Guy Naulleau

The dangers of leaving home: dispersal and mortality in snakes

For animal populations in many parts of the world, direct (albeit often accidental) killing by humans may be a significant source of mortality. Many snakes are killed by people (especially by automobiles) every year, but the determinants of a snake’s vulnerability to anthropogenic mortality (and thus, patterns of mortality with respect to sex, age and season) are poorly known. We present data on 652 French snakes of six species (Coluber viridiflavus, Elaphe longissima, Natrix maura, N. natrix, Vipera aspis, V. berus) killed either by natural predators, domestic animals or humans (including roadkills). We used information on seasonal patterns of mortality (plus information on population structure from 338 captures of live snakes) to test the hypothesis that snakes are killed mostly when they disperse from their usual home ranges. This hypothesis generates several falsifiable predictions on the expected correlates of mortality rates; most of these predictions are supported by our data. For example, young-of-the-year snakes are killed primarily in the period immediately after hatching (while they disperse); subadults (which are sedentary) generally experience low mortality rates; adult males are killed mainly during the mating season (especially in species where mate-searching males travel widely); and adult females in oviparous species are killed during their egg-laying migrations. Relative to population density, species that use frequent long-distance movements in foraging experience higher mortality than sedentary ambush foragers. In one species (E. longissima), larger males are more at risk. The success of these predictions suggests that movement patterns of snakes may oAer valuable indices of their vulnerability to direct anthropogenic mortality. # 1999 Elsevier Science Ltd. All rights reserved.

Are snake populations in widespread decline

Long-term studies have revealed population declines in fishes, amphibians, reptiles, birds and mammals. In birds, and particularly amphibians, these declines are a global phenomenon whose causes are often unclear. Among reptiles, snakes are top predators and therefore a decline in their numbers may have serious consequences for the functioning of many ecosystems. Our results show that, of 17 snake populations (eight species) from the UK, France, Italy, Nigeria and Australia, 11 have declined sharply over the same relatively short period of time with five remaining stable and one showing signs of a marginal increase. Although the causes of these declines are currently unknown, we suspect that they are multi-faceted (such as habitat quality deterioration, prey availability), and with a common cause, e.g. global climate change, at their root.

Body condition threshold for breeding in a viviparous snake

One major goal of physiological ecology is to seek links between life history traits. Identification of a body condition threshold for breeding (e.g. critical level of body reserves) provides a link between the physiological process involved in storage of body reserves and the ability to reproduce. One hundred and twenty-nine freeranging adult female Vipera aspis, a viviparous snake, were marked with electronic identification tags and/or by scale clipping, weighed, and measured at the onset of vitellogenesis, and immediately released in the field in western central France (47°03′N; 02°00′W). The 129 snakes were recaptured 2–6 months later between ovulation and parturition, and individual reproductive status was then determined. Eighty-four females (65%) captured at the onset of vitellogenesis became vitellogenic, 45 did not. There was no difference in mean body length between reproductive and non-reproductive females. Initial body condition influenced reproductive outcome: we found a precise threshold in body condition necessary for the induction of vitellogenesis. Almost all females (88%) with a body condition greater than the observed threshold became vitellogenic, 12% did not, and no female with a body condition under the threshold became vitellogenic. Body reserves were estimated in the 129 living females using data gathered on 69 autopsied females. Females which became vitellogenic had large body reserves, but females which did not were not particularly emaciated (whilst postparturiant females had few body reserves remaining). This precise condition threshold for breeding is discussed in terms of the reproductive ecology of this species.

Sexual dimorphism in snakes: different reproductive roles favour different body plans

Because snakes have a highly simplified morphology, and many species have a wide (and broadly overlapping) range of adult body sizes within each sex, they offer an excellent opportunity to compare body composition of males and females. Evolutionary theory predicts that particular body components should be differentially enlarged in the two sexes. For example, we might expect the reproductive success of females to be enhanced by enlargement of organ systems involved in the processing and storage of energy (e.g. alimentary tract, liver, fat stores) whereas males would benefit from the enlargement of systems important for mate–searching, male–male combat and sperm competition (e.g. larger mass of skeletal muscles, tail, and kidneys). Dissection of 243 specimens of three snake species (117 Vipera aspis, 43 Elaphe longissima, 83 Coluber viridflavus) broadly supported these predictions. Strong sex differences were apparent in relative sizes (masses) of all the non–gonadal body components that we weighed. For example, males consistently had more musculature (relative to body length) than did conspecific females. Dimorphism in relative muscle mass is likely to be one of the most fundamental and widespread morphological differences between males and females in the Animal Kingdom.

The Effects of Temperature on Digestion in Vipera aspis

(France) ABSTRACT. -The effects of temperature on digestion were studied in Vipera aspis at different temperatures, between 10 and 35?C. At 10?C, all prey was regurgitated. Regurgitation rate declined to 56% at 15?C and then remained approximately less than 10% at 20, 25, 30 and 35?C. The duration of digestion shortened as temperature rose; the Q 10 decreased progressively between 15 and 35?C. The mass of the prey in absolute terms or as a function of the mass of the viper had relatively little effect on the duration of digestion. The number of fecal pellets decreased with increasing temper- ature, but the percentage of wet initial mass of prey excreted was independent of temperature. Feeding was dependent on the temperature at which the vipers were kept. The incidence of food acceptance increased from 40% and 9% at 15 and 20?C, respectively, to 85% and 100% at 25 and 30?C.

What is the appropriate timescale for measuring costs of reproduction in a 'capital breeder' such as the aspic viper?

Before we can quantify the degree to which reproductive activities constitute a cost (i.e., depress an organisms probable future reproductive output), we need to determine the timescale over which such costs are paid. This is straightforward for species that acquire and expend resources simultaneously (income breeders), but more problematical for organisms that gather resources over a long period and then expend them in a brief reproductive phase (capital breeders). Most snakes are capital breeders; for example, female aspic vipers (Viperaaspis) in central western France exhibit a 2- to 3-year reproductive cycle, with females amassing energy reserves for one or more years prior to the year in which they become pregnant. We use long-term mark-recapture data on free-living vipers to quantify the appropriate timescale for studies of reproductive costs. Annual survival rates of female vipers varied significantly during their cycle, such that estimates of survival costs based only on years when the females were ‘reproductive’ (i.e., produced offspring) substantially underestimated the true costs of reproduction. High mortality in the year after reproducing was apparently linked to reproductive output; low energy reserves (poor body condition) after parturition were associated with low survival rates in the following year. Thus, measures of cost need to consider the timescale over which resources are gathered as well as that over which they are expended in reproductive activities. Also, the timescale of measurement needs to continue long enough into the post-reproductive period to detect delayed effects of reproductive ‘decisions’.

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.

Plastic vipers: influence of food intake on the size and shape of Gaboon vipers (Bitis gabonica)

Repeated measurements of captive-born Gaboon vipers Bitis gabonica from an inbred stock examined the degree to which an animal’s size and shape are affected by food intake. We also used the level of asymmetry in dorsal coloration as an index for possible genetic (inbreeding?) effects. Both of these factors, and the interaction between them, affected phenotypes of the young snakes. Snakes raised with abundant food differed from their less well-fed siblings not only in size, but also in body mass relative to snout‐vent length, head length relative to snout‐vent length, head width relative to head length, and fang length relative to jaw length. Hence, our data show that body proportions (including the feeding apparatus) can be influenced by the environment after birth.

Annual cycles in plasma testosterone and thyroxine in the male aspic viper Vipera aspis L., (Reptilia, Viperidae), in relation to the sexual cycle and hibernation

Blood samples were taken monthly from males of Vipera aspis kept in outdoor terraria. Plasma testosterone was estimated by radioimmunoassay and plasma thyroxine by the technique of isotopic competition, between October 1979 and September 1985. Plasma testosterone showed an annual bimodal profile. The highest peak was observed from February 15 to the end of March. 2 to 5 weeks after the first emergence from hibernation. Values then decreased greatly, to reach a minimum level when the vernal spermiogenesis was at its maximum. The secondary peak of plasma testosterone was lower and less well marked. It occurred at the end of summer, during the strongest spermiogenesis, and preceded the autumnal facultative mating period. Plasma thyroxine was at a maximum concentration from February to March after which levels decreased markedly. The seasonal profile of plasma thyroxine was clearly marked during the period of hibernation. From September to October, 2 months before the beginning of hibernation, thyroxine levels began to decrease, and they reached a minimum in November-December. Endocrine reactivation of the thyroid appeared at the end of hibernation. However, in contrast to the plasma testosterone, endocrine activity of the thyroid began 2 to 3 weeks before the end of hibernation. Mechanisms of reactivation for testicular and thyroidal endocrine structures are discussed.

Reproductive ecology, body fat reserves and foraging mode in females of two contrasted snake species: Vipera aspis (terrestrial, viviparous) and Elaphe longissima (semi-arboreal, oviparous)

The reproductive ecology of two snakes, female Vipera aspis (terrestrial) and Elaphe longissima (semi-arboreal), was compared. Mean clutch sizes were close in the two species; 6.17 ± 2.50 (n = 69) in the asp viper, and 6.59 ± 1.38 (n = 29) in the Aesculapian snake. When controlled for body size, body condition (hence amounts of body reserves), measured at the beginning of vitellogenesis, correlated positively with litter size in the asp viper but with clutch size in the Aesculapian snake. As in most species, maternal body length positively influenced clutch or litter size. Thus, the trade-off between maternal reserves and growth may favour reserves in the asp viper, and growth in the Aesculapian snake. The asp viper is a bi- or triennial breeder (33% of reproductive-females each year), the Ausculapian snake is an annual breeder (77% of reproductive females each year). These differences may be related to their contrasting foraging ecology. The asp viper is a terrestrial ambush predator with a specialized diet (98% Microtus) based on un-predictable prey availability. This species moves slowly (9.07 ± 8.40 m/day during the active season), and has a small home range (3,024 m 2 ); an increasing body mass (large body reserves) should not affect its activity abilities. The Aesculapian snake is a semi-arboreal predator, which feeds on a large range of prey including birds and eggs, and which is often active (118, 11 ± 134,55 m/day during the active season). This species has a large home range (11,400 m 2 ); an increasing body mass (large body reserves) should be a handicap during arboreal displacements. Vitellogenesis depends on body reserves in the asp viper, while it depends on foraging success in the Aesculapian snake.