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.     

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.     

Gestation, thermoregulation, and metabolism in a viviparous snake, Vipera aspis: evidence for fecundity-independent costs

Oxygen consumption of gestating Aspic vipers, Vipera aspis (L.), was strongly dependent on body temperature and mass. Temperature-controlled, mass-independent oxygen consumption did not differ between pregnant and nonpregnant females. Maternal metabolism was not influenced during early gestation by the number of embryos carried but was weakly influenced during late gestation. These results differ from previous investigations that show an increase in mass-independent oxygen consumption in reproductive females relative to nonreproductive females and a positive relationship between metabolism and litter size. These data also conflict with published field data on V. aspis that show a strong metabolic cost associated with reproduction. We propose that, under controlled conditions (i.e., females exposed to precise ambient temperatures), following the mobilisation of resources to create follicles (i.e., vitellogenesis), early gestation per se may not be an energetically expensive period in reproduction. However, under natural conditions, the metabolic rate of reproductive females is strongly increased by a shift in thermal ecology (higher body temperature and longer basking periods), enabling pregnant females to accelerate the process of gestation. Combining both laboratory and field investigation in a viviparous snake, we suggest that reproduction entails discrete changes in the thermal ecology of females to provide optimal temperatures to the embryos, whatever their number. This results in the counterintuitive notion that metabolism may well be largely independent of fecundity during gestation, at least in an ectothermic reptile.     

Geographic variation of body size and reproductive patterns in Continental versus Mediterranean asp vipers, Vipera aspis

The occurrence of variation in body size and reproductive traits of Vipera aspis was assessed by analysing 74 reproductive females of different populations, collected throughout a large part of the distribution range of the taxon, from central‐western France to central Italy. Six populations were analysed, two of plain habitats, in France and Italy, characterized by a Continental climate, whereas the other four derived from two coastal and two inland, hilly Italian habitats, respectively, showing a Mediterranean climate. Females of the French area showed the smallest mean body size, whereas the pre‐ and post‐partum body masses of females from the coolest, central Italic area were significantly higher. Litter size varied among habitats and was significantly correlated with maternal body size. If the snout–vent length feature varied largely among offspring of different habitats (with the longest size occurring in representatives of the coastal, central Italian area), the average of both body mass and total mass of offsprings did not exhibit any clear pattern among populations colonizing different habitats. Nevertheless, relative litter mass was higher in the French continental populations, and lower in the coolest, Mediterranean, Italian ones. It is worth emphasizing the positive correlation between the snout–vent length feature of females and the total litter mass to environmental factors, such as hottest month temperature and total rainfall. The available literature records that female body size affects offspring size and fecundity. If the present study bolsters this correlation, it also rules out any other effect of female body size on the offspring characteristics analysed. Finally, evidence is provided for the role of climatic factors on life‐history traits (e.g. pre‐partum body mass) of asp vipers, although confounding effects pursued, for example, by food availability may occur. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96 , 383–391.     

Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis

Body size can influence an organism's microevolutionary fitness either via ecological factors (ecological selection) or changes in reproductive output (sexual or fecundity selection). Published studies on sexual dimorphism in reptiles have generally focussed on sexual-selective forces on males, under the implicit assumption that the intensity of fecundity selection in females (and hence, overall selection on female body size) is likely to be relatively consistent among lineages. In this paper, we explore the degree to which larger body size enhances ecological attributes (e.g., food intake, growth, survival) and reproductive output (reproductive frequency, litter size, offspring size, offspring viability) in free-ranging female aspic vipers, Vipera aspis . The less-than-annual reproductive frequency of these animals allows us to make a direct comparison between females in years during which they concentrate on "ecological" challenges (especially building energy reserves) versus reproductive challenges (producing a litter). Because female snakes have limited abdominal space to hold the clutch (litter), we expect that fecundity should depend on body size. However, our data show that larger body size had a more consistent effect on ecological attributes (such as feeding rates and "costs of reproduction") than on reproductive output per se. Indeed, total reproductive output was maximised at intermediate body sizes. These results suggest that variation in female body size among and within species (and hence, in the degree of sexual dimorphism) may be driven by the ecological as well as reproductive consequences of body size variation in both sexes.     

An agonist of CXCR4 induces a rapid recovery from the neurotoxic effects of Vipera ammodytes and Vipera aspis venoms

People bitten by Alpine vipers are usually treated with antivenom antisera to prevent the noxious consequences caused by the injected venom. However, this treatment suffers from a number of drawbacks and additional therapies are necessary. The venoms of Vipera ammodytes and of Vipera aspis are neurotoxic and cause muscle paralysis by inducing neurodegeneration of motor axon terminals because they contain a presynaptic acting sPLA₂ neurotoxin. We have recently found that any type of damage to motor axons is followed by the expression and activation of the intercellular signaling axis consisting of the CXCR4 receptor present on the membrane of the axon stump and of its ligand, the chemokine CXCL12 released by activated terminal Schwann cells. We show here that also V. ammodytes and V. aspis venoms cause the expression of the CXCL12-CXCR4 axis. We also show that a small molecule agonist of CXCR4, dubbed NUCC-390, induces a rapid regeneration of the motor axon terminal with functional recovery of the neuromuscular junction. These findings qualify NUCC-390 as a promising novel therapeutics capable of improving the recovery from the paralysis caused by the snakebite of the two neurotoxic Alpine vipers.

     

Short-term and long-term effects of food supply on parasite burdens in Tawny Owls, Strix aluco

1. The relationships among food supply (Field Voles, Microtus agrestis ), reproduction and blood parasites was investigated in Tawny Owls, Strix aluco , in Kielder Forest, Northumberland, in 1994 and 1995. Vole populations were significantly lower in 1995 than in 1994.
2. Birds did not lose parasites after initial infection, and the level at which infections were maintained was characteristic of individual birds.
3. In 1994, the number and intensity of parasites was higher in adult owls that had experienced low food supply when they themselves were reared. This indicated that food supplied to chicks in the nest has a long-term effect on the parasite burden of adults.
4. In addition, there was evidence that parasite burdens of adults were influenced by their current food supply. Birds that suffered a decline in food abundance on their territories between 1994 and 1995 showed an increase in parasite load over the same period. In 1995, there was also a significant negative correlation between the parasite loads of owls and vole abundance on their territories.
5. The best predictor of parasite number of chicks reared in 1995 was the parasite load of their fathers. The parasites chicks developed were not the parasites with which their fathers were heavily infested. This result could be due to inherited immunity.
6. Our results indicated that food resources should be measured when investigating interactions between parasites and their hosts, and that offspring quality as well as quantity might suffer when food abundance is low.     

Sequences and structural organization of phospholipase A2 genes from Vipera aspis aspis, V. aspis zinnikeri and Vipera berus berus venom. Identification of the origin of a new viper population based on ammodytin I1 heterogeneity.

We used a PCR-based method to determine the genomic DNA sequences encoding phospholipases A2 (PLA2s) from the venoms of Vipera aspis aspis (V. a. aspis), Vipera aspis zinnikeri (V. a. zinnikeri), Vipera berus berus (V. b. berus) and a neurotoxic V. a. aspis snake (neurotoxic V. a. aspis) from a population responsible for unusual neurotoxic envenomations in south-east France. We sequenced five groups of genes, each corresponding to a different PLA2. The genes encoding the A and B chains of vaspin from the neurotoxic V. a. aspis, PLA2-I from V. a. zinnikeri, and the anticoagulant PLA2 from V. b. berus are described here. Single nucleotide differences leading to amino-acid substitutions were observed both between genes encoding the same PLA2 and between genes encoding different PLA2s. These differences were clustered in exons 3 and 5, potentially altering the biological activities of PLA2. The distribution and characteristics of the PLA2 genes differed according to the species or subspecies. We characterized for the first time genes encoding neurotoxins from the V. a. aspis and V. b. berus snakes of central France. Genes encoding ammodytins I1 and I2, described previously in Vipera ammodytes ammodytes (V. am. ammodytes), were also present in V. a. aspis and V. b. berus. Three different ammodytin I1 gene sequences were characterized: one from V. b. berus, the second from V. a. aspis, V. a. zinnikeri and the neurotoxic V. a. aspis, and the third from the neurotoxic V. a. aspis. This third sequence was identical with the reported sequence of the V. am. ammodytes ammodytin I1 gene. Genes encoding monomeric neurotoxins of V. am. ammodytes venom, ammodytoxins A, B and C, and the Bov-B LINE retroposon, a phylogenetic marker found in V. am. ammodytes genome, were identified in the genome of the neurotoxic V. a. aspis. These results suggest that the population of neurotoxic V. a. aspis snakes from south-east France may have resulted from interbreeding between V. a. aspis and V. am. ammodytes.     

Flock feeding and food intake in Little Egrets Egretta garzetta and their effects on food provisioning and reproductive success

Food provisioning to chicks of Little Egret Egretta garzetta in a colony at Ligagneau in the Camargue, southern France, was measured using electronic nest balances. Both pair members supplied food to the chicks, and each performed three to five alternating foraging trips. The loading rate during the first trip of the day (1.09 g/min) was more than three times as high as that during later trips (0.32 g/min) and accounted for 20% of the daily amount of food delivered. This food was collected while the birds were feeding in dense aggregations on mosquitofish which had become temporarily concentrated due to hypoxic conditions overnight in the surrounding marsh. Later in the day, when this concentrated food source was no longer available, the birds fed solitarily. The total amount of food delivered per day remained constant at 385 g as chick age increased from 10 to 20 days. Given the observed loading rates, 385 g is near the maximum amount of food the pair can deliver during a 16.5-h daylight period when they forage continuously throughout the day but only one parent at a time. This indicates that a time constraint limits the amount of food delivered to a brood during this stage of the breeding cycle. Given this time constraint, the total amount of food delivered per day would have been reduced by 25% if the birds had not been able to benefit from the concentrations of mosquitofish during the early morning. Breeding success was significantly higher at Ligagneau (3.25 chicks/nest) than in other Camargue colonies (2.69 chicks/nest). In addition, post-fledging survival of chicks with a low rank in the brood hierarchy was probably better at Ligagneau than elsewhere in the Camargue. We attribute this elevated reproductive output at Ligagneau to the exceptionally large amount of food collected by egrets during the early morning aggregations, which were probably formed in response to predictable concentrations of mosquitofish in the permanent marshes surrounding this colony. Such aggregations were rarely observed in the temporary marshes surrounding the other colonies, probably because the occurrence and location of fish concentrations are difficult to predict in this habitat due to rapidly falling water levels.     

Mating does not influence reproductive investment, in a viviparous lizard

Mating is crucial for females that reproduce exclusively sexually and should influence their investment into reproduction. Although reproductive adjustments in response to mate quality have been tested in a wide range of species, the effect of exposure to males and mating per se has seldom been studied. Compensatory mechanisms against the absence of mating may evolve more frequently in viviparous females, which pay higher direct costs of reproduction, due to gestation, than oviparous females. To test the existence of such mechanisms in a viviparous species, we experimentally manipulated the mating opportunity of viviparous female lizard, Lacerta (Zootoca) vivipara. We assessed the effect of mating on ovulation, postpartum body condition and parturition date, as well as on changes in locomotor performances and body temperatures during the breeding cycle. Female lizards ovulated spontaneously and mating had no influence on litter size, locomotor impairment or on selected body temperature. However, offspring production induced a more pronounced locomotor impairment and physical burden than the production of undeveloped eggs. Postpartum body condition and parturition dates were not different among females. This result suggests that gestation length is not determined by an embryonic signal. In the common lizard, viviparity is not associated with facultative ovulation and a control of litter size after ovulation, in response to the absence of mating.     

Transgenerational effects of food availability on age at maturity and reproductive output in an asexual collembolan species

Transgenerational effects of environmental conditions can have several important ecological and evolutionary implications. We conducted a fully factorial experiment manipulating food availability across three generations in the collembolan Folsomia candida, a springtail species that inhabits soil and leaf litter environments which vary in resource availability. Maternal and grandmaternal food availability influenced age at maturity and reproductive output. These effects appear to be cumulative rather than adaptive transgenerational life-history adjustments. Such cumulative effects can profoundly influence eco-evolutionary dynamics in both stable and fluctuating environments.     

Fat pad-specific effects of lipectomy on foraging, food hoarding, and food intake

Unlike most species, after food deprivation, Siberian hamsters increase foraging and food hoarding, two appetitive ingestive behaviors, but not food intake, a consummatory ingestive behavior. We previously demonstrated (Wood AD, Bartness TJ, Am J Physiol Regul Integr Comp Physiol 272: R783-R792, 1997) that increases in food hoarding are triggered by directly decreasing body fat levels through partial surgical lipectomy; however, we did not test if lipectomy affected foraging, nor if the magnitude of the lipid deficit affected food hoard size. Therefore, we tested whether varying the size of the lipectomy-induced lipid deficit and/or foraging effort affected foraging, food hoarding, or food intake. This was accomplished by housing adult male Siberian hamsters in a foraging/hoarding system and removing (x) both epididymal white adipose tissue (EWATx) pads, both inguinal white adipose tissue (IWATx) pads, or both EWAT and IWAT pads (EWATx + IWATx) and measuring foraging, food hoarding, and food intake for 12 wk. The lipectomy-induced lipid deficit triggered different patterns of white adipose tissue mass compensation that varied with foraging effort. Foraging for food (10 wheel revolutions to earn a food pellet) abolished the EWATx-induced compensation in IWAT pad mass. The magnitude of the lipid deficit did not engender a proportional change in any of the appetitive or consummatory ingestive behaviors. EWATx caused the greatest increase in food hoarding compared with IWATx or EWATx + IWATx, when animals were required to forage for their food. Collectively, it appears that the magnitude of a lipid deficit does not affect appetitive or consummatory behaviors; rather, when energy (foraging) demands are increased, loss of specific (gonadal) fat pads can preferentially stimulate increases in food hoarding.