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We studied ontogenetic shifts in sexual dimorphism and female reproduction in the Reeves's Butterfly Lizard, Leiolepis reevesii (Agamidae), from Hainan, southern China. The smallest reproductive female was 84 mm snout–vent length (SVL). The largest female and male were 136 mm and 166 mm SVL, respectively. Sexual dimorphism in head size and tail size was evident in adults, with adult males having larger heads and longer tails than did adult females of the same SVL. Head size relative to SVL was greatest in hatchlings and smallest in adults, with juveniles in between. Tail length relative to SVL was shorter in hatchlings than in juveniles and adults but did not differ between juveniles and adults. Females produced a single clutch of 2–8 eggs per breeding season stretching from mid-April to mid-July. Clutch size, egg mass, and clutch mass were all positively related to female SVL. Egg mass was negatively correlated with clutch size when holding female SVL constant, and egg length was negatively correlated with egg width when holding egg mass constant. Larger females increased reproductive output primarily through production of more and larger eggs (and hence heavier clutches). Males are the larger sex in L. reevesii presumably because (1) the selective pressure toward increased male size is strong; (2) the selective pressure toward increased female size is comparatively low; and (3) somatic growth is more likely to be constrained by reproduction in smaller females because of a negative correlation between relative clutch mass and SVL.
The acoustic structure of 18 male advertisement calls of the “music frog” (Babina daunchina), indigenous to the Emei mountain area of Sichuan province in southwest China was analyzed. Previous results showed that Babina typically call from within hidden burrows made by the males and must rely strongly on acoustic information for mate choice. Functioning ecologically as nests, burrows are used for mating, egg-laying, and pre- and postembryonic development. Male Babina calls are spectrally and temporally complex consisting of a sequence of 3–8 notes. Each note consists of a stack of frequency bands, which are nearly integer multiples of the fundamental residue. For all calls the fundamental frequency of successive notes increases monotonically. Moreover, there is a negative correlation between the lowest harmonic (F0) value of the first call note and the increments in fundamental frequency between notes in the same call, implying that constraints exist in the production mechanism. Hierarchical cluster and multidimensional scaling analysis of 29 temporal and spectral call parameters indicate that most of the variance between calls and between males is accounted for by three clusters of call features. The first includes 19 tightly correlated temporal and modulation features including note durations and modulation patterns and total call duration. The second cluster includes the successively increasing fundamental frequencies of the call notes and may reflect that individual males can alter fundamental frequency from call to call. The third cluster includes the dominant frequency bands in calls and may reflect the filter properties of each male's burrow.
Resistance to cutaneous evaporative water loss has been examined in anuran amphibians that occupy a variety of habitats, except for the ocean. We measured evaporative water loss rate and cutaneous resistance to evaporation in the Crab-eating Frog, Fejervarya cancrivora, a euryhaline species that enters the sea. Studies were conducted on Hoga Island, southeastern Sulawesi, Indonesia. Area-specific evaporative water loss rate was significantly lower in living F. cancrivora than in agar replicas of the frogs and total water loss rate was dependent on body mass. Cutaneous resistance to evaporative water loss was 0.27 sec cm−1, which is the lowest significant resistance known for frogs. Cutaneous resistance may have evolved as a way for F. cancrivora to reduce water loss while on land, thereby offsetting high osmotic losses to seawater before frogs have fully acclimated to higher salinities.
We studied the movement patterns and habitat selection of 33 radio-tagged Plateau Brown Frogs (Rana kukunoris) in the Zoige Alpine Wetland in southeastern Qinghai-Tibet plateau. Our goals were to (1) understand postbreeding movement patterns of R. kukunoris; (2) describe microhabitat use, with special reference to use of small mammal burrows; (3) test for movement pattern and microhabitat use differences between sexes and between seasons; and (4) provide a preliminary description of overwintering sites. We found no differences in movement patterns between sexes in R. kukunoris, however, directional movement trends differed between habitats. Male and female R. kukunoris showed similar microhabitat selection with regard to air temperature, relative humidity, and vegetation height. Although males used mammal burrows more frequently than females at one study site, BaiHua, both sexes used these microhabitats frequently during their movements. Overwintering sites of R. kukunoris were characterized by year-round flowing water. Results from this study will assist in making decisions about conservation and land protection for this species.
The influence of the presence of nonlethal predators on antipredator defense behavior and metamorphic traits was studied in the toad Bufo melanostictus. Tadpoles reared with caged predaceous tadpoles of Hoplobatrachus tigerinus delayed metamorphosis and also emerged at a smaller size compared to those in a predator-free environment. Different predaceous cues (kairomones, alarm cues and dietary cues, derived after feeding the predator with conspecific prey) induced increase in stationary phase and swimming speed and decrease in swimming spurts and time used for feeding. The intensity of defense behaviors varied with the cue. They were more intense in response to cues of predators fed on conspecific prey item. The response to alarm cues or kairomones or predators fed on heterogeneric tadpole species was similar but lower in magnitude compared to that elicited in response to predators fed on conspecific prey item. Most intense defense behavior in response to the odors of the predator that consumed conspecific members is possibly caused by a combined effect of kairomones, alarm, and dietary cues. The findings suggest that B. melanostictus tadpoles are capable of assessing levels of predation risk and modulating the intensity of their defense behavior in accordance with the perceived threat. Interestingly, despite longer larval period, size at metamorphosis of the toadlets was smaller in the presence of caged predator.
I studied the egg-laying behavior of the frog Buergeria japonica in the coastal areas of Okinawa, Japan, to clarify whether females avoid high salinity areas to reduce egg mortality. I compared the distribution of oviposition sites to the salinity gradient and evaluated the physical cues used by females to select oviposition sites. Females selected oviposition sites above the high tide line at spring tide, where eggs would not be disturbed by incursion of seawater. Above this high tide line, females selected oviposition sites from which eggs would not be washed out or desiccate, by using cues such as water depth and substrate. Examination of conditions at two spatial scales helps to clarify the evolution of oviposition site selection.
Competition and predation are two of the most important factors structuring communities, and these interactions may be exaggerated when two closely related species share similar resource requirements. We studied size-based habitat selection of artificial phytotelmata for deposition of tadpoles in two species of poison-dart frogs, Dendrobates auratus and Oophaga granulifera, in Costa Rica. Dendrobates auratus exhibits male parental care, and its tadpoles are predaceous, whereas O. granulifera exhibits biparental care, and its tadpoles are obligatory trophic egg eaters. These behavioral traits are integral factors in habitat selection for these two species. We found that the predaceous D. auratus selected large- and medium-sized pools, whereas O. granulifera selected all pool sizes but had a preference for small pools. Oophaga granulifera paid a high cost for exploiting large pools experiencing 100% mortality when sharing a pool with D. auratus. The use of small versus large pools in these species is rooted in each species' divergent parental care strategies and tadpole feeding behaviors.
We validated the diagnostic tests for the high-profile disease, chytridiomycosis, in wild amphibian populations. We compared histological samples with a Taqman real time quantitative PCR (qPCR) test in five species of frogs at different times of the year at six locations in the wet tropics of northern Queensland. The sensitivity and specificity of each test were estimated using prior estimates from previous laboratory studies and Bayesian methods. The qPCR test was almost three times as sensitive 72.9% (62.7–82.2%) than histology 26.5% (19.9–33.9%) but was less specific 94.2% (89.3–98.6%) than histology 99.5% (98.4–100%), which was likely caused by contamination. Monitoring of the negative control success rate of the qPCR test is potentially a good indicator of specificity. It is likely that using individual gloves for handling amphibians reduces cross-contamination and, therefore, improves specificity rather than cause inhibition of the qPCR. Classifying indeterminate results as positive will increase the qPCR test sensitivity but will lower specificity to a lesser degree depending on the likelihood of contamination. Although PCR is the preferred test for amphibian populations, histology is useful when wishing to confirm a diagnosis of infection and in situations where observing the severity of infection and pathology in skin is desired. In this study, we show that diagnostic test validation in wild animals is now relatively straight forward using modern computing power and can incorporate prior knowledge generated from laboratory studies using Bayesian approaches.
Normal tables of development intentionally ignore variation that results from both environmental and genetic sources. However, variation is important to consider when determining which characters most reliably indicate the stage of embryos. Our objective was to quantify variation in the relative time of the appearance and duration of character states for embryos of the lizard Uta stansburiana. The expression of the number of pharyngeal slits, development of optic capsule, eye pigmentation, and body size were highly variable, that is, these character states spanned multiple nominal stages. In general, the assessment of character variation in concert with the construction of normal tables would facilitate staging embryos for descriptive, experimental, and comparative studies.
Sexually dimorphic traits are used for mate selection either by female choice (intersexual selection) or male–male competition (intrasexual selection). In anurans, both types of selection mechanisms, especially intersexual selection, generally will favor large males. In bufonids, however, male size does not seem to be a factor in mate selection. Very little is known about the mating preferences of the endangered Houston Toad (Bufo houstonensis). Studies examining the breeding dynamics of B. houstonensis were conducted during the early 1980s, with conflicting results. To further examine mate selection, 329 Houston Toads were collected from Bastrop State Park, Texas, and the snout–urostyle length (SUL) was measured. There was no significant difference in size for males found in amplexus, suggesting females may not select larger males.
Species that exhibit extreme traits can provide valuable insight into the evolution of those traits. Bitis schneideri has the smallest body size of all vipers, reportedly reaching a maximum length of 254 mm. We studied size, sexual size dimorphism, and growth in a population of B. schneideri from the Northern Cape Province, South Africa to better understand these traits in the smallest viperid. We weighed and measured 285 snakes (124 males, 101 females, 60 juveniles) over three austral summers. We recorded a maximum body length of 251 mm and body mass of 38 g. Mean adult female body length (207.4 ± 27.6 mm) was longer than mean adult male body length (191.6 ± 20.2 mm). As predicted, female snakes were heavier bodied than males of the same length, had shorter tails, and had relatively larger heads. Growth rate was rapid and did not appear to differ among the sexes. Individuals reach mean adult body length in approximately 2.2 years, and male snakes are likely to reach reproductively mature size in approximately 10 months. We suggest that sexually dimorphic traits have evolved primarily through fecundity selection for females. Additionally, we propose that the evolution of small body size in B. schneideri is a result of the selective thermoregulatory, foraging, and predator avoidance advantages gained by being small enough to shuffle into sandy substrates.
The tadpole of Plectrohyla arborescandens is described. This tadpole resembles other Plectrohyla by having labial tooth row formula 2(2)/3 and large submarginal papillae. Plectrohyla arborescandens differs from the other species of Plectrohyla with overlapping distributions and known larvae, by having uniserial marginal papillae surrounding the oral disc. We suggest that the tadpole of Plectrohyla cyclada is the one presently assigned to Plectrohyla sabrina.
The high frequency of various kinds of phenotypic abnormalities in some local amphibian populations has long been a puzzle. In this paper, we report malformations in the populations of two species of frogs, Pelophylax saharicus and Discoglossus pictus, inhabiting water bodies created by an artificial dam in an area devoted to intensive agriculture in the northeastern part of Tunisia. More than 35% of recently metamorphosed and young froglets in P. saharicus, and 25% in D. pictus, display morphological abnormalities that can be distributed in 18 types involving limbs, spine, eyes, or skin. Although we did not investigate the cause of these malformations, the unusually high malformation rate (33.3%) in these populations, as compared to conspecific individuals from other, noncultivated areas, points to an environmental disturbance.
Most lizard species feed on small arthropods, and although some are omnivorous, only a few species are strict herbivores. We studied the diet of Dicrodon guttulatum, a teiid lizard endemic to the arid coastal deserts and dry forests of northern Peru. Herbivory by this lizard has been identified as a potential limiting factor in the regeneration of plant communities in these dry ecosystems. We collected gastric and fecal samples of adult males, adult females, and juveniles of D. guttulatum in different plant communities. Based on the ontogenetic shift from insectivory to herbivory observed in other herbivorous lizards, we hypothesized that juvenile D. guttulatum would have an omnivorous or insectivorous diet. We found D. guttulatum to be almost exclusively herbivorous (78–100%) and to feed largely (12–95%) on mesquite (Prosopis pallida) leaves and flowers across all plant communities and locations. Contrary to our predictions, there was a large overlap in diet between adult males and juveniles, whereas adult females were most likely to include plant species other than P. pallida in their diet. The consistency of herbivory in both juveniles and adults makes the origin of herbivory in D. guttulatum very interesting. We discuss potential factors promoting the evolution of herbivory in this species and the importance of lizard herbivory in the dry ecosystems of northern Peru.
Understanding habitat selection is a fundamental goal of ecology and is vitally important for effective species conservation. Dekay's Brownsnake (Storeria dekayi; hereafter “Brownsnake”) is one of the most widespread snake species in eastern North America, and its association with cover objects is generally well known, but details regarding choice of refuges are largely unknown. We investigated Dekay's Brownsnake microhabitat use during annual surveys at Point Pelee National Park, Ontario, Canada from 1990 to 2010. We systematically checked all woody debris in stabilized dune habitat for snakes and noted the size and state of decay of woody debris that was used. Nearly all of our observations were of gravid females under woody debris. Greater use of large, moderately decayed woody debris relative to the range of available debris provided strong evidence of selection. Although most snakes observed were solitary, we found a significant number of aggregations. Female Brownsnakes appear to migrate to stabilized dune from other habitats in the park to select suitable woody debris for gestation and parturition. Although these refuge sites would reduce predation risk, they also provide a moister and cooler microclimate than ambient conditions. Numerous observations of shed skins also suggested that this woody debris provides important microhabitat for ecdysis. Analysis of relative abundance over time showed considerable variation in numbers (1–31/yr) and an increasing trend. Our results provide strong evidence of microhabitat selection by this species and highlight the importance of not making generalizations about microhabitat requirements, even for common snake species.
Wide-ranging snake species are particularly sensitive to landscape fragmentation, and understanding area requirements is important for their conservation. We used radiotelemetry to quantify how Eastern Indigo Snake home-range sizes were influenced by sex, land cover, and the length of time (weeks) individuals were radio tracked. We found that Eastern Indigo Snakes had the largest home ranges among other snake species studied. Female home ranges averaged 44 and 76 ha, respectively, for kernel and minimum convex polygon estimators. Male home ranges averaged 156 and 202 ha, respectively, for kernel and minimum convex polygon estimators. Many animal species respond to habitat fragmentation by using larger areas than in unfragmented landscapes, but we found that Indigo Snakes in fragmented landscapes used much smaller areas. The length of time that snakes were tracked had almost no influence on home-range size compared to sex and land cover type. Our results suggest that maintaining populations of this large wide-ranging predator will require large conservation areas with minimum fragmentation.
Ephemeral, fishless wetlands with open canopies are known to be quality breeding habitats for pond-breeding amphibians. Yet many wetlands including these are commonly invaded by exotic plants, resulting in vegetation shifts from diverse native vegetation to monotypic stands of novel material. I tested the hypothesis that an invasive grass, reed canary grass (Phalaris arundinacea), would reduce survival, growth, and development rates of four tadpole species relative to a mixture of native grasses. I manipulated grass type and amount in fully replicated mesocosm experiments that contained American Toads (Anaxyrus americanus), Cope's Gray Treefrogs (Hyla chrysoscelis), Pickerel Frogs (Lithobates palustris), or Wood Frogs (Lithobates sylvatica). Counter to expectations, I found little evidence that diverse vegetation enhanced wetland quality for amphibians, because the quantity of decomposing plant matter influenced tadpole performance more than type of plant matter. Growth and development of tadpoles was generally not affected by RCG, indicating that this invasive grass produced minimal direct (e.g., toxic alkaloids) or indirect (i.e., through the food web) effects on tadpoles. However, differences in survival were found. I suggest that large amounts of grass supplied excess organic matter that decomposed rapidly underwater, potentially causing a pulse of nutrients early in the larval period and anoxia. Wetlands invaded by reed canary grass may successfully produce metamorphs given that hydroperiods are adequate and eutrophic conditions do not occur in the wetland.
Florida scrub is a fire-maintained ecosystem with a high concentration of endemic and imperiled species. To assist in the conservation of these taxa, we evaluated how communities and populations of amphibians and reptiles varied with fire history in rosemary (Ceratiola ericoides) scrub. We calculated species richness, evenness, total abundance, and individual species abundance for all amphibians and reptiles captured from May through August 2003 and May 2004 at 12 rosemary scrub sites in Highlands County, Florida, that differed in fire history (time since last fire, TSF). Vegetation structure (bare ground and canopy cover) varied polynomially with TSF, with intermediate TSF sites most open and long-unburned sites least open. Species richness, evenness, and total abundance did not vary with fire history. At the species level, only two species, Plestiodon reynoldsi and Aspidoscelis sexlineata, showed significant relationships with TSF: P. reynoldsi was most common in least open, longest-unburned areas and least common in most open, intermediately burned areas, whereas A. sexlineata was most common in most open and intermediately burned areas and least common in recently and long-unburned areas. The close relationship of abundance to vegetation structure suggests that indirect fire-induced changes may be more important than fire per se. In sum, amphibian and reptile communities did not vary with fire history; however abundances of some species did.
Multiple mating and sperm storage can influence reproductive strategies of males and females. Male reproductive success is often limited by the ability to acquire mates; therefore, males have evolved strategies to mate with multiple females. In contrast, the number of offspring a female produces is generally not limited by the quantity of sexual partners; thus, selection for multiple matings is expected to be weaker than in males. Evidence of polyandry and sperm storage is widespread among lizards. We investigated whether female Common Five-lined Skinks (Plestiodon fasciatus) could store viable sperm between reproductive cycles, estimated the frequency of multiple paternity, and examined the sharing of paternity within clutches. Females were unable to store viable sperm between successive clutches. Most clutches (65%) had multiple sires, but within those clutches, there was unequal sharing of paternity. Although we cannot determine the function of polyandry from our data, we suggest possible causes of polyandry in the mating system of this species.
Anuran amphibians feature at least two olfactory systems, the main olfactory organ and the vomeronasal organ (VNO). Although the main olfactory organ is known to detect air-borne olfactory stimuli, the capacities of the anuran VNO are still under discussion. One unresolved question is how chemical stimuli reach the vomeronasal sensory epithelium. The present study investigates, for the first time, the anatomical relationship between the anuran lateral nasal glands (LNG) and the VNOs of adult and developing animals. Based on the histological results, it seems very likely that the LNG is involved in the functioning of the vomeronasal system. First, the orifice of the LNG in adult animals of three investigated anuran species is always located nearby the external naris but, at the same time directly above the entrance to the lower nasal cavities and, thus, the VNO. Secretions discharged by the gland are observed to move toward this entrance. Furthermore in the development of the gland during metamorphosis, the spatial affiliation between the glandular opening and the VNO becomes prominent. The secretions of the LNG may carry chemical stimuli from the entrance of the nasal cavity to the vomeronasal sensory epithelium, a scenario already described for so-called odorant-binding proteins (OBP), found in secretions of the mammalian LNG. The question of whether the stimuli trapped by the gland secretions may be volatile is discussed in the light of the present and previous results.
Caiman latirostris (Broad-Snouted Caiman) is widely distributed in wetlands and rivers of South America. Hematological and blood chemistry reference values are necessary for detecting the effects of environmental, infectious, parasitic, or toxicological stress on C. latirostris health. Peripheral blood samples were obtained from 24 healthy 6- to 18-month-old caimans. Blood cell dimensions and cytochemistry profiles were described; and reference intervals for hematological parameters, enzyme activities, and clinical analytes were established. Based on the caiman mass frequency distribution, two classes were distinguished: 125–900 g and 901–3,100 g. Although an overlap in age ranges was observed, total length and snout–vent length range values from both mass classes differed. This finding is particularly useful because, in the wild, caiman age is unknown, whereas growth parameters can be easily recorded. Caiman blood cells exhibited morphological features similar to those of other reptiles, with lymphocytes being the most numerous type of leukocytes. Significant positive correlations between mass and hemoglobin concentration, hematocrit, red blood cell, and white blood cell counts were observed. Neither sex nor age was associated with differences in these parameters. Analysis of blood chemistry values found in this study was done by comparing with values reported for related species. Both similarities and discrepancies with values from other crocodiles are discussed. This study provides baseline information from healthy juvenile caimans to which subsequent measurements can be compared. These data will aid in the medical management of caiman farms, zoo conservation programs, and field studies.
We studied captive Balkan Whip Snakes (Hierophis gemonensis) to determine blood biochemical parameters that are useful indicators of physiological status during different periods of the biological cycle, including pre- and posthibernation, hibernation, sexual activity, and normal activity. In addition to classic statistical analyses, six machine-learning methods using 10 times 10-fold cross-validation evaluation were used to determine the best classification model for the blood biochemistry data. Results of the machine-learning models indicated that using three of the blood biochemistry variables simultaneously—urea, glucose, and lactate dehydrogenase—is enough to discriminate accurately between different physiological conditions during the biological cycle. This approach clarifies the role and importance of physiological processes, which show diversity of functional characteristics of various biochemical parameters in ecological relation to snakes held under laboratory conditions mimicking natural environmental changes.
Morphological and molecular information is invaluable in the description of cryptic diversity and the evolutionary processes driving diversification within closely related species that exhibit morphological homoplasy. We present a distribution-wide data set consisting of both molecular and morphological information, providing a taxonomic revision of the Diporiphora nobbi species group, and develop preliminary hypotheses regarding the evolutionary history of D. nobbi. We show deep molecular divergence between D. nobbi and a newly described sister lineage associated with divergence in meristic characters. Our molecular data also show large divergences among subclades within nominate D. nobbi associated with different habitats rather than specific biogeographc barriers. We further discuss potential diversification mechanisms within the D. nobbi species group.
Public concern for the humane treatment of animals in research has led to specific guidelines for appropriate treatment of study organisms. Field research poses special challenges that Institutional Animal Care and Use Committees find difficult to address based on existing guidelines. Toe clipping is a common but contentious example whose use has been called barbaric and whose efficacy has been questioned. We provide a brief review of the ethical bases for such positions, the legal framework they have engendered, and the scientific evidence regarding the impacts of the practice. Leading philosophical views vary but tend to focus on the suffering or distress of individual animals, primarily vertebrates. The law has adopted this individual-centered view. Biologists, in contrast, tend to more wholistic views that focus on populations and ecosystems. Scientific studies of the impacts of toe clipping, most of them relatively recent, have become increasingly sophisticated statistically. Most show little impact of toe clipping on study animals, the exception being the likelihood of recapture of toe-clipped individuals in some frogs. If unaccounted for, effects of methodology can bias scientific findings. The few studies focusing on physiological indicators of distress show no increase resulting from toe-clipping. Thus, toe clipping of reptiles and amphibians meets legal and ethical expectations and should remain acceptable where it meets study needs. Biologists have long been concerned about the possible ethical implications of their methods. Philosophical inquiry has been beneficial in improving our understanding of these methods, but the need of biologists for better philosophical elaboration of ecological ethics has only partially been addressed.