Emily N. Taylor

Effects of food supplementation on the physiological ecology of female Western diamond-backed rattlesnakes (Crotalus atrox).

Food availability is an important factor in the life histories of organisms because it is often limiting and thus can affect growth, mass change, reproduction, and behaviors such as thermoregulation, locomotion, and mating. Experimental studies in natural settings allow researchers to examine the effects of food on these parameters while animals are free to behave naturally. The wide variation among organisms in energy demands and among environmental food resources suggest that responses to changes in food availability may vary among organisms. Since most supplemental feeding field experiments have been conducted on species with high energy demands, we conducted a supplemental feeding study on free-ranging, female Western diamond-backed rattlesnakes (Crotalus atrox), a species with low energy demands and infrequent reproductive investment. Snakes were offered thawed rodents 1–4 times per week. Over two active seasons, we collected data on surface activity, home range size, growth, mass change, and reproduction of supplementally fed and control snakes. Fed and control snakes did not differ in surface activity levels (proportion of time encountered above versus below ground) or home range size. Fed snakes grew and gained mass faster, and had a dramatically higher occurrence of reproduction than control snakes. Also, fed snakes were in better body condition following reproduction than snakes that were not fed. However, litter characteristics such as offspring number and size were not increased by feeding, suggesting that these characteristics may be fixed. These data experimentally demonstrate that food availability can directly impact some life history traits (i.e., growth and reproduction for C. atrox), but not others (i.e., surface activity and home range size for C. atrox). The relationship between food availability and life history traits is affected in a complex way by ecological traits and physiological constraints, and thus interspecific variation in this relationship is likely to be high.

When does a reproducing female viper (Vipera aspis) 'decide' on her litter size?

Some organisms rely on stored energy to fuel reproductive expenditure (capital breeders) whereas others use energy gained during the reproductive bout itself (income breeders). Most species occupy intermediate positions on this continuum, but few experimental data are available on the timescale over which food intake can affect fecundity. Mark–recapture studies of free-ranging female aspic vipers Vipera aspis have suggested that reproductive output relies not only on the energy in fat bodies accumulated in previous years, but also on food intake immediately before ovulation. A simple experiment was conducted to test this hypothesis, maintaining female snakes in captivity throughout the vitellogenic period and controlling their food intake. The energy input of a female strongly influenced the amount of mass that she gained and the number of ova that she ovulated. Multiple regression showed that litter size in these snakes was affected both by maternal body condition in early spring (an indicator of foraging success over previous years) and by food intake in the spring before ovulation. Our experimental data thus reinforce the results of descriptive studies on free-ranging snakes, and emphasize the flexibility of energy allocation patterns among vipers. Reproducing female vipers may combine energy from ‘capital’ and ‘income’ to maximize their litter sizes in the face of fluctuating levels of prey abundance.

The Relationship between Plasma Steroid Hormone Concentrations and the Reproductive Cycle in the Northern Pacific Rattlesnake, Crotalus oreganus

We describe the reproductive cycle of Northern Pacific rattlesnakes (Crotalus oreganus) by quantifying steroid hormone concentrations and observing reproductive behaviors in free-ranging individuals. Additionally, we examined reproductive tissues from museum specimens. Plasma steroid hormone concentrations were quantified for both male and female snakes throughout the active season (March-October). We measured testosterone (T), 5alpha-dihydrotestosterone (DHT), and corticosterone (B) concentrations in both sexes and 17beta-estradiol (E2) and progesterone (P) in females only. We observed reproductive behaviors (e.g., consortship, courtship, and copulation) in the field and measured testis and follicle size in male and female snakes from museum collections to relate steroid hormone concentrations to the timing of reproductive events. Our study revealed that C. oreganus in central California exhibits a bimodal pattern of breeding, with most mating behavior occurring in the spring and some incidences of mating behavior observed in late summer/fall. Each breeding period corresponded with elevated androgen (T or DHT) levels in males. Testes were regressed in the spring when the majority of reproductive behavior was observed in this population, and they reached peak volume in August and September during spermatogenesis. Although we did not detect seasonal variation in female hormone concentrations, some females had high E2 in the spring and fall, coincident with mating and with increased follicle size (indicating vitellogenesis) in museum specimens. Females with high E2 concentrations also had high T and DHT concentrations. Corticosterone concentrations in males and females were not related either to time of year or to concentrations of any other hormones quantified. Progesterone concentrations in females also did not vary seasonally, but this likely reflected sampling bias as females tended to be underground, and thus unobtainable, in summer months when P would be expected to be elevated during gestation. In females, P was positively correlated with T and DHT, and E2 was positively correlated with T.

Proximate developmental mediators of sexual dimorphism in size: case studies from squamate reptiles.

Sexual dimorphism in size (sexual size dimorphism; SSD) is nearly ubiquitous, but the relative importance of genetic versus environmental control of SSD is not known for most species. We investigated proximate determinants of SSD in several species of squamate reptiles, including three species of Sceloporus lizards and the diamond-backed rattlesnake (Crotalus atrox). In natural populations of these species, SSD is caused by sexual differences in age-specific growth. Males and females, however, may often share similar potentials for growth: growth is strongly responsive to the availability of food, and sexual differences in growth can be greatly suppressed or completely absent under common environmental conditions in the laboratory. Sexually divergent growth is expressed in natural environments because of inherent ecological differences between males and females and because of potential epigenetic effects of sex-specific growth regulators. In field-active Sceloporus, sexual differences in growth rate are associated with sexual divergence in plasma testosterone. Experiments confirm that testosterone inhibits growth in species in which females are larger (for example, S. undulatus and S. virgatus) and stimulates growth in those in which males are larger (for example, S. jarrovii). Interestingly, however, sexual divergence in plasma testosterone is not accompanied by divergence in growth in S. jarrovii or in male-larger C. atrox in the laboratory. Furthermore, experimental effects of castration and testosterone replacement on growth are not evident in captive S. jarrovii, possibly because growth effects of testosterone are superseded by an abundant, high-quality diet. In female-larger S. undulatus, growth may be traded-off against testosterone-induced reproductive costs of activity. In male-larger species, costs of reproduction in terms of growth are suggested by supplemental feeding of reproductive female C. atrox in their natural environment and by experimental manipulation of reproductive cost in female S. jarrovii. Growth costs of reproduction, however, do not contribute substantially to the development of SSD in male-larger S. jarrovii. We conclude that the energetic costs of testosterone-induced, male reproductive behavior may contribute substantially to the development of SSD in some female-larger species. However, despite strong evidence that reproductive investment exacts a substantial cost in growth, we do not support the reproductive cost hypothesis as a general explanation of SSD in male-larger species.

Reproductive Ecology of Western Diamond-Backed Rattlesnakes (Crotalus atrox) in the Sonoran Desert

Abstract We studied the reproductive ecology of a population of Western Diamond-Backed Rattlesnakes (Crotalus atrox) in south-central Arizona for four active seasons using radiotelemetry and portable ultrasonography. Snakes mate in the spring and fall, and females undergo vitellogenesis exclusively in the spring, ovulate in the early summer, and give birth in the late summer. Although parturition occurs at the same time of year in all rattlesnake species studied, females of most species initiate vitellogenesis in the fall, and it is unusual for females to delay this process until the spring. No females gave birth more than once in this study, indicating that reproduction is less than annual. Litter sizes range from 2–7 neonates (mean = 4.5). The sex ratio of the neonates was approximately equal, but male neonates were longer in snout–vent length and heavier than female neonates. There was no significant relationship between maternal snout–vent length and clutch mass, number of neonates, mean neonate mass, or mean neonate snout–vent length. Maternal postparturient mass was positively correlated with mean neonate mass, but not the other variables.

Experimentally Altered Navigational Demands Induce Changes in the Cortical Forebrain of Free-Ranging Northern Pacific Rattlesnakes (Crotalus o. oreganus)

The hippocampus of birds and mammals plays a crucial role in spatial memory and navigation. The hippocampus exhibits plasticity in adulthood in response to diverse environmental factors associated with spatial demands placed on an animal. The medial and dorsal cortices of the telencephalon of squamate reptiles have been implicated as functional homologues to the hippocampus. This study sought to experimentally manipulate the navigational demands placed on free-ranging northern Pacific rattlesnakes (Crotalus o. oreganus) to provide direct evidence of the relationship between spatial demands and neuroplasticity in the cortical telencephalon of the squamate brain. Adult male rattlesnakes were radio-tracked for 2 months, during which time 1 of 3 treatments was imposed weekly, namely 225-meter translocation in a random direction, 225-meter walk and release at that day’s capture site (handling control) or undisturbed (control). Snakes were then sacrificed and the brains were removed and processed for histological analysis of cortical features. The activity range was larger in the translocated (Tr) group compared to the handled (Hd) and undisturbed control (Cn) groups when measured via 95% minimum convex polygon (MCP). At the 100% MCP level, Tr snakes had larger activity ranges than the Cn snakes only. The volume of the medial cortex (MC) was larger in the Tr group compared to the Cn group. The MC of Hd snakes was not significantly different from that of either of the other groups. No differences in dorsal cortex (DC) or lateral cortex volumes were detected among the groups. Numbers of 5-bromo-2′-deoxyuridine (BrdU)-labeled cells in the MC and DC 3 weeks after BrdU injection were not affected by treatment. This study establishes a causal relationship between navigational demands and greater MC volume in a free-ranging reptile.

Physiological and Behavioral Effects of Repeated Handling and Short-Distance Translocations on Free-Ranging Northern Pacific Rattlesnakes (Crotalus oreganus oreganus)

Abstract 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 days 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.

The Effect of Exogenous Testosterone on Ectoparasite Loads in Free‐Ranging Western Fence Lizards

Numerous factors impact the dynamics of host-parasite relationships, such as host sex, hormonal state, reproductive condition, host health, and behavior. In particular, males from a variety of taxa frequently carry heavier parasite burdens than females, particularly during breeding season when testosterone concentrations are elevated. Using western fence lizards (Sceloporus occidentalis), we tested the hypothesis that high circulating testosterone concentrations in male lizards induce high tick and mite loads. We implanted male lizards with either testosterone or control implants in the field during the spring, when tick and mite loads are highest. One month later, testosterone-implanted males had significantly higher tick loads, but lower mite loads, than control males. These results suggest that testosterone differentially impacts ectoparasitic acarine burdens. Testosterone may modulate aspects of lizard physiology and behavior that enhance or diminish parasitism by certain acarines during periods of peak reproductive effort.

Hormones and Reproductive Cycles in Snakes

Publisher Summary This chapter focuses on current knowledge of the hormonal regulation of reproduction in snakes. Studies conducted have disproportionately examined temperate zone viperid and colubrid snakes, especially the redsided garter snake (Thamnophis sirtalis parietalis). Indeed, extensive observational and experimental studies on T. s. parietalis form the basis for our understanding of the hormonal regulation of reproduction in snakes. This review focuses on seasonal hormone concentrations in snakes in relation to events in the reproductive cycle; the limited data available on hypothalamic hormones, gonadotropins (GTHs), hormone receptors, and binding globulins; the neuroendocrinology of reproduction; and the environmental, social, physiological, and embryonic aspects of hormonal regulation of reproduction in snakes. Suggestions for future research are also provided, including studies of a more diverse ecological and taxonomic representation of snakes, experimental studies on the effects of hormones on reproductive tissues and behaviors, and further research into the neuroendocrinology of reproduction in this highly diverse group of animal. This chapter attempts to provide a broad overview of the effects of hormones on reproduction in snakes, focusing on seminal studies.

Diet of the Baja California Rattlesnake, Crotalus enyo (Viperidae)

Abstract The Baja California rattlesnake, Crotalus enyo, is a medium-sized rattlesnake restricted to the southern two-thirds of the Baja California peninsula. Very little is known about the natural history of this species. The goal of this study was to document the diet of C. enyo. I dissected the stomachs and hindguts of 113 preserved museum specimens of C. enyo and identified the ingested prey items. The diet of C. enyo consists of small rodents, lizards, and centipedes. Crotalus enyo of all sizes eat rodents and lizards, in contrast to many other rattlesnakes that eat almost exclusively lizards as juveniles and mammals as adults. However, C. enyo exhibits a modest ontogenetic shift in diet: small snakes eat lizards more often than do large snakes, and large snakes eat mammals more often than do small snakes. Adult C. enyo also eat large centipedes of the genus Scolopendra. Larger snakes tended to contain multiple prey items more often than smaller snakes, but this trend was not significant. Crotalus enyo is sexually dimorphic in size, with males being significantly larger than females. However, there is no significant gender difference in diet.