Cues for reproduction in squamate reptiles

To maximize fitness, animals should initiate reproduction based on information from suites of cues that communicate three variables critical to reproductive success: 1) environmental conduciveness for successful reproduction, and survival of offspring and (usually) parents; 2) physiological capability of parents to reproduce; and 3) likelihood of successful mating

Bioenergetic components of reproductive effort in viviparous snakes : costs of vitellogenesis exceed costs of pregnancy

Reproductive effort has been defined as the proportion of an organism's energy budget that is allocated to reproduction over a biologically meaningful time period. Historically, studies of reproductive bioenergetics considered energy content of gametes, but not costs of gamete production. Although metabolic costs of vitellogenesis (MCV) fundamentally reflect the primary bioenergetic cost of reproductive allocation in female reptiles, the few investigations that have considered costs of reproductive allocation have focused on metabolic costs of pregnancy (MCP) in viviparous species. We define MCP as energetic costs incurred by pregnant females, including all costs of maintaining gestation conditions necessary for embryogenesis. MCP by our definition do not include fetal costs of embryogenesis. We measured metabolic rates in five species of viviparous snakes (Agkistrodon contortrix, Boa constrictor, Eryx colubrinus, Nerodia sipedon, and Thamnophis sirtalis) during vitellogenesis and pregnancy in order to estimate MCV and MCP. Across all species, MCV were responsible for 30% increases in maternal metabolism. Phylogenetically-independent contrasts showed that MCV were significantly greater in B. constrictor than in other species, likely because B. constrictor yolk energy content was greater than that of other species. Estimates of MCP were not significantly different from zero in any species. In viviparous snakes, MCV appear to represent significant bioenergetic expenditures, while MCP do not. We suggest that MCV, together with yolk energy content, represent the most significant component of reptilian reproductive effort, and therefore deserve greater attention than MCP in studies of reptilian reproductive bioenergetics

Bioenergetic components of reproductive effort in viviparous snakes : costs of vitellogenesis exceed costs of pregnancy

Reproductive effort has been defined as the proportion of an organism's energy budget that is allocated to reproduction over a biologically meaningful time period. Historically, studies of reproductive bioenergetics considered energy content of gametes, but not costs of gamete production. Although metabolic costs of vitellogenesis (MCV) fundamentally reflect the primary bioenergetic cost of reproductive allocation in female reptiles, the few investigations that have considered costs of reproductive allocation have focused on metabolic costs of pregnancy (MCP) in viviparous species. We define MCP as energetic costs incurred by pregnant females, including all costs of maintaining gestation conditions necessary for embryogenesis. MCP by our definition do not include fetal costs of embryogenesis. We measured metabolic rates in five species of viviparous snakes (Agkistrodon contortrix, Boa constrictor, Eryx colubrinus, Nerodia sipedon, and Thamnophis sirtalis) during vitellogenesis and pregnancy in order to estimate MCV and MCP. Across all species, MCV were responsible for 30% increases in maternal metabolism. Phylogenetically-independent contrasts showed that MCV were significantly greater in B. constrictor than in other species, likely because B. constrictor yolk energy content was greater than that of other species. Estimates of MCP were not significantly different from zero in any species. In viviparous snakes, MCV appear to represent significant bioenergetic expenditures, while MCP do not. We suggest that MCV, together with yolk energy content, represent the most significant component of reptilian reproductive effort, and therefore deserve greater attention than MCP in studies of reptilian reproductive bioenergetics

Stable isotope tracer reveals that viviparous snakes transport amino acids to offspring during gestation

Viviparity and placentation have evolved from oviparity over 100 times in squamate reptiles (lizards and snakes). The independent origins of placentation have resulted in a variety of placental morphologies in different taxa, ranging from simple apposition of fetal and maternal tissues to endotheliochorial implantation that is homoplasious with mammalian placentation. Because the eggs of oviparous squamates transport gases and water from the environment and calcium from the eggshell, the placentae of viviparous squamates are thought to have initially evolved to accomplish these functions from within the maternal oviduct. Species with complex placentae have also been shown to rely substantially, or even primarily, on placental transport of organic nutrients for embryonic nutrition. However, it is unclear whether species with only simple placentae are also capable of transporting organic nutrients to offspring. Among viviparous squamates, all of the snakes that have been studied thus far have been shown to have simple placentae. However, most studies of snake placentation are limited to a single lineage, the North American Natricinae. We tested the abilities of four species of viviparous snakes - Agkistrodon contortrix (Viperidae), Boa constrictor (Boidae), Nerodia sipedon (Colubridae: Natricinae) and Thamnophis sirtalis (Colubridae: Natricinae) - to transport dietderived amino acids to offspring during gestation. We fed [ 15N]leucine to pregnant snakes, and compared offspring 15N content with that of unlabeled controls. Labeled females allocated significantly more 15N to offspring than did controls, but 15N allocation did not differ among species. Our results indicate that viviparous snakes are capable of transporting diet-derived amino acids to their offspring during gestation, possibly via placentation

The role of thermal contrast in infrared-based defensive targeting by the copperhead, Agkistrodon contortrix

The facial pit organs of the copperhead are the end organs of a complex infrared-imaging system that allows accurate and precise strikes on potential prey. Anecdotal and recent experimental observations show that pit vipers can use their infrared-imaging systems to discriminate between cool and warm features in the environment. We tested the hypothesis that the infrared-imaging system is a thermal contrast detector and determined whether behavioural responses of copperheads differ with contrast type. We found that blindfolded copperheads responded behaviourally towards both warm objects moving against cool backgrounds and cool objects moving against warm backgrounds. Responses towards the former were more robust than those towards the latter. Furthermore, oscillating warm targets generated rhythmic following behaviour in-phase with target motion, while oscillating cool targets generated rhythmic behavioural movement in antiphase to target motion. The results show that the infrared-imaging system of pit vipers operates on the basis of thermal contrast, but the differences in behavioural responses with respect to contrast type indicate that pit vipers preferentially target the warm aspect of thermal differentials. Our results also demonstrate that the infrared-imaging system allows defensive targeting of potential endothermic predators

Influence of relative trophic position and carbon source on selenium bioaccumulation in turtles from a coal fly-ash spill site

Selenium (Se) is a bioaccumulative constituent of coal fly-ash that can disrupt reproduction of oviparous wildlife. In food webs, the greatest enrichment of Se occurs at the lowest trophic levels, making it readily bioavailable to higher consumers. However, subsequent enrichment at higher trophic levels is less pronounced, leading to mixed tendencies for Se to biomagnify. We used stable isotopes (15N and 13C) in claws to infer relative trophic positions and relative carbon sources, respectively, of seven turtle species near the site of a recently-remediated coal fly-ash spill. We then tested whether Se concentrations differed with relative trophic position or relative carbon source. We did not observe a strong relationship between δ15N and Se concentration. Instead, selenium concentrations decreased with increasing δ13C among species. Therefore, in an assemblage of closely-related aquatic vertebrates, relative carbon source was a better predictor of Se bioaccumulation than was relative trophic position

No implantation in an extra-uterine pregnancy of a placentotrophic reptile

Placentation is a common feature of live-bearing reptiles and mammals. Placentae are variable between species and can be classified by the extent that embryonic tissue breaches (invades) the uterus. Non-invasive placentation in eutherians is maternally imposed as extra-uterine embryos of species with epitheliochorial placentation will readily invade non-uterine tissues. This study documents the first observation of an extra-uterine pregnancy in a reptile; Pseudemoia entrecasteauxii, which in-utero exhibits non-invasive epitheliochorial placentation. The extra-uterine embryo did not invade maternal tissue suggesting fundamental differences between the nature and evolution of placentation in P. entrecasteauxii and eutherian mammals

High food abundance permits the evolution of placentotrophy : evidence from a placental lizard, Pseudemoia entrecasteauxii

Mechanisms of reproductive allocation are major determinants of fitness because embryos cannot complete development without receiving sufficient nutrition from their parents. The nourishment of offspring via placentas (placentotrophy) has evolved repeatedly in vertebrates, including multiple times in squamate reptiles (lizards and snakes). Placentotrophy has been suggested to evolve only if food is sufficiently abundant throughout gestation to allow successful embryogenesis. If scarcity of food prevents successful embryogenesis, females should recoup nutrients allocated to embryos via abortion, reabsorption, and/or cannibalism. We tested these hypotheses in the placentotrophic southern grass skink Pseudemoia entrecasteauxii. We fed females one of four diets (high constant, high variable, low constant, and low variable) during gestation and tested the effects of both food amount and schedule of feeding on developmental success, cannibalism rate, placental nutrient transport, offspring size, and maternal growth and body condition. Low food availability reduced developmental success, placental nutrient transport, offspring size, and maternal growth and body condition. Cannibalism of offspring also increased when food was scarce. Schedule of feeding did not affect offspring or mothers. We suggest that high food abundance and ability to abort and cannibalize poor-quality offspring are permissive factors necessary for placentotrophy to be a viable strategy of reproductive allocation

Snakes allocate amino acids acquired during vitellogenesis to offspring : are capital and income breeding consequences of variable foraging success?

Reproductive allocation strategies have been historically described as lying on a continuum between capital and income breeding. Capital breeders have been defined as species that allocate stored reserves to reproduction, whereas income breeders have been defined as species that allocate relatively recently-ingested food resources to reproduction. Snakes are considered capital breeders because they efficiently store large amounts of nutrients and energy, potentially enough to support an entire reproductive bout without feeding. We examined the abilities of five viviparous snake species to allocate income to follicles during vitellogenesis. We fed 15N-labelled L-leucine to experimental females of each species during vitellogenesis, whereas control females were fed unlabelled meals. After ovulation, we measured yolk 15N p.p.m. using mass spectrometry. Maternal scale samples taken before labelling were used to estimate endogenous 15N concentrations, which should represent 'capital'. Scale samples taken at ovulation were used to determine whether snakes assimilated 15N-labelled-leucine from labelled diets. Yolks and post-ovulatory scales of labelled females were significantly more enriched in 15N than those of unlabelled females in all species, indicating significant assimilation and allocation of income-derived amino acids to the yolk during vitellogenesis. The lack of among-species differences suggests that all species allocated income amino acids to vitellogenesis. The results obtained in the present study suggest that proportional utilization of income or capital depends on the frequency and timing of foraging success during reproductive events. Therefore, capital and income breeding may be consequences of both life-history and environmental constraints on foraging success, rather than strategies of reproductive allocation

Residual yolk energetics and postnatal shell growth in Smooth Softshell Turtles, Apalone mutica

We examined functions of residual yolk (RY. 11RY: residual yolk.) in hatchling Smooth Softshell Turtles (Apalone mutica). Removal of RY did not affect survival, shell growth, or resting metabolic rates of turtles for 40 d after hatching. Our estimates of metabolic rate suggest that RY can fuel maintenance and activity metabolism for approximately 25. days. A. mutica absorb more than 1. g of water in the first 2 weeks of life, which appears to be the basis of post-hatch shell expansion rather than yolk-provisioned growth. Post-hatch growth may be limited by the magnitude of RY remaining at hatching, but RY protein and lipid proportions do not differ from those of freshly-laid eggs. In addition, A. mutica did not use RY to fuel nest emergence. Our results suggest that RY does not fulfill several hypothetical functions in A. mutica, including postnatal growth, catabolic fuel for nest emergence, and long-term nutritional sustenance for maintenance, activity, or hibernation. Instead, A. mutica appear to absorb most yolk prior to hatching, and are left with a minimum of RY. Variation in RY mass with incubation regime in other species suggests that mothers may overprovision their eggs to ensure successful development across a diversity of possible incubation conditions