimental oxygen partial pressures (PO(2)). We estimated in utero PO(2) from a standard curve generated from the stage and dry mass of experimental embryos incubated for 10 d at known PO(2). The standard curve was then used to predict the PO(2) associated with the observed rate of development of embryos retained in utero. The results of this study showed that the degree of embryonic development attained in utero during egg retention was positively associated with in utero PO(2). The results indicate that oxygen availability in utero is associated with interspecific differences in the capacity to support intrauterine development in sceloporine lizards.

Effects of temperature and moisture on embryonic diapause of the veiled chameleon (Chamaeleo calyptratus).

The development of lizard embryos is typically initiated at fertilization and continues until birth or hatching. In contrast, embryonic development of some chameleons is arrested at the gastrula stage, and embryos remain at this stage for months after the eggs are laid. Our research tested the hypothesis that increased temperature, moisture, or both, are associated with the resumption of development by diapausing embryos of Chamaeleo calyptratus, the veiled chameleon. After 40 days of incubation at 25 degrees C in a relatively dry substrate, eggs were subjected to: 1) no change in temperature or moisture, 2) no change in temperature but change from a dry to a wet substrate, 3) change to a warmer temperature but no change in substrate moisture, or 4) an increase in both temperature and substrate moisture. Overall, embryos initiated development after 50-60 days to 80 or more days of incubation. Neither substrate moisture nor water uptake by eggs was related to the interval when development resumed. In contrast, development was initiated about 10 days earlier for eggs in the high temperature treatment compared to eggs in the low temperature treatment. Our results suggest that neither water availability nor water uptake by eggs affect the length of diapause but that an increase in ambient temperature initiates development of diapausing embryos of C. calyptratus.

Low oxygen: a constraint on the evolution of viviparity in reptiles.

The evolution of reptilian viviparity (live bearing) from oviparity (egg laying) is thought to require transitional stages of increasingly longer periods of embryonic development in utero, that is, longer periods of egg retention by the gravid female. Studies on sceloporine lizards demonstrate that embryonic responses to egg retention that is extended beyond the time of normal oviposition range from developmental arrest to normal development. The present study was designed to test the hypothesis that O(2) availability is the proximate factor that determines the rate and degree of development that reptilian embryos undergo in utero. Eggs of Sceloporus undulatus were incubated under conditions of low (LOX), normal (NOX), and high (HOX) oxygen both early and late in development. The LOX treatment consistently had a negative effect on development in terms of embryonic differentiation and growth, length of incubation, egg mortality, and hatchling size. Moreover, the LOX treatment had a stronger negative effect later in development than earlier in development. The results support the hypothesis that limited oxygen availability in utero acts as a developmental constraint. They further indicate that selection for extended egg retention, per se, will not lead to viviparity unless each incremental increase in the duration of egg retention is coupled with selection for traits (e.g., vascularity of oviduct and chorioallantois, hemoglobin oxygen affinity, etc.) that enhance O(2) availability to embryos. Such selection would be the most efficacious in cold climates where the effects of hypoxia would be the least likely to limit embryonic development.

Predation on lizard eggs by ants: species interactions in a variable physical environment.

One explanation for long-term fluctuations in population density is that the intensity of interactions between species is variable. A population can experience variation in the intensity of a species interaction if (1) the density of species with which it directly interacts changes and/or (2) the strength of the interaction (i.e., per capita effects) changes. At Barro Colorado Island, Panama, the tropical lizard Anolis limifrons exhibits wide annual fluctuations in density. Previous studies have indicated that (1) the density of A. limifrons is negatively correlated with the amount of wet-season rainfall, (2) fluctuations in density are related more to variation in egg mortality than to variation in lizard mortality or to fecundity, and (3) most egg mortality is the result of predation by Solenopsis ants. We hypothesized that the amount of wet-season rainfall indirectly alters the density of A. limifrons by producing variation in the intensity of egg predation by Solenopsis. Additionally, we also wanted to determine if variation in the amount of egg mortality was influenced more by variation in the density of Solenopsis, or by variation in the rate of predation. We tested this hypothesis by manipulating litter moisture on experimental plots to simulate the wettest (HW) and driest (LW) wet seasons in the last 20 years, and then monitoring the density of Solenopsis, amount of egg mortality, and rate of predation. The amount of egg mortality was greater on the HW than on the LW treatment and all egg mortality resulted from predation by Solenopsis. ANCOVA indicated that the amount of egg mortality was significantly higher on plots with a greater density of Solenopsis. Treatment effects, however, explained more of the variation in the amount of egg mortality than did Solenopsis density. Our water manipulations did not change the density of Solenopsis, but Solenopsis found and attacked eggs faster on the HW than on the LW treatment. This suggests that moisture during the wet season modified the strength of the interaction between Solenopsis and A. limifrons, supporting the hypothesis that annual variation in the amount of wet-season rainfall indirectly produces parallel variation in annual density of lizard populations by modifying the rate of ant predation on eggs.

Demographic correlates of variable egg survival for a tropical lizard.

Anolis limifrons is a small iguanid lizard that is found in lowland rainforest in Central America. Important life attributes include early maturity (3-4 mo), multiple clutches of a single egg per breeding season, and low survival. Population turnover is essentially annual as less than 5% adults live more than one year. My objectives were to resolve the following specific questions: 1) Where are eggs laid? 2) Does survival differ among different types of oviposition site? 3) How is the survival of eggs related to the density and age distribution of lizards at different areas? Most eggs are laid beneath litter on the ground. Eggs laid aboveground are placed in accumulations of soil and litter in stumps, crevices in buttressed trees and vines, holes in trees, and on the tops of logs. Eggs were found in aboveground sites in proportion to the abundance of those sites. The major cause of mortality was predation by Solenopsis ants. Judging by the ratio of eggs known to have hatched to those that were predated, survival did not differ among the various types of oviposition site. Study areas with high egg survival in the middle of the wet season had relatively more young (<4-6 mo old) lizards at the end of the wet season than areas with low egg survival. The strong correlation between the relative number of young individuals and egg survival is a consequence of the seasonal cycle of growth and reproduction. Most eggs are laid in the wet season (May-December). Hatchlings complete growth during the dry season (January-April) and become reproductive adults in their second wet season. However, because hatchlings can grow to reproductive size in approximately 3 months, individuals that hatch early in the wet season may themselves produce offspring that will be <4-6 mo old in the late wet season. The relative survival of juveniles (eggs) and adults is an important datum for many theories of life history evolution. For A. limifrons, survival of eggs was two to three times more variable than survival of lizards on both temporal and spatial scales. Comparative data for reptiles are not available to put this information into an evolutionary prespective.