Harvey B. Lillywhite

The Role of Behavioral Thermoregulation in the Growth Energetics of the Toad, Bufo Boreas

Newly metamorphosed Western toads, Bufo boreas, are diurnally active and thermoregulate by the behavioral exploitation of available microenvironments including exposure to solar radiation. In the laboratory, toads thermoregulate by basking beneath incandescent lamps when placed within a photothermal gradient. Basking depends on feeding, and when food is withheld, individuals abandon the available heat source and assume lower body temperatures. The preferred temperature of feeding individuals is around 26—27 degrees C as determined from animals both in the laboratory and in nature; fasting animals remain between 15—20 degrees C. Growth of young toads with ad libitum food supply was measured at a variety of temperatures. Energy ingestion (appetite), linear growth, weight increase, and gross conversion efficiencies were all maximal at 27 degrees C and were nearly identical to that of toads allowed to thermoregulate in a photothermal gradient. Weight—specific energy ingestion, weight—specific growth, and gross conversion efficiency decreased with age. Survivorship of starved toads in a thermal gradient was prolonged over that of toads maintained at a constant 27 degrees C. Metabolism increased with body temperature over the range 10—33 degrees C. We have concluded that this terrestrial ectotherm has evolved a behavioral thermoregulatory mechanism which maximizes growth and economic utilization of energy. The diurnal behavior patterns of small toads (compared with the more strictly nocturnal adults) may have evolved to maximize the growth rates of younger individuals, thus shortening their time to adult size.

Resting and maximal heart rates in ectothermic vertebrates

Resting and maximal heart rates (HR) in ectothermic vertebrates are generally lower than those in endotherms and vary by more than an order of magnitude interspecifically. Variation of HR transcends phylogeny and is influenced by numerous factors including temperature, activity, gas exchange, intracardiac shunts, pH, posture, and reflexogenic regulation of blood pressure. The characteristic resting HR is rarely the intrinsic rate of the pacemaker, which is primarily modulated by cholinergic inhibition and adrenergic excitation in most species. Neuropeptides also appear to be involved in cardiac regulation, although their role is not well understood. The principal determinants of resting HR include temperature, metabolic rate and hemodynamic requirements. Maximal HRs generally do not exceed 120 b min-1, but notable exceptions include the heterothermic tuna and small reptiles having HRs in excess of 300 b min-1 at higher body temperatures. Temperature affects the intrinsic pacemaker rate as well as the relative influence of adrenergic and cholinergic modulation. It also influences the evolved capability to increase HR, with maximal cardiac responses matched to preferred body temperatures in some species. Additional factors either facilitate or limit the maximal level of HR, including: (1) characteristics of the pacemaker potential; (2) development of sarcoplasmic reticulum as a calcium store in excitation-contraction coupling; (3) low-resistance coupling of myocardial cells; (4) limitations of force development imposed by rate changes; (5) efficacy of sympathetic modulation; and (6) development of coronary circulation to enhance oxygen delivery to myocardium. In evolutionary terms, both hemodynamic and oxygen requirements appear to have been key selection pressures for rapid cardiac rates.

Lipid Barrier to Water Exchange in Reptile Epidermis

Extraction of lipids from the shed epidermis of the terrestrial snake Elaphe obsoleta obsoleta increases cutaneous water loss in vitro as much as 15-fold. Partial denaturation of epidermal keratin without lipid extraction increases cutaneous water loss only twofold. Histological observations and thin-layer and gas-liquid chromatography of the lipid extracts indicate a complex mixture of polar and neutral lipids predominantly in the mesos layer of the cornified epidermis. Comparative measurements of cutaneous water loss in other species of snakes and a lizard show that permeabilities differ naturally but are essentially identical after lipid extraction. These findings establish the importance of lipids in the permeability barrier of reptilian skin and suggest that keratin or scale morphology are of nominal importance in limiting water exchange.

Movement of Water over Toad Skin: Functional Role of Epidermal Sculpturing

When live toads (Bufo) are placed on a water-saturated surface, it can be demonstrated that a film of water moves upward over the sides of the body and, in some individuals, reaches the dorsal midline. Movement of water over the skin follows interconnecting channels which characterize the outer epidermis of many terrestrial species. It was demonstrated that such water movement may replenish evaporative losses from skin surfaces and act to retard both cutaneous desiccation and elevated temperatures in individuals which are forced to bask in the laboratory. Observations and experiments suggest the possibility that epidermal sculpturing of terrestrial Bufonidae may have a functional role in relation to water uptake, thermoregulation and the prevention of integumentary desiccation.

Sea Snakes (Laticauda spp.) Require Fresh Drinking Water: Implication for the Distribution and Persistence of Populations

Dehydration and procurement of water are key problems for vertebrates that have secondarily invaded marine environments. Sea snakes and other marine reptiles are thought to remain in water balance without consuming freshwater, owing to the ability of extrarenal salt glands to excrete excess salts obtained either from prey or from drinking seawater directly. Contrary to this long‐standing dogma, we report that three species of sea snake actually dehydrate in marine environments. We investigated dehydration and drinking behaviors in three species of amphibious sea kraits (Laticauda spp.) representing a range of habits from semiterrestrial to very highly marine. Snakes that we dehydrated either in air or in seawater refused to drink seawater but drank freshwater or very dilute brackish water (10%–30% seawater) to remain in water balance. We further show that Laticauda spp. can dehydrate severely in the wild and are far more abundant at sites where there are sources of freshwater. A more global examination of all sea snakes demonstrates that species richness correlates positively with mean annual precipitation within the Indo–West Pacific tropical region. The dependence of Laticauda spp. on freshwater might explain the characteristically patchy distributions of these reptiles and is relevant to understanding patterns of extinctions and possible future responses to changes in precipitation related to global warming. In particular, metapopulation dynamics of the Laticauda group of sea snakes are expected to change in relation to projected reductions of tropical dry‐season precipitation.

Oxygen Consumption and the Energetics of Island‐Dwelling Florida Cottonmouth Snakes

We measured oxygen consumption (V̇o2) to estimate standard metabolic rates (SMR) in cottonmouth snakes (Agkistrodon piscivorus conanti) from Seahorse Key and the adjacent peninsula of northern Florida. The island population is unusual because adult snakes feed on fish that are dropped by colonial nesting birds, and food resources are temporally limited relative to that of mainland populations. We found no differences in SMR between island and mainland snakes at any of four experimental temperatures (15°–30°C), suggesting that any adjustments to energy limitations involve other aspects of physiology or behavior. As with other viperid species, the SMR of cottonmouths is about one‐half of that expected from interspecific allometric regressions previously reported for snakes generally. Allometric mass exponents of SMR averaged 0.76 and were not affected by temperature. We found that V̇o2 increased with temperature (Q10 = 2.4–2.8) and was elevated 29% during scotophase compared with photophase. Neonates exhibited elevated V̇o2 compared with older juveniles of similar size, apparently due to assimilation of yolk that is present in the neonatal gut. In adult snakes, specific dynamic action (SDA) following feeding resulted in four‐ to eightfold increases in V̇o2, with magnitude and duration related positively to relative meal size. The total energy devoted to SDA increased with meal size and averaged 32.8% ± 4.4% of total ingested energy. We estimate that a nonreproductive 500‐g adult cottonmouth at Seahorse Key uses 3,656 kJ of assimilated energy annually for maintenance and activity, which requires ingestion of approximately 1 kg of fish.

A comparative study of integumentary mucous secretions in amphibians.

Abstract 1. 1. The temporal patterns of discharge from cutaneous mucous glands were quantified over a broad range of body temperature in selected species of amphibians from diverse habitats and having different behavior. Seventy-eight animals representing thirteen species and eight different families were examined. 2. 2. Species which bask in direct sunlight, regardless of phylogenetic position, generally discharge a watery fluid onto their integuments, especially at higher body temperatures. Discharges tend to combine to form a liquid film. 3. 3. In non-basking species, discharge of fluid from cutaneous glands is infrequent or absent. 4. 4. These findings support the theory that “mucous” secretions have a major adaptive role in preventing integumentary desiccation. This would also imply importance of skin secretions in relation to thermoregulation and cutaneous gas exchange.

Physiological correlates of basking in amphibians.

Abstract 1. Body temperatures, heart rate, lung ventilation frequency, and evaporative water loss were determined simultaneously from anuran amphibians, mostly Rana catesbeiana, during exposure to radiation in the laboratory. 2. Observations of integuments and measurements of both subcutaneous temperatures and evaporative water loss suggest that blood circulation is relatively more important than mucous secretions in maintaining normal levels of skin hydration during artificial sun-basking. 3. Evaporative water loss in R. catesbeiana is predominantly cutaneous; losses from buccopharyngeal and pulmonary surfaces account for probably less than 8% of the total. 4. “Panting” responses were not observed at any level of body temperature.

Neural Regulation of Arterial Blood Pressure in Snakes

Systemic arterial pressures of snakes vary interspecifically in relation to gravitational demands imposed by environment and behavior. Terrestrial scansorial and arboreal species are characterized by comparatively high pressures thought to reflect generally greater levels of total peripheral resistance. Pulmonary arterial pressures exhibit less interspecfic variation and are generally lower than systemic pressures, such differences being greater in arboreal species. Both systemic and pulmonary arterial pressures are regulated by neurogenic reflexes, with arboreal species demonstrating superior capability for regulating blood pressure during posture change. Baroreceptors have been identified in the truncus arteriosus and central arteries of snakes, and other mechanoreceptive sites are also likely. Efferent mechanisms affecting vascular muscle tone are correlated with dense adrenergic innervation of vessels that varies interspecifically as well as regionally within species. The evolution of dense but variable adrenergic and peptidergic innervation of the heart and vasculature of snakes emphasizes the importance of autonomic reflexes in mediating regulation of hemodynamics.

Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies

Chemical defenses are widespread among animals, and the compounds involved may be either synthesized from nontoxic precursors or sequestered from an environmental source. Defensive sequestration has been studied extensively among invertebrates, but relatively few examples have been documented among vertebrates. Nonetheless, the number of described cases of defensive sequestration in tetrapod vertebrates has increased recently and includes diverse lineages of amphibians and reptiles (including birds). The best-known examples involve poison frogs, but other examples include natricine snakes that sequester toxins from amphibians and two genera of insectivorous birds. Commonalities among these diverse taxa include the combination of consuming toxic prey and exhibiting some form of passive defense, such as aposematism, mimicry, or presumptive death-feigning. Some species exhibit passive sequestration, in which dietary toxins simply require an extended period of time to clear from the tissues, whereas other taxa exhibit morphological or physiological specializations that enhance the uptake, storage, and/or delivery of exogenous toxins. It remains uncertain whether any sequestered toxins of tetrapods bioaccumulate across multiple trophic levels, but multitrophic accumulation seems especially likely in cases involving consumption of phytophagous or mycophagous invertebrates and perhaps consumption of poison frogs by snakes. We predict that additional examples of defensive toxin sequestration in amphibians and reptiles will be revealed by collaborations between field biologists and natural product chemists. Candidates for future investigation include specialized predators on mites, social insects, slugs, and toxic amphibians. Comprehensive studies of the ecological, evolutionary, behavioral, and regulatory aspects of sequestration will require teams of ecologists, systematists, ethologists, physiologists, molecular biologists, and chemists. The widespread occurrence of sequestered defenses has important implications for the ecology, evolution, and conservation of amphibians and reptiles.