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Most reptiles are oviparous (egg-laying), but viviparity (live-bearing) has evolved about 100 times in lizards and snakes. Geographic biases in the distribution of viviparous species stimulated the “cold-climate hypothesis,” proposed independently by three field-based researchers in the early 1900s. Mell (in China) and Weekes (in Australia) viewed viviparity as a mechanism for thermal buffering of embryos from nighttime frosts, whereas Sergeev (in Russia) suggested that eggs retained in utero would develop faster because they were kept warmer, enabling early hatching. Although alternative adaptationist hypotheses proliferated over the next few decades, many had logical flaws (failing to consider intermediate stages). Phylogenetically based analyses identified around 100 independent origins of viviparity from oviparity, and revealed a strong trend for viviparity to evolve in cold climates. After experimental studies showed that incubation temperatures affect offspring phenotypes as well as rates of development and survival, I proposed (in 1995) that by retaining eggs in utero, a mother can manipulate the phenotypic traits of her offspring (and thus, enhance their fitness). This mother of all hypotheses subsumes the cold-climate hypothesis, and has been supported by studies on both oviparous and viviparous squamates, and in tropical as well as cold-climate areas. The history of this research topic illustrates the emergence of similar ideas from different researchers (sometimes creating tensions); the major roles of happenstance and field experience in suggesting ideas and allowing them to be tested; and the vital contributions of concepts, methodologies, and technologies from other fields to our understanding of reptilian viviparity.
Reproductive cycles of lizards have long been studied in both field and laboratory scenarios. However, comparisons of spermatogenic cycles and germ cell development strategies in different populations across a large geographic range have yet to be explored. The purpose of this study is to A) describe the spermatogenic cycle and germ cell development strategy of a population of Sceloporus consobrinus in southeast Louisiana, B) compare this cycle to a more northern population of this species, and C) compare the reproductive cycles of species within Sceloporus (N = 21). In S. consobrinus from Louisiana, recrudescence begins in the fall (October and November), and the peak of spermatogenesis is reached the following spring/summer (May, June, July). This spermatogenic cycle is similar to that of a more northern population of S. consobrinus from Missouri. Within the genus Sceloporus, there are two seasonal patterns of spermatogenesis: initiation of spermatogenesis in the summer/fall and initiation of spermatogenesis in the spring. In both summer/fall and spring spermatogenic patterns, spermiogenesis occurs in the spring and may continue into the summer. The seasonal timing of recrudescence is an extremely plastic trait that has evolved multiple times throughout the Sceloporus clade. However, there appears to be an association of summer/fall and spring recrudescence with latitude. Tropical populations have a higher frequency of spring recrudescence and temperate populations have a higher frequency of summer/fall recrudescence.
The genus Phymaturus, entirely viviparous and mostly herbivorous, inhabits the cold and harsh environments of the Andean highlands of Argentina and Chile, and the Patagonian steppe of Argentina. Phymaturus punae is a vulnerable lizard endemic to the Biosphere Reserve San Guillermo (National Park and Provincial Reserve) in San Juan (Argentina) that inhabits high altitudes of 3,100–4,200 m. The reproductive cycles of males and females of P. punae have been described previously. Males perform a prenuptial and annual cycle of spermatogenesis, and females reproduce once every 2 yr. As a consequence, the adjustment in the timing of males to the reproductive cycles of females must be very precise to ensure reproductive success. We elucidate the time of mating and the asynchrony of male and female reproductive events in P. punae based on endocrine and ultrastructural studies. Present hormonal results support the idea that copulation in P. punae occurs at the end of the activity season. Ultrastructural features observed in Sertoli and Leydig cells indicate that both types of cells have the potential to synthesize steroid hormones, to support the spermatogenic cycle and the mating period, respectively. In P. punae the cases of temporal asynchrony in steroid activity suggest that this mechanism must be important to start the spermatogenesis in spring, supported by the steroid activity of Sertoli cells, as Leydig cells are inactive. Nevertheless the asynchronic steroid mechanism seems to be more necessary in Phymaturus species with continuous or postnuptial cycles than in species with prenuptial cycles, like P. punae.
El género Phymaturus, enteramente vivíparo y mayormente herbívoro, habita ambientes fríos y rigurosos de la Cordillera de los Andes en Argentina y Chile, y de la estepa Patagónica Argentina. Phymaturus punae es un lagarto vulnerable, endémico de la Reserva de la Biósfera San Guillermo (Parque Nacional y Reserva Provincial) en San Juan (Argentina), que habita a altas altitudes entre los 3.100 y 4.200 metros. Los ciclos reproductivos masculinos y femeninos de P. punae fueron descriptos. Los machos realizan un ciclo espermatogénico anual prenupcial, y las hembras se reproducen una vez cada dos años. En consecuencia, el ajuste de los tiempos de los machos al ciclo reproductivo femenino debe ser muy preciso para asegurar los sucesos reproductivos. Dilucidamos el período de cópula y la asincronía de los eventos reproductivos de machos y hembras de P. punae, en base a estudios endócrinos y ultraestructurales. Los resultados hormonales obtenidos apoyan la idea que la cópula en P. punae ocurre al final de la temporada de actividad. Las observaciones ultraestructurales en células de Sertoli y de Leydig indican que ambos tipos celulares tienen el potencial para sintetizar hormonas esteroideas, para mantener la espermatogénesis y la cópula, respectivamente. En P. punae los casos de asincronía temporal en la actividad esteroidea, sugieren que este mecanismo es importante para iniciar la espermatogénesis en primavera, sostenida por la actividad esteroidea de las células de Sertoli, mientras las células de Leydig están inactivas. No obstante, el mecanismo de asincronía esteroidea parece ser más necesario en especies de Phymaturus con ciclos continuos o postnupciales, que en especies con ciclos prenupciales, como P. punae.
To understand the seasonal reproductive dynamics of Hypsiboas albopunctatus, a Neotropical treefrog, we studied the following components: 1) the influence of abiotic factors on seasonality, 2) how this seasonality relates to population dynamics, and 3) male breeding recruitment. We conducted fieldwork every month from August 2007 to July 2008 within an ecotone connecting semideciduous Atlantic Forest and Cerrado (Brazilian Savanna) in São Paulo State, southeastern Brazil. Over the course of the prolonged breeding season, we recorded the maximum number of calling males and measured their snout–vent lengths; we then compared our data from the beginning and the end of the breeding season. We found that the breeding pattern of H. albopunctatus is correlated with climatic, physical, and biological factors. Male competition and aggression varied according to the population density, most likely as a function of resource availability. There appears to be a social hierarchy among males of H. albopunctatus according to body size. Large calling males dominated the chorus in the beginning of the breeding season, but smaller males contributed more to the assemblage as the breeding season progressed. The average size of calling males at the end of the breeding season was significantly smaller. Smaller males occurred most in January and February, marking the H. albopunctatus breeding recruitment, when an abundance of adequate breeding microhabitats exist. Our full-season study serves as a cautionary tale: hypotheses based on body size, particularly for prolonged anuran breeder species, may be affected by seasonality.
Along the coasts of Florida, beach erosion caused by large storms and hurricanes coincides with the nesting season of the Loggerhead Sea Turtle. Here, we report the effects of beach renourishment and nest relocation on the success of Loggerhead Sea Turtle (Caretta caretta) eggs and hatchlings. Data on ∼53,700 Loggerhead Sea Turtle eggs from 517 clutches were collected over a six-year period, 2006 through 2011, on the Gulf Coast beaches of Pinellas County, Florida. We compared the proportion of eggs that hatched and hatchlings that emerged based on relocation; the type of beach on which breeders deposited their eggs (natural or renourished), and the type of beach to which clutches were relocated (natural or renourished). In this study, beach renourishment had no adverse effect on the proportion of eggs that hatched or the proportion of hatchlings that emerged. In contrast, clutch relocation decreased the proportion of inundated clutches 10-fold from 28–3%; an important finding as water inundation destroyed nearly half of the eggs per clutch. These findings add to a growing body of research on beach renourishment and clutch relocation with important implications for the continued management of Loggerhead Sea Turtle nests.
Understanding the response of species to land-use change is necessary for the improvement of management and conservation policies. We assessed the impact of vegetation cover and land-use change on Morelet's crocodile populations in nine wetlands located in central Veracruz, Mexico, to test the hypothesis that higher forest cover and lower anthropogenic impact increases crocodile density. We correlated the relative density of crocodiles with wetland attributes, including depth, pH, salinity, and richness and structure of bordering vegetation; and with anthropogenic disturbance factors, including the proportion of modified land surrounding the water body, road density, and road type. The relative density of crocodiles was correlated positively with vegetation cover and correlated negatively with plant density and with the presence of nonpaved roads, particularly in the zone that bordered the water bodies (core zone). Our findings suggest that as long as the water bodies are bordered with arboreal vegetation, land-use change and paved road density in inland areas had minor impacts on Morelet's crocodile populations in Mexican wetlands. The vegetation cover and the number of nonpaved roads within the core zone are useful indicators of habitat suitability for the Morelet's crocodile. The conservation of mangroves and forest remnants is therefore essential for the maintenance of crocodile populations.
Entender la respuesta de las especies al cambio de uso del suelo es necesario para mejorar las políticas de gestión y conservación de los recursos naturales. Evaluamos el impacto de la cobertura vegetal y el cambio de uso del suelo sobre nueve poblaciones del cocodrilo de pantano localizadas en el centro de Veracruz, México. Se sometió a prueba la hipótesis de que el aumento en la cobertura forestal y la reducción del impacto antrópico incrementan la densidad de cocodrilos. Correlacionamos las densidades relativas de los cocodrilos con atributos de los humedales, tales como profundidad, pH, salinidad, riqueza y estructura de la vegetación, y con atributos de disturbio antropogénicos como la proporción de tierras modificadas que rodean el cuerpo de agua, la densidad de caminos y los tipos de carretera. La densidad relativa de los cocodrilos aumentó cuando la proporción de cobertura vegetal natural fue mayor y disminuyó con la el aumento en el número de carreteras no pavimentadas, particularmente cuando éstas se encontraban alrededor de los cuerpos de agua (zona núcleo). Nuestros hallazgos sugieren que, mientras que los cuerpos de agua estén rodeados de vegetación arbórea, el cambio de uso de suelo y la densidad de carreteras pavimentadas lejanos al cuerpo de agua tendrán un impacto mínimo sobre las poblaciones de cocodrilo de pantano en los humedales mexicanos. La cobertura de la vegetación en la zona núcleo y el número de carreteras no pavimentadas son indicadores útiles de calidad del hábitat para el cocodrilo de pantano. La preservación de los bosques remanentes y los manglares es esencial para el mantenimiento de las poblaciones de cocodrilos.
Many populations normally experience high levels of mortality throughout larval development, but this is generally overlooked with laboratory experimental protocols. Evidence suggests that mortality is nonrandom in natural tadpole populations, so high survivorship, typical of laboratory populations, may poorly represent populations in nature. We compared survival, growth and development, and population variance of tadpoles in natural ponds with those in the laboratory at low and high densities. In the laboratory, high-density groups were reared with no selection and with selection imposed against different size classes to identify if, and how, mortality influences natural tadpole populations and to investigate whether imposing selection against certain size classes produces responses more consistent with those observed in natural systems. Our results suggest that selective mortality removes smaller individuals in natural populations. We demonstrate that introducing selection against small individuals artificially, in the laboratory, results in individual growth and development, population variance, and statistical power that more closely resembles that observed in natural populations. This is important from an ecological perspective because it demonstrates how selection acts on natural tadpole populations. More importantly, this demonstrates that laboratory experiments can be designed to provide better qualitative estimates for responses of natural populations by considering and simulating natural rates of mortality.
Foraging modes were described originally for insectivorous lizards, but many species are omnivorous or herbivorous. Because seeking and consuming plants might alter foraging, we studied foraging by the omnivorous Podarcis lilfordi at two sites: one where lizards licked nectar from flowers of Euphorbia paralias and the other where they sought insects. Movements per minute (MPM) did not differ among groups. Proportion of time spent moving (PTM) was similar in lizards that licked flowers and those that did not. Average speed (AS) was slower, and speed while moving (MS) was faster when foraging for nectar than for insects. Lizards foraging for nectar did not eat insects; those foraging for insects frequently ate them. For lizards foraging for prey, MPM increased as PTM, AS, and capture attempts increased and as PTM decreased. PTM increased as AS and capture attempts increased and decreased as MS increased. AS increased as MS increased. For lizards that licked, proportion of time licking (PTL) was unrelated to MPM, PTM, or AS but increased marginally as MS increased. Lizards foraging for nectar retained the PTM of lizards foraging for prey, but added a large PTL. The ancestral active foraging mode has been retained for hunting insects but modified to search for and lick nectar. While foraging for nectar, lizards greatly reduce attacks on insects, suggesting that, at a given time, an individual forages exclusively for nectar or prey. Reduced predation pressure on islands may have freed lizards to expand the diet by reducing risk during intervals exposed to view while climbing plants and licking nectar.
Mapping species' distributions is a primary challenge when managing cryptic lineages of conservation concern. In the case of unisexual Ambystoma salamanders, mapping geographic distribution of genotypes can also help us understand the evolutionary dynamics of one of the most intriguing vertebrate reproductive systems. We combined a mitochondrial sequencing technique with existing nuclear microsatellite methods to map genotypes in 15 Ambystoma populations throughout Massachusetts. We found that the host species A. jeffersonianum and A. laterale have disjunct east/west distributions, whereas unisexuals are distributed widely in Massachusetts. We did not find both host species at any single locality. In our samples, unisexuals outnumbered either host species in 11 of 15 populations. Ambystoma jeffersonianum nuclear genomes were present in at least 97% of unisexual salamanders in regions where A. laterale and unisexuals exist but A. jeffersonianum mitochondria were absent. If previous studies of the unisexual reproductive mode are correct, our observations suggest that natural selection favors hybrid nuclei in these populations.
The genus Pristimantis contains many species and species groups that are difficult to differentiate. These frogs show high intraspecific morphological variability and low morphological divergence between species, which contributes to misclassification of taxa and systematic uncertainties. Morphometric assessments coupled with the use of molecular markers are opening new avenues to resolve the taxonomy of this group, allowing for identification of informative characters. Morphometric and genetic analyses were applied to differentiate three species of Pristimantis (P. calcaratus, P. kelephas, and P. jubatus) previously confused in their identification and description. We evaluated 51 qualitative and quantitative morphological characters with sequences of two mitochondrial (mt) genes (16S and cytochrome oxidase subunit I [COI]). We used discriminant analysis to show that these species could be differentiated by two qualitative morphological characters (posterior surfaces of thighs and longitudinal stripes on the dorsum), whereas one quantitative variable (distance from tympanum to eye) differentiates only adults of the three species. Our genetic data showed highest divergence in comparisons of P. jubatus (>13%) with the other two species, whereas comparisons between P. kelephas and P. calcaratus were 2.6% and 8.3% for 16S and COI, respectively. These differentiations suggest that they are well-delimited species on the basis of morphological and mt deoxyribonucleic acid data. Nevertheless, the genetic differentiation between P. calcaratus and P. kelephas implied a recent divergence and showed the importance of using both morphometric and genetic analysis in species recognition.
Several observational and experimental studies have shown that perch diameter has an impact on the development of hind-limb length (HL) in Anolis species. This “phenotypic plasticity” in relative hind-limb growth (RHG) has implications for short-term and long-term adaptation to different structural habitats. Our study is the first to replicate research in which hatchling/juvenile Anolis sagrei were reared on narrow-diameter or broad-diameter dowels in a laboratory setting. Although subjects reared on different dowel diameters did not differ significantly in RHG at 5 weeks into the experiment, results at 15 weeks revealed a significant effect of treatment but not of sex: subjects in the broad (N = 69) treatment group exhibited significantly greater RHG than did subjects in the narrow (N = 61) treatment group. We extended this research with a novel follow-up study: we placed our lab-reared subjects into outdoor enclosures where they had a choice of narrow- or broad-diameter dowels on which to perch. Results showed that subjects in both treatment groups chose broad-diameter dowels as perches more often than narrow-diameter dowels. We offer several potential explanations for the strong preference of our subjects for broad-diameter dowels irrespective of the dowel diameter on which they were reared.
Translocation, a management and conservation strategy used commonly in which animals are moved from their sites of origin to other localities, has proven controversial. We examined the physiological and behavioral impacts of repeated handling and short-distance translocation on rattlesnakes, which are often translocated from areas of human use because of a perceived threat to people. Northern Pacific Rattlesnakes (Crotalus oreganus oreganus) were radiotracked for 2 months, during which time one of three treatments was imposed weekly: translocation, walk and release at that day's capture site (handling control), and undisturbed control. At both the beginning (spring) and the end (summer) of the study, blood samples were obtained before and after an acute handling stressor, and plasma concentrations of corticosterone (CORT) and testosterone (T) were determined. All rattlesnakes showed a CORT stress response, but baseline and stressed concentrations of neither hormone were affected by either translocation or handling. However, the response of both hormones to stress differed between spring and summer, with a greater increase in CORT and a detectable decrease in T occurring in summer. Activity range size was affected by translocation, whereas no effects on snake behaviors recorded during observer approach were detected. Rattlesnakes appear quite resilient to the potential impacts of frequent handling or short-distance translocation.
Quantitative studies of the axial undulatory swimming techniques used by secondarily aquatic vertebrates have been largely restricted to crocodilians. Numerous members of the suborder Lacertilia (lizards) are also known to swim using axial undulatory techniques, but how they do so has received minimal attention from the scientific community. We investigated the morphology and undulatory locomotor kinematics adopted by the Eastern Water Dragon (Intellagama lesueurii) through observation of natural swimming and filming of animals in a flume tank with a high speed camera. We found that morphological modifications associated with improved swimming ability and correlations between wave characteristics and swimming velocity are limited to the tail. The shape of dorsal spines and the reduction in the width of transverse processes of the caudal vertebrae result in a mediolaterally compressed tail instead of the typically rounded or dorsoventrally compressed tail seen in other Australian agamids. Axial undulatory swimming in I. lesueurii was found to be conceptually similar to that of crocodilians, but the relatively long and thin terminal part of the tail produces a different shaped undulatory wave. Unlike crocodilians and fishes, I. lesueurii does not use frequency moderated velocity control. Instead, changes in velocity are solely controlled by the phase speed of the propagating wave. The combined effect of these traits is comparable efficiency and performance in the water relative to that of crocodilians and an improvement relative to terrestrial lizards.
Brightly colored frogs of Dendrobatidae contain alkaloid-based chemical defenses which appear to be utilized as a deterrent to predators. The conspicuous coloration of these frogs is generally considered to be an aposematic signal to color-visioned predators. A previous field-based experiment tested this hypothesis in the dendrobatid frog Oophaga pumilio (Strawberry Poison Frog) from the La Selva Biological Station using a stationary clay model experiment to assess natural predation. Avian predation rates on brown frog models were almost twice that of red frog models, supporting the hypothesis that coloration in O. pumilio is aposematic. A criticism of clay model experiments has been that they do not accurately represent natural organisms, especially with regard to movement. Many predators utilize movement in prey selection and, therefore, may not perceive motionless clay models as prey. In an attempt to understand the importance of movement better in assessing natural predation rates using clay model experiments, we conducted a similar field-based clay model experiment but instead used moving models of O. pumilio and of brown control frogs. Moving brown models were attacked more than nine times the rate of moving red models, supporting the finding of the previous study and providing further evidence that color is aposematic in O. pumilio. When compared directly to the previous study using stationary clay models, birds attacked moving brown models significantly more whereas red moving models were attacked significantly less. Our findings suggest that moving models may provide a better estimate of natural predator responses to an aposematic frog.
I describe a new species of Liophryne from Cape Nelson, southeastern New Guinea, that is unique in its combination of rather large size, a single-note call emitted from an underground burrow, and absence of vocal slits. This species also has a variety of morphometric and color-pattern features that distinguish it from one or more congeners. The new species is among the more-variable species of Liophryne in dorsal color pattern, being either brown, ochre, or a combination of the two. It is known currently only from the upper elevations of an extinct volcano and may be restricted in distribution to the broader volcanic massif that includes the type locality, inasmuch as this massif appears to have evolved in situ.
Highly aquatic freshwater turtle species are at risk of vehicular encounters during terrestrial nesting forays; however, injuries and mortality incurred during boat collisions may present considerable threats as well. Additionally, effects of other injuries from predation or disease may augment the likelihood of population decline. We report injury rates from captures of two turtle species-at-risk, Northern Map Turtles (Graptemys geographica) and Stinkpots (Sternotherus odoratus), along the Trent–Severn Waterway in Ontario, Canada. We examined whether habitat fragmentation attributable to locks and dams would result in higher rates of boat propeller and predation injuries because of the higher human impact in fragmented areas. Fragmented areas of the waterway had similar injury rates to continuous areas; however, more female Map Turtles (28.6% of captured females) had injuries consistent with boat propeller strikes than males (12.8%). Map Turtles in general had higher rates of injury (48.5%) than Stinkpot Turtles (20.0%), although actual rates of boat or predator encounters may be confounded by the lowered probability of survival for a smaller-bodied turtle (e.g., Stinkpot, male Map Turtles). All species encountered on the waterway, including incidental captures of Blanding's Turtles (Emydoidea blandingii) and Snapping Turtles (Chelydra serpentina), showed some evidence of boat propeller strikes, suggesting that conservation strategies for aquatic turtle assemblages should consider restricting boat access, speed limits, or both, in areas of high turtle densities.
Fragmentation of natural landscapes by linear anthropogenic features, such as roads, has several negative consequences, including decreasing connectivity between habitats, inhibiting animal movements, and isolating populations. Roads limit animal movements through behavioral avoidance and mortality during crossing attempts. We investigated the impact of a road network on the movement patterns of Blanding's Turtles (Emydoidea blandingii) in Québec, Canada. We tested the hypothesis that roads act as a barrier to movements. We monitored 52 Blanding's Turtles (22 females, 24 males, and 6 juveniles) via radiotelemetry during their active season from May to August 2010. Road avoidance was quantified for each individual by comparing the number of inferred road crossings with the number of expected road crossings predicted by 1,000 movement path randomizations. Overall, Blanding's Turtles significantly avoided crossing roads. Roads were a significant barrier to movement for 3–6 of the 52 turtles, and an individual's tendency to cross roads was not influenced by its sex or by the road surface (unpaved or paved). Preserving demographic and genetic connectivity of animal populations separated by roads is a major conservation challenge for species at risk such as the Blanding‘s Turtle.
The International Code of Zoological Nomenclature (ICZN; hereafter, the Code) governs not only the availability and application of scientific zoological names once they enter the realm of nomenclature but also what is to be considered published work for the purpose of zoological nomenclature. Article 8.1.1 of the Code clearly demands that to be considered published in the meaning of the Code, works “…must be issued for the purpose of providing a permanent public and scientific record.” This requirement is often unfulfilled with the publication of nomenclatural acts in hobbyist magazines and amateur literature. Nevertheless, some names published in such outlets are in use today although, under strict application of the Code, these names could be de facto nonexistent for the purpose of nomenclature and cannot be made available simply by subsequent usage (ICZN, 1999: Articles 11.5.2, 16.1). In this paper, I discuss the application of Article 8.1.1 to the nonscientific literature and, as a consequence, resolve a nomenclatural problem posed by two populations of snakes in the genus LeiopythonHubrecht, 1879 that have been recognized as valid species but that do not have valid names under the requirements of the Code.
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