Effects of body mass, meal size, fast length, and temperature on specific dynamic action in the timber rattlesnake (Crotalus horridus)

Detailed analysis of animal energy budgets requires information on the cost of digestion (specific dynamic action [SDA]), which can represent a significant proportion of ingested energy (up to 30% in infrequent feeders). We studied the effects of snake mass, temperature (25 degrees and 30 degrees C), fasting time (1 and 5 mo), and prey size (10%-50% of snake mass) on SDA in 26 timber rattlesnakes (Crotalus horridus). We used flow-through respirometry to measure hourly CO(2) production rates (VCO2) for 1 d before and up to 17 d after feeding. Crotalus horridus, like previously studied viperids and boids, show large and ecologically relevant increases in metabolism due to feeding. Depending on treatment and individual, VCO2 increased to 2.8-11.8 times the resting metabolic rate within 12-45 h postfeeding and decreased to baseline within 4.3-15.4 d. Significant effects of snake mass, meal mass, and fast length were detected. Increased temperature decreased the time required to complete the process but had little effect on total energy expended on SDA. Energy expended on SDA increased with increasing fast length, snake mass, and prey mass. Considering all of our data, we found that a simple allometric relationship explained 96.7% of the variation in total CO(2) production during SDA. Calculations suggest that energy devoted to SDA may approach 20% of the total annual energy budget of snakes in nature. Discrepancies between our data and some previous studies draw attention to the fact that the measurement, expression, and analysis of SDA may be sensitive to several methodological and statistical assumptions.     

Variation in oxygen consumption of the western diamondback rattlesnake (Crotalus atrox): implications for sexual size dimorphism

Variation in metabolism affects energy budgets of individuals and may serve as a mechanism that influences variation at whole organism or population levels. For example, sex differences in metabolic expenditure may contribute to bioenergetic sources of sexual size dimorphism. We measured oxygen consumption rates of 48 western diamondback rattlesnakes (Crotalus atrox) from a sexually dimorphic population and tested the effects of body mass, body temperature and time of day, in three groups of snakes: males, non-reproductive females, and vitellogenic females. Metabolic rates of male and non-reproductive female C. atrox were similar to rates reported for other rattlesnakes (mass exponents ranging from 0.645–0.670). Oxygen consumption was affected by body mass, body temperature and time of day, and was approximately 1.4 times greater in vitellogenic females than in non-reproductive females. No differences were found between males and non-reproductive females. Accordingly, differences in metabolic rate apparently do not contribute directly to sexual dimorphism in this population. Nevertheless, estimates of size-dependent maintenance expenditure lead us to hypothesize that adult female body size may represent a compromise between selection for increased litter size (accomplished by increasing body size), and selection for increased reproductive frequency (accomplished by decreasing body size, and, therefore inactive maintenance expenditure); this is a mechanistic scenario suggested previously for some endotherms. Accepted: 20 May 1998     

Respiratory cooling in rattlesnakes

We used infrared thermography to study respiratory cooling in the rattlesnakes (Viperidae: Crotalinae) and to partition the effects of air temperature, humidity, and activity levels on head-body temperature differences. We observed a single, cooled region centered around the mouth and nasal capsule that extended across the pit membrane at air temperatures above 20 degrees C. Both head and body temperatures of rattlesnakes increased linearly with air temperature. Head-body temperature differentials also increased with air temperature, but declined significantly at higher relative humidities. Rattling rattlesnakes exhibited significantly greater head-body temperature differentials than did resting rattlesnakes. We suggest that respiratory cooling may provide a thermal buffer for the thermoreceptive pit organs at high air temperatures, but caution that this adaptive hypothesis must be tested with direct neural or behavioral assays.     

Duration of strike-induced chemosensory searching in long-term captive rattlesnakes at national zoo,audubon zoo,and San Diego Zoo

Rattlesnakes typically strike and release adult rodent prey. Striking is followed by a sustained, high rate of tongue flicking that guides the snake to the envenomated, dead prey. Wild-caught rattlesnakes exhibited this chemosensory searching for about 2.5 h, and the present study demonstrated that long-term captive rattlesnakes (Crotalus atrox, C durissus, C horridus, C vegrandis, C unicolor) at three zoos did the same. Because these zoo-raised snakes had always been offered dead rodents and because the snakes had become accustomed to ingesting them without striking, the present snakes had rarely exercised their innate predatory repertoires. The duration of chemosensory searching in these snakes indicates that this important aspect of the predatory repertoire had not been degraded as a consequence of long-term captive husbandry.     

Comparative skin permeability of neonatal and adult timber rattlesnakes (Crotalus horridus)

Skin permeability and lipid content were determined using shed epidermis of neonatal and adult timber rattlesnakes (Crotalus horridus) from the Coastal Plain Pine Barrens of New Jersey and from the Appalachian Mountains of northern Pennsylvania. Differences between populations due to habitat and within populations due to age were tested. Skin permeability was not found to differ according to locality (P>0.05), but rates were significantly different for age. Permeability of adult epidermis was greater than that of neonates (P<0.01). Lipid content did not differ by locality (P>0.05), but differed between ages, paralleling the results found for permeation rates. Neonate sheds had a greater amount of extractable lipids than adult sheds (P<0.01). Despite the lower skin permeability of neonates, our estimates indicate that the percentage of their total body water content lost per hour may still be 2.2 times that of adults. Resistance to cutaneous water loss may be advantageous to neonates given their relatively large surface area-to-volume ratio.     

An application of randomization for detecting evidence of thermoregulation in timber rattlesnakes (Crotalus horridus) from northwest Arkansas

Most reptiles maintain their body temperatures within normal functional ranges through behavioral thermoregulation. Under some circumstances, thermoregulation may be a time-consuming activity, and thermoregulatory needs may impose significant constraints on the activities of ectotherms. A necessary (but not sufficient) condition for demonstrating thermoregulation is a difference between observed body temperature distributions and available operative temperature distributions. We examined operative and body temperature distributions of the timber rattlesnake (Crotalus horridus) for evidence of thermoregulation. Specifically, we compared the distribution of available operative temperatures in the environment to snake body temperatures during August and September. Operative temperatures were measured using 48 physical models that were randomly deployed in the environment and connected to a Campbell CR-21X data logger. Body temperatures (n=1,803) were recorded from 12 radiotagged snakes using temperature-sensitive telemetry. Separate randomization tests were conducted for each hour of day within each month. Actual body temperature distributions differed significantly from operative temperature distributions at most time points considered. Thus, C. horridus exhibits a necessary (but not sufficient) condition for demonstrating thermoregulation. However, unlike some desert ectotherms, we found no compelling evidence for thermal constraints on surface activity. Randomization may prove to be a powerful technique for drawing inferences about thermoregulation without reliance on studies of laboratory thermal preference.     

Respiratory adaptation to chronic hypercapnia in newborn rats

We asked 1) whether newborn rats respond to chronic hypercapnia with a persistent increase in ventilation and 2) whether changes in lung mass were accompanying the respiratory adaptation to chronic hypercapnia, as previously observed during neonatal chronic hypoxia. Five litters of rats were kept in 7% CO2 (with 21% O2) from day 1 to 7 after birth (CO2exp) and compared with six litters of control rats growing in normocapnia-normoxia (C). Body weight was similar between the two groups. Ventilation, measured by flow plethysmography, increased in CO2exp from day 2 and remained steadily elevated, and at day 7 it almost doubled (174%) the C value because of the large increase in tidal volume and mean inspiratory flow (192 and 189%, respectively) with no changes in respiratory frequency. Two days after return to normocapnia, ventilation was still 33% higher than in C; at this time, acute exposure to hypercapnia increased ventilation relatively less in the CO2exp than in C because of a lower increase in tidal volume. Neither the lung weight-to-body weight nor the heart weight-to-body weight ratios increased in CO2exp. We conclude that 1) chronic hypercapnia in newborn rats induces a steady increase in ventilation, which persists at least 2 days after return to normocapnia with a reduction in the acute response to CO2, and 2) hyperventilation per se is not the cause of the increased lung mass observed during chronic neonatal hypoxia.     

Influence of pregnancy on the thermal biology of the lizard, Sceloporus jarrovi: why do pregnant females exhibit low body temperatures?

1. Selected body temperatures of female lizards, Sceloporus jarrovi , were measured on a photothermal gradient during late pregnancy and again when postpartum, and pregnant females were subjected to one of three fluctuating temperature regimes that simulated body temperatures of (1) pregnant females, (2) postpartum females or (3) allowed normal thermoregulation.
2. Overall, females selected lower body temperatures when pregnant (mean = 32·0°C) than when postpartum (mean = 33·5°C).
3. Females regulated body temperature more precisely when pregnant than when postpartum as judged by their smaller variances in body temperature throughout the day.
4. When pregnant, females selected a lower mean maximum body temperature (mean: pregnant = 32·8°C; postpartum = 34·5°C) than when postpartum, but selected mean minimum body temperatures did not differ.
5. None of the experimental temperature treatments was detrimental to pregnant females. Female body length increased during pregnancy but the rate of increase did not differ among treatments. Moreover, length-adjusted body mass of postpartum females did not differ among treatments.
6. Pregnant females that experienced postpartum body temperatures produced neonates that were smaller in body mass and length than pregnant females that experienced pregnant body temperatures and females that were allowed to thermoregulate.
7. For neonates resulting from the postpartum body temperature treatment, the disparity in the body length, but not mass, was still observed at 9 days of age, although survival and growth of neonates was high and did not differ among treatments.
8. The results demonstrate that pregnant females could maintain higher postpartum body temperatures without compromising their physical condition, but select relatively low body temperatures, presumably to avoid decrements in offspring fitness.     

Rattlesnake denning: theoretical considerations on winter temperatures

Aggregations of over-wintering rattlesnakes are considered as a hypothetical metabolic unit. Estimates of fat consumption are utilized to predict heat production during the denning season. Previously determined temperature heat production curves allow prediction of a mean body temperature for the winter season which is around 15°C above the ambient den site temperature. An estimate from the previously derived relationship between heat production per unit surface area and body temperature predicts a reduction in aggregate effective surface area of 40 % of the summed surface areas of the individual animals constituting the hypothetical aggregation.     

Rattlesnake predatory behaviour: Mediation of prey discrimination and release of swallowing by cues arising from envenomated mice

Responses of rattlesnakes to envenomated mice were examined in five experiments. In experiment 1 rattlesnakes (Crotalus durissus terrificus and C. viridis viridis) discriminated mice that they had envenomated, as indexed by number of tongue flicks and accumulated investigation time, when these prey items were paired with control mice killed by the experimenter. Experiment 2 demonstrated that rattlesnakes also exhibited this discrimination when presented with mice envenomated by a conspecific and controls killed by the experimenter. In experiments 1 and 2, we observed that rattlesnakes delivered a large number of tongue flicks to exudates associated with nasal-oral tissues of envenomated mice. It has commonly been noted that rattlesnakes typically swallow envenomated, dead mice head first. In experiment 3 this observation was statistically verified. Evidence obtained in experiment 4 indicated that nasal-oral tissues of envenomated, dead mice were discriminated from anogenital tissues by rattlesnakes. Cues arising from the nasal-oral tissues probably (1) assisted the snakes in locating the head-end of the rodent, and (2) released the swallowing modal-action pattern, the final phase of the predatory sequence. In experiment 5, rattlesnakes exhibited no discrimination between nasal-oral and anogenital tissues of non-envenomated, dead mice, indicating that the results of experiment 4 were probably dependent upon effects of envenomation.     

Hepatozoon species of the timber rattlesnake in northern Florida: description of a new species, evidence of salivary gland oocysts, and a natural cross-familial transmission of an Hepatozoon species

Two species of Hepatozoon, i.e., H. sauritus and H. horridus n. sp., were present in 1 of 8 timber rattlesnakes, Crotalus horridus. The narrow gamonts of H. sauritus are 15.0-19.0 x 3.5-5.0 microm, with LW 58-86 microm2 and L/W 3.2-4.7, with a narrow, rounded anterior end. The spherical to slightly ovoid oocysts produce ovoid to elongate sporocysts, 21-43 x 12-24 microm, L/W 1.20-2.7, containing on average 22.1 (10-34) sporozoites. This is the first report of a natural cross-familial transfer of a Hepatozoon species. Gamonts of H. horridus n. sp. are 13.0-17.0 x 4.0-6.0 microm, with LW 63-102 microm2 and L/W 2.6-4.0, and have broadly rounded ends. The gamont cytoplasm is vacuolated. The spherical to ovoid oocysts form spherical to elongate sporocysts 14-45 x 11-25 microm, L/W 1.0-2.3, producing an average of 13.0 (8-21) sporozoites. The salivary gland in 1 of 5 mosquitoes dissected contained 1 mature oocyst.     

Kin recognition in rattlesnakes

Snakes are often regarded as the least social of all vertebrate groups, but this assumption stems from the fact that they are secretive and difficult to observe in nature, rather than direct evidence. Recent studies have revealed a surprising degree of social complexity in snakes. Here, I examine the ability of captive-raised timber rattlesnakes (Crotalus horridus) to recognize siblings by measuring the mean separation distance and frequency of contact between pairs of individuals housed together. The results show that female siblings associate more closely with each other than nonsibling pairs. Previous studies have shown that timber rattlesnakes occupying the same hibernacula have higher relatedness than snakes using neighbouring hibernacula, and frequently form social aggregations. Rattlesnakes exhibit other characteristics consistent with advanced sociality, including group defence, conspecific alarm signals and maternal defence of young. These findings reinforce the notion that, rather than being solitary and asocial, some snake species may form family groups.     

Rattling Behavior of Prairie Rattlesnakes (Crotalus viridis viridis,Viperidae) in Relation to Sex,Reproductive Status,Body Size,and Body Temperature

We examined whether sex, reproductive status, body size, or body temperature of prairie rattlesnakes (Crotalus viridis viridis) was related to when snakes rattled in response to an approaching observer. We found that gravid females allowed significantly closer approaches than males, suggesting that females relied on crypsis to avoid predation, possibly because pregnancy constrained their locomotive ability. Smaller snakes allowed significantly closer approaches than did larger snakes. Smaller snakes may be more cryptic or slower, which may influence their waiting to rattle until the observer was close. Overall, we found no consistent relationship between the distance from the observer that a snake rattled and its body temperature. However, cooler gravid females allowed closer approaches by the observer than did warmer gravid females. In summary, reproductive status, body size, and body temperature appear to influence the costs and benefits of crypsis vs. active defense of rattlesnakes.     

Inter-sexual differences in resting metabolic rates in the Texas tarantula, Aphonopelma anax

Intra-specific variation in life history and mating strategies can lead to differences in energy allocation and expenditure in males and females. This may, in turn, explain large-scale evolutionary patterns. In this study, I investigated the effects of body mass, temperature and sex on resting metabolic rates (RMRs) in sexually mature male and female tarantulas (Aphonopelma anax (Chamberlin)), a species that exhibits extreme inter-sexual differences in life history after reaching sexual maturity. RMRs were measured as rates of CO(2) production in an open-flow respirometry system at 20, 25, 30 and 35 degrees C. These temperatures are typical to what this species experiences under natural conditions. In addition, a respiratory quotient (RQ) of 0.92 was calculated from rates of CO(2) production and O(2) consumption in a closed, constant-volume respirometry system. As expected, RMRs increased with increasing temperature and body mass. However, after adjusting for the influence of body mass, males had substantially higher metabolic rates than females at each temperature. This higher metabolic rate is proposed as an adaptive strategy to support higher energetic demands for males during their active, locomotory search for females during the mating season.     

Temperature as a control over ecosystem CO<Subscript>2</Subscript> fluxes in a high-elevation,subalpine forest

We evaluated the hypothesis that CO(2) uptake by a subalpine, coniferous forest is limited by cool temperature during the growing season. Using the eddy covariance approach we conducted observations of net ecosystem CO(2) exchange (NEE) across two growing seasons. When pooled for the entire growing season during both years, light-saturated net ecosystem CO(2) exchange (NEE(sat)) exhibited a temperature optimum within the range 7-12 degrees C. Ecosystem respiration rate ( R(e)), calculated as the y-intercept of the NEE versus photosynthetic photon flux density (PPFD) relationship, increased with increasing temperature, causing a 15% reduction in net CO(2) uptake capacity for this ecosystem as temperatures increased from typical early season temperatures of 7 degrees C to typical mid-season temperatures of 18 degrees C. The ecosystem quantum yield and the ecosystem PPFD compensation point, which are measures of light-utilization efficiency, were highest during the cool temperatures of the early season, and decreased later in the season at higher temperatures. Branch-level measurements revealed that net photosynthesis in all three of the dominant conifer tree species exhibited a temperature optimum near 10 degrees C early in the season and 15 degrees C later in the season. Using path analysis, we statistically isolated temperature as a seasonal variable, and identified the dynamic role that temperature exhibits in controlling ecosystem fluxes early and late in the season. During the spring, an increase in temperature has a positive effect on NEE, because daytime temperatures progress from near freezing to near the photosynthetic temperature optimum, and R(e )values remain low. During the middle of the summer an increase in temperature has a negative effect on NEE, because inhibition of net photosynthesis and increases in R(e). When taken together, the results demonstrate that in this high-elevation forest ecosystem CO(2) uptake is not limited by cool-temperature constraints on photosynthetic processes during the growing-season, as suggested by some previous ecophysiological studies at the branch and needle levels. Rather, it is warm temperatures in the mid-summer, and their effect on ecosystem respiration, that cause the greatest reduction in the potential for forest carbon sequestration.     

Cryptic sociality in rattlesnakes (Crotalus horridus) detected by kinship analysis

Research on social behaviour has largely concentrated on birds and mammals in visually active, cooperatively breeding groups (although such systems are relatively rare) and focused much less on species that rarely interact other than for mating and parental care. We used microsatellite markers to characterize relatedness among aggregations of timber rattlesnakes (Crotalus horridus), a putatively solitary reptile that relies heavily on chemical cues, and found that juveniles and pregnant females preferentially aggregate with kin under certain conditions. The ability to recognize kin and enhance indirect fitness thus might be far more widespread than implied by studies of animals whose behaviour is primarily visually and/or acoustically mediated, and we predict that molecular markers will reveal many additional examples of 'cryptic' sociality.     

Body mass loss of moulting female southern elephant seals,Mirounga leonina,at Macquarie Island

Thirteen female southern elephant seals moulting at Macquarie Island lost an average of 4.46±0.80 kg/day (10.01±1.20g/kg/day). There was no significant difference between this rate of body mass loss and that reported for moulting female southern elephant seals from South Georgia. Moulting female southern elephant seals however exhibited larger mass specific mass loss than either female northern elephant seals or male southern elephant seals, indicating a higher metabolic cost of moult in these animals.     

Behavioral thermal tolerances of free-ranging rattlesnakes (Crotalus oreganus) during the summer foraging season

Increasing temperature due to climate change is one of the greatest challenges for wildlife worldwide. Behavioral data on free-ranging individuals is necessary to determine at what temperatures animals modify activity as this would determine their capacity to continue to move, forage, and mate under altered thermal regimes. In particular, high temperatures could limit available surface activity time and time spent on fitness-related activities. Conversely, performance, such as feeding rate, can increase with temperature potentially having positive fitness effects. Here, we examine how the hunting behaviors of free-ranging Northern Pacific Rattlesnakes (Crotalus oreganus) associate with air temperature and body temperature. We continuously recorded snakes in the field using videography, capturing behaviors rarely considered in past studies such as movements in and out of refuge and strikes on prey. We found that as mean daily air temperature increased, hunting activity and the likelihood of hunting at night decreased, while the number of movements and distance moved per day increased. Snakes typically retreated to refuge before body temperatures reached 31 °C. Body temperatures of snakes hunting on the surface were lower compared to temperatures of non-hunting snakes in refuge in the morning, while this relationship was inverted in the afternoon. Snake body size influenced the disparity of these temperatures. Finally, strike initiation and success occurred across a wide range of body temperatures, indicating hunting performance may not be strongly constrained by temperature. These results on the temperatures at which free-ranging rattlesnakes exhibit fitness-related behaviors could be valuable for understanding their vulnerabilities to future climates.     

Snake venomics of Crotalus tigris: the minimalist toxin arsenal of the deadliest Neartic rattlesnake venom. Evolutionary Clues for generating a pan-specific antivenom against crotalid type II venoms

We report the proteomic and antivenomic characterization of Crotalus tigris venom. This venom exhibits the highest lethality for mice among rattlesnakes and the simplest toxin proteome reported to date. The venom proteome of C. tigris comprises 7-8 gene products from 6 toxin families; the presynaptic β-neurotoxic heterodimeric PLA(2), Mojave toxin, and two serine proteinases comprise, respectively, 66 and 27% of the C. tigris toxin arsenal, whereas a VEGF-like protein, a CRISP molecule, a medium-sized disintegrin, and 1-2 PIII-SVMPs each represent 0.1-5% of the total venom proteome. This toxin profile really explains the systemic neuro- and myotoxic effects observed in envenomated animals. In addition, we found that venom lethality of C. tigris and other North American rattlesnake type II venoms correlates with the concentration of Mojave toxin A-subunit, supporting the view that the neurotoxic venom phenotype of crotalid type II venoms may be described as a single-allele adaptation. Our data suggest that the evolutionary trend toward neurotoxicity, which has been also reported for the South American rattlesnakes, may have resulted by pedomorphism. The ability of an experimental antivenom to effectively immunodeplete proteins from the type II venoms of C. tigris, Crotalus horridus , Crotalus oreganus helleri, Crotalus scutulatus scutulatus, and Sistrurus catenatus catenatus indicated the feasibility of generating a pan-American anti-Crotalus type II antivenom, suggested by the identification of shared evolutionary trends among South and North American Crotalus species.     

Discontinuous gas exchange in the fire ant,Solenopsos invicta Buren: Caste differences and temperature effects

The discontinuous gas exchange cycle (DGC), the cyclic release of CO(2) and uptake of O(2), were investigated in workers and female and male alates of the red imported fire ant, Solenopsis invicta Buren, using real-time CO(2) emission measurement by flow-through respirometry. All S. invicta castes displayed discontinuous emission of CO(2) in the temperature range of 15-25 degrees C, but only male alates and workers exhibited a DGC at 30 degrees C. The closed (C) and flutter (F) periods of the DGC were distinguishable in alates of both sexes at the lowest temperature, but not clearly differentiated in females at temperatures above 15 degrees C, in males above 20 degrees C, or workers at any temperature. DGC frequency increased for all castes as temperature increased, ranging from a low of 0.9+/-0.05 mHz (male alates at 15 degrees C) to 18+/-0.79 mHz (workers at 30 degrees C). O period (or burst) volumes of all castes decreased as temperature increased, and increased with body mass - this mass effect was most pronounced at lower temperatures. Q(10) values for DGC frequency (4.27, 5.81, and 5.62 for workers, female and male alates, respectively) were high compared with Q(10)'s for standard Vdot;(CO(2)). Differences in the salient characteristics of the DGC between castes are presented and discussed, and S. invicta DGC patterns are compared to known values for some other ant species.