Viviparous Snake Research Articles

Sex-specific fitness returns are too weak to select for non-random patterns of sex allocation in a viviparous snake

When environmental conditions exert sex-specific selection on offspring, mothers should benefit from biasing their sex allocation towards the sex with the highest fitness in a given environment. Yet, studies show mixed support for such adaptive strategies in vertebrates, which may be due to mechanistic constraints and/or weak selection on facultative sex allocation. In an attempt to disentangle these alternatives, we quantified sex-specific fitness returns and sex allocation (sex ratio and sex-specific mass at birth) according to maternal factors (body size, age, birth date, and litter size), habitat, and year in a viviparous snake with genotypic sex determination. We used data on 106 litters from 19years of field survey in two nearby habitats occupied by the meadow viper Vipera ursinii ursinii in south-eastern France. Maternal reproductive investment and habitat quality had no differential effects on the growth and survival of sons and daughters. Sex ratio at birth was balanced despite a slight female-biased mortality before birth. No sexual mass dimorphism between offspring was evident. Sex allocation was almost random apart for a trend towards more male-biased litters as females grew older, which could be explained by an inbreeding avoidance strategy. Thus, a weak selection for facultative sex allocation seems sufficient to explain the almost equal sex allocation in the meadow viper.

Developmental expression of carbonic anhydrase II in the extraembryonic membranes of oviparous and viviparous snakes

Oviparous reptile embryos receive a significant proportion of their calcium from the eggshell. For chickens, ≥ 80% of hatchling calcium originates from the shell while for oviparous snakes the shell accounts for 20–25% of hatchling calcium. The chick chorioallantois, which lies just beneath the eggshell, expresses carbonic anhydrase II (CAII) late in development. CAII is hypothesized to provide protons that are pumped out of the chorionic epithelium to acidify the inner surface of the shell, dissolving calcium carbonate and liberating calcium ions for transport to the embryo. Using immunoblotting, we determined the pattern of chorioallantoic CAII expression during the development of an oviparous (Pantherophis guttatus) and viviparous (Virginia striatula) snake to test the hypotheses that 1) oviparous snakes express a mechanism similar to chickens for dissolving shell calcium and 2) CAII is not expressed placental calcium transport in viviparous snakes. In P. guttatus, chorioallantois expression of CAII increases late in development coincident with shell calcium transport to the snake embryo, supporting hypothesis 1. In V. striatula, chorioallantoic expression of CAII also increases coincident with placental calcium transport late in development suggesting that CAII may be involved in additional chorioallantoic functions such as gas exchange and/or acid‐base balance. Supported by NSF grant IOB‐06515695.

Cohort variation in offspring growth and survival: prenatal and postnatal factors in a late‐maturing viviparous snake

1. Recruitment to adulthood plays an important role in the population dynamics of late-maturing organisms as it is usually variable. Compared to birds and mammals, few studies assessing the contributions to this variation of environmental factors, offspring traits and maternal traits have been carried out for late-maturing snakes. 2. Cohort variation in recruitment through offspring growth and survival in the meadow viper (Vipera ursinii ursinii) was evaluated from 13 years of mark-recapture data collected at Mont Ventoux, France. In this species, females are mature at the age of 4-6 years and adult survival and fecundity rates are high and constant over time. 3. Offspring were difficult to catch during the first 3 years of their lives, but their mean annual probability of survival was reasonably high (0.48 +/- 0.11 SE). Mass and body condition at birth (mass residuals) varied significantly between years, decreased with litter size, and increased with maternal length. 4. Cohorts of offspring in better condition at birth grew faster, but offspring growth was not affected by sex, habitat or maternal traits. 5. Survival varied considerably between birth cohorts, some cohorts having a high-survival rate and others having essentially no survivors. No difference in mass or body condition at birth was found between cohorts with 'no survival' and 'good survival'. However, offspring survival in cohorts with good survival was positively correlated with mass at birth and negatively correlated with body condition at birth. 6. Thus, variation in offspring performance was influenced by direct environmental effects on survival and indirect environmental effects on growth, mediated by body condition at birth. Effects of maternal traits were entirely channelled through offspring traits.

Embryonic mobilization of calcium in a viviparous reptile: Evidence for a novel pattern of placental calcium secretion

Yolk reserves supply the majority of embryonic nutrition in squamate reptiles, including calcium. Embryos of oviparous squamates exploit the eggshell for supplemental calcium, while embryos of viviparous species may receive additional calcium via the placenta. Developmental uptake of calcium in oviparous snakes increases during the interval of greatest embryonic growth (stage 35 to parturition). However, the pattern of embryonic calcium acquisition is unknown for viviparous snakes. Furthermore, while the uterus of oviparous species transports calcium early in embryonic development during mineralization of the eggshell, the timing of uterine calcium secretion in viviparous snakes is unknown. We studied a viviparous snake, Virginia striatula, to determine the ontogenetic pattern of yolk and embryonic calcium content. The pattern of embryonic calcium uptake of V. striatula is similar to that of oviparous snakes but the sources of calcium differ. In contrast to oviparous species, embryos of V. striatula acquire half of total neonatal calcium via placental provision, of which 71% is mobilized between stage 35 and parturition. Furthermore, we report for the first time in a viviparous squamate an increase in yolk calcium content during early stages of embryonic development, indicating that uterine secretion of calcium occurs in V. striatula coincident with shelling in oviparous squamates. Thus, uterine calcium secretion in this viviparous species may either occur continuously or in two phases, coincident with the timing of shelling in oviparous species and again during the last stages of development. Whereas, the pattern of embryonic calcium acquisition in V. striatula is plesiomorphic for squamates, the pattern of uterine calcium secretion includes both retention of a plesiomorphic trait and the evolution of a novel trait.

Disappearance of eggs during gestation in a viviparous snake ( Vipera aspis ) detected using non-invasive techniques

th August. Abstract. The number of eggs released at ovulation may be greater than the number of offspring born, if some of these ovulated eggs and/or embryos disappear during ges - tation. Although this process can potentially exert significant effects on reproductive output, logistical problems have discouraged studies on the disappearance of eggs and embryos in most kinds of vertebrates. Nuclear Magnetic Resonance (NMR) imaging and ultrasound Doppler-imaging have not been applied previously to such questions. Using these techniques, we monitored changes in the female's oviduct through gestation in a viviparous snake. We documented a case of disappearance of two ovulated eggs (from a litter of four) in the aspic viper, Vipera aspis. The female ovulated four normal- sized eggs, two of which contained living embryos when examined by NMR and ultra - sound Doppler-imaging early in gestation. Subsequent NMR imaging midway through gestation showed the same situation, but a third imaging session immediately prior to parturition revealed that the oviducts contained only the two live embryos. The two nonviable eggs had disappeared. The female gave birth to the two live offspring, with no evidence of any additional material. These data thus offer the strongest evidence so far available for egg disappearance (resorption?) during gestation in reptiles. More gen - erally, NMR imaging offers a valuable tool for investigating processes inside the body cavity, where direct observation is otherwise difficult or impossible. The technique does not require sacrifice of the animals, and hence allows dynamic investigations over time.

The Physiological Cost of Pregnancy in a Tropical Viviparous Snake

During pregnancy, the metabolic rate of females may increase above basal levels to support metabolically active tissues and developing embryos. In mammals, this energetic cost of supporting the pregnancy (MCP) is an important component of reproductive effort, but less is known about the magnitude of this cost in ectothermic vertebrates. We estimated the metabolic cost of supporting pregnancy in a tropical viviparous snake, the Northern Death Adder, Acanthophis praelongus. We measured the metabolic rates of non-gravid and gravid females throughout gestation and following parturition. We also measured the oxygen consumption of a sample of neonates from each clutch within 24 h of birth. The metabolic rate of gravid females rose slowly during pregnancy, but was significantly elevated during the last three weeks of gestation. Considering the late term metabolism of gravid females as 100%, then the baseline metabolism of female Death Adders represented 36.6%, embryo metabolism accounted for 37.0%, and the cost of supporting the pregnancy was 26.4% of the total metabolic rate. Neonate metabolism during the first 24 h of birth was 2.9 times higher than the estimate for embryo metabolism. Thus, our results do not support the assumption that the metabolism of embryos (prior to birth) and neonates is similar in this species. Although gravid female Death Adders maintain high and constant body temperatures during late gestation, the energetic cost of supporting the pregnancy is only a minor component of the total reproductive effort for females of this species.

Scanning electron microscopy of the fetal membranes of an oviparous squamate, the corn snake Pituophis guttatus (Colubridae)

Although the fetal membranes of viviparous squamates have received much study, morphology of their homologues among oviparous reptiles is poorly understood. The scarcity of information about these membranes in egg-laying reptiles hampers attempts to distinguish specializations for viviparity from ancestral oviparous features. We used scanning electron microscopy to examine fetal membranes of an oviparous snake (Pituophis guttatus) throughout the developmental period from oviposition to hatching. The external surface of the chorion contains broad, flattened cells that lack surface features; these cells form a continuous layer over the allantoic capillaries and offer a minimal barrier to respiratory exchange. In contrast, the surface epithelium of the omphalopleure bears elaborate surface ridges suggestive of absorptive capabilities. These ridges are prominent in the first few weeks after oviposition, but diminish thereafter. During development, the isolated yolk mass (IYM) of the omphalopleure becomes depleted, and the tissue becomes heavily vascularized by allantoic vessels. Surface features of the omphalopleure progressively take on the appearance of the chorioallantois, but the changes are not synchronous with loss of the IYM or membrane vascularization. Previous studies on viviparous snakes suggest that the chorioallantois and omphalopleure are respectively specialized for gas exchange and absorption in the intrauterine environment. Our studies of fetal membranes in P. guttatus offer evidence that cytological specializations for these functions originated under oviparous conditions, reflecting functional capacities that predate viviparity.

Modelling the distribution of the Boid snakes, Epicrates cenchria alvarezi and Boa constrictor occidentalis in the Gran Chaco (South America)

AbstractThe viviparous snake species Epicrates cenchria alvarezi and Boa constrictor occidentalis inhabit the Gran Chaco region of South America. Ecological factors determining their distribution are poorly known. GIS-based modelling of a species' environmental requirements using occurrence records provides essential information of the species' distribution. We modelled the geographical distribution of E. c. alvarezi and B. c. occidentalis in the Gran Chaco and analyzed the degree to which their distribution is associated with different environmental variables (precipitation, normalized difference vegetation index (NDVI), land surface temperature and altitude) using Logistic Regression Analysis. We found that E. c. alvarezi and B. c. occidentalis would be more frequent in areas with high levels of NDVI (positive relationship with NDVI1), with low levels of precipitation (negative relationship with PRE1) and with lower altitude (negative relationship with ALT). However, the analysis also revealed specific differences in the environmental requirements of the snakes, showing that B. c. occidentalis is more frequent than E. c. alvarezi at sites with higher levels of NDVI. Additionally, E. c. alvarezi is more frequent at sites with lower temperatures in the dry season. The maps obtained show that both are highly likely to be present in the Dry subregion of the Gran Chaco. The results of the present study can be an important contribution to a better understanding of the ecological requirements of the species and of the impact of global environmental change on its distribution.

Influence of income and capital on reproduction in a viviparous snake: direct and indirect effects

Influence of income and capital on reproduction in a viviparous snake: direct and indirect effects

Income breeding allows an aquatic snake Seminatrix pygaea to reproduce normally following prolonged drought‐induced aestivation

1. Capital breeding is an ideal reproductive strategy for many ectotherms because it provides a disassociation between feeding and reproduction, a necessary requirement for animals that become anorexic during pregnancy. Among ectotherms, some viviparous snakes (e.g. Viperidae) exemplify the capital breeding strategy because many species (i) do not feed during pregnancy due to behavioural conflicts between reproduction and foraging, and (ii) take more than one season to accumulate sufficient energetic stores for reproduction. 2. Isolated wetlands often exhibit extreme annual fluctuations in environmental conditions with prolonged droughts periodically leaving wetlands completely dry and devoid of prey. Following droughts, however, wetlands can be extremely productive, rendering prey resources virtually unlimited for some species. 3. This study examines drought survival strategy and reproductive ecology of a small aquatic snake Seminatrix pygaea (Cope) in an isolated wetland. Seminatrix pygaea are atypical from most sympatric snake species in that (i) their small body size, reliance on aquatic prey, and high rates of evaporative water loss make them ill-suited to overland movement, and (ii) they may not be subject to costs typically associated with feeding during pregnancy. 4. We hypothesized that S. pygaea would survive periodic multiyear droughts by aestivating within the dried wetland, a survival strategy heretofore undocumented in snakes. Further, we hypothesized that if S. pygaea rely on 'typical' snake reproductive strategies of 'adaptive anorexia' and capital breeding, reproductive output would be reduced in the first wet year following drought. 5. By encircling a 10-ha wetland with a continuous drift fence before it refilled we were able to demonstrate that S. pygaea were present within the dried wetland prior to the onset of spring rains that refilled the wetland in 2003. Our results suggest that S. pygaea are capable of surviving multiyear droughts by aestivating within the dried wetland. 6. Despite having presumably depleted energy reserves during the drought, S. pygaea reproduced with the same frequency and fecundity during the first season following refilling of the wetland as in pre-drought years. 7. The ability of S. pygaea to rebound rapidly from the stresses of prolonged drought is due in part to their reproductive ecology. Seminatrix pygaea readily feed throughout pregnancy and consequently can rapidly translate high prey abundances into reproductive output through income breeding.

Influence of income and capital on reproduction in a viviparous snake: direct and indirect effects

AbstractA central issue in life‐history studies is the extent to which organisms are ‘capital’ versus ‘income’ breeders (i.e. using stored resources vs. current food intake). Snakes are primarily capital breeders, but income during vitellogenesis can also contribute to reproductive output. In Manitoba, the garter snake Thamnophis sirtalis has a short active season, with mating occurring upon emergence from hibernation and vitellogenesis shortly thereafter. Given the brevity of this sequence, animals in these populations should be almost exclusively capital breeders. Consistent with this prediction, in this experiment the reproductive output of recently mated snakes was influenced by mass of the mother at the time of mating but not by her food intake shortly after mating. Food eaten during pregnancy contributed significantly to postpartum mass but not to litter mass. However, the initial mass of snakes influenced both postpartum and litter mass. For snakes given a high ration of food, a female's relative mass (i.e. adjusted for body length) significantly influenced the actual amount she consumed (relatively lighter snakes ate more). Perhaps most important, among pregnant snakes, those that were initially relatively heavier gave birth substantially and significantly earlier. Thus, snakes that are relatively heavy when they mate may gain further fitness benefits following pregnancy (e.g. more time to acquire resources and for offspring to grow before winter), which can also be interpreted as indirect effects on reproduction. These life‐history variations may be relevant to population dynamics.

Evidence for Selection on Thermoregulation: Effects of Temperature on Embryo Mortality in the Garter SnakeThamnophis elegans

Abstract Despite widespread belief that selection molds thermoregulatory behaviors, direct evidence for fitness effects is extremely rare. We studied the effect of developmental temperature on embryo mortality in a viviparous snake. Seventy-four female Thamnophis elegans were maintained at one of nine constant temperatures during pregnancy (21–33 C). The duration of pregnancy was recorded for each female as well as the sex, snout–vent length, mass, and survival of 504 newborns. Embryo survival was highest at an intermediate temperature (26.6 C). The developmental temperature of maximum survivorship in T. elegans corresponds to the temperature that induces minimum developmental abnormality and the optimum temperature for whole organism performance. These three thermal optima together correspond with the average temperatures imposed on embryos by free-ranging pregnant females (26.6 C). This correspondence implies that thermal optima are coadapted to thermoregulation in T. elegans.

The effects of body size, age, and food intake during pregnancy on reproductive traits of a viviparous snake, Thamnophis ordinoides

:Litter characteristics of viviparous snakes presumably can be influenced by the mother’s state (e.g., mass) at the onset of pregnancy, by food acquired during vitellogenesis, or by food eaten by the mother during pregnancy and delivered to the developing embryos via the placenta. Alternatively, food consumed while pregnant could be allocated to the female herself, potentially influencing her future survivorship and/or reproduction. We tested the effects of food consumption during pregnancy on litter traits of the garter snake, Thamnophis ordinoides, along with the effects of body size and age of mother. We also measured trade-offs between traits. Age was significantly correlated with body size of female snakes, but it had no direct influence on reproductive traits. Initial body size, by contrast, especially snout-vent length, significantly and positively influenced litter size and mass. Food intake by gravid females declined during pregnancy, and snakes became relatively anorexic prior to giving birth; their appetite resumed following parturition. Snakes offered smaller amounts of food while pregnant ate less than those fed ad lib, but had similar postpartum appetites. Higher food intake during pregnancy resulted in higher postpartum mass of females, but not higher litter mass or size of offspring. There was strong evidence of a trade-off between litter size and offspring size and between postpartum mass and litter mass. Overall, our data are consistent with the hypothesis that reproductive traits of viviparous snakes are determined proximately by previously accumulated stores (capital) and/or food consumed during vitellogenesis (income), but not by resources acquired during pregnancy.

Climate affects embryonic development in a viviparous snake, Vipera aspis

Climatic conditions during embryonic development can exert profound and long‐term effects on many types of organisms, but most previous research on this topic has focussed on endothermic vertebrates (birds and mammals). Although viviparity in ectothermic taxa allows the reproducing female to buffer ambient thermal variation for her developing offspring, even an actively thermoregulating female may be unable to provide optimal incubation regimes in severe weather conditions. We examined the extent to which fluctuations in natural thermal conditions during pregnancy affect reproduction in a temperate viviparous snake, the aspic viper (Vipera aspis). Data gathered from a long term field study demonstrated that ambient thermal conditions influenced (1) female body temperatures and (2) gestation length, embryo viability, and offspring phenotypes. Interestingly, thermal conditions during each of the three months of gestation affected different aspects of reproduction. Hotter weather early in gestation (June) increased ventral scale counts (=number of body segments) of neonates; hotter weather mid‐gestation (July) hastened development and thus the date of parturition; and hotter weather late in gestation (August) reduced the incidence of stillborn neonates. The population that we studied is close to the northern limit of the species’ range, and embryonic thermal requirements may prevent Vipera aspis from extending into cooler conditions further north.

Histology of the extraembryonic membranes of an oviparous snake: towards a reconstruction of basal squamate patterns.

An understanding of the evolutionary morphology of extraembryonic membranes in reptiles requires information about oviparous as well as viviparous species. We are studying histology and ultrastructure of the extraembryonic membranes of snakes to clarify the evolutionary history of reptilian fetal membranes, including determination of basal (ancestral) ophidian and squamate patterns. Microscopic anatomy of the membranes of oviparous corn snakes (Elaphe guttata) was examined using light and electron microscopy. At mid-development the inner surface of the eggshell is lined by two extraembryonic membranes, the chorioallantois and the omphalallantoic membrane. The chorioallantois consists of a bilayered cuboidal epithelium that overlies the allantoic blood vessels. During development, allantoic capillaries become more abundant, and the chorionic epithelium thins, decreasing the diffusion distance for respiratory gas exchange. The abembryonic pole of the egg is delimited by a bilaminar omphalopleure and isolated yolk mass, the latter of which is lined on its inner face by the allantois. The isolated yolk mass regresses developmentally, and patches of yolk droplets become isolated and surrounded by allantoic blood vessels. By late development, the abembryonic hemisphere has been fully vascularized by allantoic vessels, forming a "secondary chorioallantois." With regard to its extraembryonic membranes, Elaphe gutatta is similar to viviparous snakes. However, this species exhibits features that have not previously been reported among squamates, perhaps reflecting its oviparous reproductive habits. Morphological evidence for the uptake of eggshell material by epithelia of the chorion and omphalopleure suggests that the potential for absorption by extraembryonic membranes predates the origin of viviparity.

Ultrastructure of the placentae of the natricine snake, Virginia striatula (Reptilia: Squamata).

Virginia striatula is a viviparous snake with a complex pattern of embryonic nutrition. Nutrients for embryonic development are provided by large, yolked eggs, supplemented by placental transfer. Placentation in this species is surprisingly elaborate for a predominantly lecithotrophic squamate reptile. The embryonic-maternal interface consists of three structurally distinct areas, an omphalallantoic placenta and a regionally diversified chorioallantoic placenta. The chorioallantoic placenta over the embryonic hemisphere (paramesometrial region) of the egg, features close apposition of embryonic and uterine blood vessels because of the attenuate form of the interceding epithelial cells. The periphery of the chorioallantoic placenta, which is adjacent to the omphalallantoic placenta, is characterized by a simple cuboidal uterine epithelium apposed to a stratified cuboidal chorionic epithelium. There are no sites with attenuate epithelial cells and close vascular apposition. The morphology of the omphalallantoic placenta is similar to that of the peripheral chorioallantoic placenta, except that the height of uterine epithelial cells is greater and allantoic blood vessels are not associated with the embryonic epithelium. The functional capabilities of the three placental regions are not known, but structural characteristics suggest that the omphalallantoic placenta and peripheral zone of the chorioallantoic placenta are sites of nutritional provision via histotrophy. The paramesometrial region of the chorioallantoic placenta is also nutritive, in addition to functioning as the primary embryonic respiratory system. The structure of the chorioallantoic placenta of V. striatula is a new placental morphotype for squamate reptiles that is not represented by a classic model for the evolution of reptilian placentation.

Capital‐breeding and reproductive effort in a variable environment: a longitudinal study of a viviparous snake

1 The ways that fluctuations in prey abundance and weather conditions can affect reproductive output in a ‘capital breeding’ ectotherm, the aspic viper (Vipera aspis) were examined. 2 Our longitudinal study confirms that female aspic vipers adjust reproductive investment by integrating allocations of energy from stores (‘capital’) and facultative feeding (‘income’). Thus, long-term energy storage enabled females to reproduce successfully even in years when prey were scarce. 3 Not surprisingly, temporal changes in body reserves of female vipers preparing for reproduction depended upon current feeding rates. However, the mean environmental temperature during the active season also affected mass gain. 4 Allometric patterns suggest that reproductive output was limited by energy availability in 8 out of the 9 years of our study. In the other year, high prey availability in the preceding season meant that reproductive output was maximized within the constraints set by maternal body size (and thus, abdominal volume). 5 High summer temperatures increased basking opportunities of gravid vipers and thus accelerated gestation. However, maternal metabolic costs also increased in such situations, resulting in low postpartum body condition.

Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis)

Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis)

Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis)

Spontaneous anorexia has been documented in various animal species and is usually associated with activities competing with food intake. In natural conditions, most female aspic vipers (Vipera aspis) stop feeding during the two months of pregnancy. We carried out a simple experiment on 40 pregnant females to determine whether anorexia was obligatory or facultative, and to investigate the energetic consequence of fasting on post-partum body condition and litter traits. Three diet treatments were applied during gestation: no food, one feeding occasion, and two feeding occasions. Twelve nonpregnant, unfed females were used as a control group. Most gravid females accepted captive mice during gestation, suggesting that anorexia reported in the field was a side effect of the tremendous changes in activity pattern associated with pregnancy. Mass loss was high for unfed reproductive females, indicating high energy expenditure associated with embryo maintenance. Prey consumption allowed compensation for metabolic expenditure and enhanced post-partum female body condition, but had no effects on litter characteristics. The magnitude of the metabolic expenditure during gestation appeared to be independent of fecundity.

Phenotypic plasticity in reproductive traits: geographical variation in plasticity in a viviparous snake

Summary Previous experiments showed that Checkered Garter Snakes (Thamnophis marcianus) from south Texas, USA (an environment subject to high seasonal and annual variation in environmental conditions), demonstrated marked phenotypic plasticity in clutch size and clutch mass in response to experimental changes in prey availability. In this study, the extent of phenotypic plasticity in life‐history traits in Checkered Garter Snakes from south Texas was experimentally compared with a population of the same species from south‐eastern Arizona, where the environment may be more constant. Unlike results from south Texas, Checkered Garter Snakes from Arizona showed no significant phenotypic plasticity in clutch size, clutch mass or any other life‐history trait in response to changes in food availability, at least within the boundaries of our experimental conditions. The data indicate that the degree of phenotypic plasticity in life‐history traits differs among populations within the same species. However, these differences are subject to both adaptive and non‐adaptive explanations.