Modeling the costs and benefits associated with the evolution of endothermy using a robotic python.

Endothermy provides considerable benefits to an organism but requires large energy investment. To understand potential driving forces that would lead to the evolution of endothermy, it is important to understand the energy costs and potential benefits of intermediate steps between ectothermy and homeothermic endothermy as well as the influences of environmental conditions on energetic costs. However, efforts to examine intermediate conditions are greatly limited by the predominant natural dichotomy between ectothermy and endothermy. Facultative endothermy by brooding pythons provides a fortunate study system where endothermy is beneficial but not essential. As one cannot control the extent of energy investment in heat production by a female python, we created an artificial snake with controllable heating capability. This enabled us to determine the energetic costs of maintaining a clutch at a preferred temperature, and to determine the relative thermal benefit of limited energy-producing capability (i.e. 50% of the required energy to maintain the preferred developmental temperature). We manipulated the pseudoserpent's clutch size (5, 10, 15 eggs), diel ambient temperature cycle (2, 4, 6°C) and insulation (with and without) at each of these power levels: unlimited power, half required power and no power. We found no significant effect of clutch size on either power requirements or developmental temperature. Energy requirements increased with the amplitude of the diel cycle and decreased with the addition of insulation, while the quality of the thermal environment decreased with the amplitude of the diel cycle. Interestingly, the quality of the thermal environment also decreased with the addition of insulation. We discuss these results within the context of the reproductive model of the evolution of endothermy.

Low cost of gastric acid secretion during digestion in ball pythons.

Due to their large metabolic responses to digestion (specific dynamic action, SDA), snakes represent an interesting animal group to identify the underlying mechanisms for the postprandial rise in metabolism. The SDA response results from the energetic costs of many different processes ranging over prey handling, secretions by the digestive system, synthesis of enzymes, plasticity of most visceral organs, as well as protein synthesis and nitrogen excretion. The contribution of the individual mechanisms, however, remains elusive. Gastric acid secretion has been proposed to account for more than half of the SDA response, while other studies report much lower contributions of the gastric processes. To investigate the energetic cost of gastric acid secretion, ball pythons (Python regius) were fed meals with added amounts of bone meal (up to 25 g bone meal kg(-1) snake) to achieve a five-fold rise in the buffer capacity of the meals. Direct measurements within the stomach lumen showed similar reduction in gastric pH when buffer capacity was increased, but we found no effects on the rise in oxygen consumption over the first three days of digestion. There was, however, a slower return of oxygen consumption to resting baseline. We conclude that gastric acid secretion only contributes modestly to the SDA response and propose that post-absorptive processes, such as increased protein synthesis, are likely to underlie the SDA response.

Gripping during climbing of arboreal snakes may be safe but not economical.

On the steep surfaces that are common in arboreal environments, many types of animals without claws or adhesive structures must use muscular force to generate sufficient normal force to prevent slipping and climb successfully. Unlike many limbed arboreal animals that have discrete gripping regions on the feet, the elongate bodies of snakes allow for considerable modulation of both the size and orientation of the gripping region. We quantified the gripping forces of snakes climbing a vertical cylinder to determine the extent to which their force production favoured economy or safety. Our sample included four boid species and one colubrid. Nearly all of the gripping forces that we observed for each snake exceeded our estimate of the minimum required, and snakes commonly produced more than three times the normal force required to support their body weight. This suggests that a large safety factor to avoid slipping and falling is more important than locomotor economy.

Structural and performance costs of reproduction in a pure capital breeder, the Children's python Antaresia childreni.

Females often manage the high energy demands associated with reproduction by accumulating and storing energy in the form of fat before initiating their reproductive effort. However, fat stores cannot satisfy all reproductive resource demands, which include considerable investment of amino acids (e.g., for the production of yolk proteins or gluconeogenesis). Because capital breeders generally do not eat during reproduction, these amino acids must come from internal resources, typically muscle proteins. Although the energetic costs of reproduction have been fairly well studied, there are limited data on structural and performance costs associated with the muscle degradation required to meet amino acid demands. Thus, we examined structural changes (epaxial muscle width) and performance costs (constriction and strength) over the course of reproduction in a pure capital breeder, the children's python (Antaresia childreni). We found that both egg production (i.e., direct resource allocation) and maternal care (egg brooding) induce muscle catabolism and affect performance of the female. Although epaxial muscle loss was minimal in nonreproductive females, it reached up to 22% (in females after oviposition) and 34% (in females after brooding) of initial muscle width. Interestingly, we found that individuals with higher initial muscular condition allocated more of their muscle into reproduction. The amount of muscle loss was significantly linked to clutch mass, underscoring the role of structural protein in egg production. Egg brooding significantly increased proteolysis and epaxial loss despite no direct allocation to the offspring. Muscle loss was linked to a significant reduction in performance in postreproductive females. Overall, these results demonstrate that capital-breeding females experience dramatic costs that consume structural resources and jeopardize performance.

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.

Cooking and grinding reduces the cost of meat digestion.

The cooking of food is hypothesized to have played a major role in human evolution partly by providing an increase in net energy gain. For meat, cooking compromises the structural integrity of the tissue by gelatinizing the collagen. Hence, cooked meat should take less effort to digest compared to raw meat. Likewise, less energy would be expended digesting ground meat compared to intact meat. We tested these hypotheses by assessing how the cooking and/or grinding of meat influences the energy expended on its digestion, absorption, and assimilation (i.e., specific dynamic action, SDA) using the Burmese python, Python molurus. Pythons were fed one of four experimental diets each weighing 25% of the snake's body mass: intact raw beef, intact cooked beef, ground raw beef, and ground cooked beef. We measured oxygen consumption rates of snakes prior to and up to 14 days following feeding and calculated SDA from the extra oxygen consumed above standard metabolic rate. Postprandial peak in oxygen consumption, the scope of peak rates, and SDA varied significantly among meal treatments. Pythons digesting raw or intact meals exhibited significantly larger postprandial metabolic responses than snakes digesting the cooked ground meals. We found cooking to decrease SDA by 12.7%, grinding to decrease SDA by 12.4%, and the combination of the two (cooking and grinding) to have an additive effect, decreasing SDA by 23.4%. These results support the hypothesis that the consumption of cooked meat provides an energetic benefit over the consumption of raw meat.

Snakes survive starvation by employing supply- and demand-side economic strategies.

Animals vary widely in their abilities to tolerate extended periods of food limitation. Although some snakes are known for their unique ability to survive periods of inanition that last up to 2 years, very little is known about the biological mechanisms that allow them to do this. Consequently, the present study examined physiological, compositional, and morphological responses to 168 days of starvation among three distantly related snake species (i.e., ball python, Python regius; ratsnake, Elaphe obsoleta; and western diamondback rattlesnake, Crotalus atrox). Results revealed that each of these species was able to successfully tolerate starvation by adaptively utilizing supply- and demand-side regulatory strategies. Effective demand-side strategies included the ability of snakes to depress their resting metabolic demands by up to 72%. Moreover, supply-side regulation of resources was evidenced by the ability of snakes to spare their structurally critical protein stores at the expense of lipid catabolism. Such physiological strategies for minimizing endogenous mass and energy flux during periods of resource limitation might help explain the evolutionary persistence of snakes over the past 100 million years, as well as the repeated radiation of snake lineages into relatively low-energy environments. The final section of this study outlines a novel modeling approach developed to characterize material and chemical flux through animals during complete inanition. This approach was used to make comparisons about the efficacy of various supply- and demand-side starvation strategies among the three species examined, but could also be used to make similar comparisons among other types of animals.

An ecological risk assessment of nonnative boas and pythons as potentially invasive species in the United States.

The growing international trade in live wildlife has the potential to result in continuing establishment of nonnative animal populations in the United States. Snakes may pose particularly high risks as potentially invasive species, as exemplified by the decimation of Guam's vertebrate fauna by the accidentally introduced brown tree snake. Herein, ecological and commercial predictors of the likelihood of establishment of invasive populations were used to model risk associated with legal commercial imports of 23 species of boas, pythons, and relatives into the United States during the period 1989-2000. Data on ecological variables were collected from multiple sources, while data on commercial variables were collated from import records maintained by the U.S. Fish and Wildlife Service. Results of the risk-assessment models indicate that species including boa constrictors (Boa constrictor), ball pythons (Python regius), and reticulated pythons (P. reticulatus) may pose particularly high risks as potentially invasive species. Recommendations for reducing risk of establishment of invasive populations of snakes and/or pathogens include temporary quarantine of imports to increase detection rates of nonnative pathogens, increasing research attention to reptile pathogens, reducing the risk that nonnative snakes will reach certain areas with high numbers of federally listed species (such as the Florida Keys), and attempting to better educate individuals purchasing reptiles.

The effects of fasting duration on the metabolic response to feeding in Python molurus: an evaluation of the energetic costs associated with gastrointestinal growth and upregulation.

The oxygen uptake of Python molurus increases enormously following feeding, and the elevated metabolism coincides with rapid growth of the gastrointestinal organs. There are opposing views regarding the energetic costs of the gastrointestinal hypertrophy, and this study concerns the metabolic response to feeding after fasting periods of different duration. Since mass and function of the gastrointestinal organs remain elevated for several days after feeding, the metabolic increment following a second meal given soon after the first can reveal whether the metabolic costs relate to the upregulation of gastrointestinal organs or merely the metabolic cost of processing a meal. Eight juvenile pythons were kept on a regular feeding regime for 6 mo after hatching. At the beginning of the metabolic measurements, they were fed mice (20% of body mass), and the metabolic response to similarly sized meals was determined following 3, 5, 7, 14, 21, 30, and 60 d of fasting. Our data show that the metabolic response following feeding was large, ranging from 21% to 35% of ingested energy (mean=27%), but the metabolic response seems independent of fasting duration. Hence, the extraordinarily large cost of digestion in P. molurus does not appear to correlate with increased function and growth of gastrointestinal organs but must be associated with other physiological processes.