Christopher R. Tracy

Physiology on a Landscape Scale: Plant-Animal Interactions

Abstract We explore in this paper how animals can be affected by variation in climate, topography, vegetation characteristics, and body size. We utilize new spatially explicit state-of-the-art models that incorporate principles from heat and mass transfer engineering, physiology, morphology, and behavior that have been modified to provide spatially explicit hypotheses using GIS. We demonstrate how temporal and spatial changes in microclimate resulting from differences in topography and vegetation cover alter animal energetics, and behavior. We explore the impacts of these energetic predictions on elk energetics in burned and unburned stands of conifer in winter in Yellowstone National Park, chuckwalla lizard distribution limits in North America, California Beechey Ground squirrel and Dusky Footed woodrat mass and energy requirements and activity patterns on the landscape, their predator prey interactions with a rattlesnake, Crotalus viridis, and shifts in that food web structure due to topographic and vegetative variation. We illustrate how different scales of data/observation provide different pieces of information that may collectively define the real distributions of a species. We then use sensitivity analyses of energetic models to evaluate hypotheses about the effects of changes in core temperature (fever) global climate (increased air temperature under a global warming scenario) and vegetation cover (deforestation) on winter survival of elk, the geographic distribution of chuckwallas and the activity overlap of predator and prey species within a subset of commonly observed species in a terrestrial food web. Variation in slope and aspect affect the spatial variance in solar radiation incident on the ground, hence ground surface temperature, at the same elevation, same hourly 2 m air temperatures, and wind speeds. We illustrate visually how spatial effects and landscape heterogeneity make statistical descriptions of animal responses problematic, since multiple distributions of their responses to climate, topography, and vegetation on the landscape can yield the same descriptive statistics, especially at high (30 m) resolution. This preliminary analysis suggests that the model has far-reaching implications for hypothesis testing in ecology at a variety of spatial and temporal scales.

The digestive adaptation of flying vertebrates: High intestinal paracellular absorption compensates for smaller guts

Anecdotal evidence suggests that birds have smaller intestines than mammals. In the present analysis, we show that small birds and bats have significantly shorter small intestines and less small intestine nominal (smooth bore tube) surface area than similarly sized nonflying mammals. The corresponding >50% reduction in intestinal volume and hence mass of digesta carried is advantageous because the energetic costs of flight increase with load carried. But, a central dilemma is how birds and bats satisfy relatively high energy needs with less absorptive surface area. Here, we further show that an enhanced paracellular pathway for intestinal absorption of water-soluble nutrients such as glucose and amino acids may compensate for reduced small intestines in volant vertebrates. The evidence is that l-rhamnose and other similarly sized, metabolically inert, nonactively transported monosaccharides are absorbed significantly more in small birds and bats than in nonflying mammals. To broaden our comparison and test the veracity of our finding we surveyed the literature for other similar studies of paracellular absorption. The patterns found in our focal species held up when we included other species surveyed in our analysis. Significantly greater amplification of digestive surface area by villi in small birds, also uncovered by our analysis, may provide one mechanistic explanation for the observation of higher paracellular absorption relative to nonflying mammals. It appears that reduced intestinal size and relatively enhanced intestinal paracellular absorption can be added to the suite of adaptations that have evolved in actively flying vertebrates.

Comparative Analysis of Cutaneous Evaporative Water Loss in Frogs Demonstrates Correlation with Ecological Habits

Most frog species show little resistance to evaporative water loss (EWL), but some arboreal species are known to have very high resistances. We measured EWL and cutaneous resistance to evaporation (Rc) in 25 species of frogs from northern Australia, including 17 species in the family Hylidae, six species in the Myobatrachidae, and one each in the Bufonidae and the Microhylidae. These species display a variety of ecological habits, including aquatic, terrestrial, and arboreal specialisations, with the complete range of habits displayed within just the one hylid genus, Litoria. The 25 species measured in this study have resistances that range from Rc = 0 to 63.1. These include low values indistinguishable from a free water surface to high values typical of “waterproof” anuran species. There was a strong correlation between ecological habit and Rc, even taking phylogenetic relationships into account; arboreal species had the highest resistance, aquatic species tended to have little or no resistance, and terrestrial species tended to have resistance between those of arboreal and aquatic frogs. For one species, Litoria rubella, we found no significant changes in EWL along a 1,500‐km aridity gradient. This study represents the strongest evidence to date of a link between ecological habits and cutaneous resistance to water loss among species of frogs.

ESTIMATING AGE OF TURTLES FROM GROWTH RINGS: A CRITICAL EVALUATION OF THE TECHNIQUE

The technique of counting growth rings to estimate age of turtles is widespread in the scientific literature. Review articles to date have provided primarily lists of authors who have found the technique useful or not, but these reviews have failed to evaluate properly how well the technique actually works. In an attempt to examine how well the published literature supports a biologically meaningful relationship between age and number of growth rings, we surveyed 145 scientific papers that have used counts of rings on scutes to estimate age of individual turtles. Of the 145 papers surveyed, the authors of 44 papers, which comprised 49 case studies, presented data testing the use of growth ring counts for a population of turtles. Of these 49 case studies, 6 reported that the use of the technique was reliable for aging their turtle species past sexual maturity, 15 reported its use to be reliable for aging turtles to young adult (i.e., sexual maturity), 8 reported its use to be reliable for aging juvenile turtles, 2 found it to be reliable with no age limit given, and 8 reported its use unreliable as a method for aging their turtles. The remainder of the case studies presented data that were difficult for us to interpret as reliable or unreliable. Although 22 papers addressed the pattern of growth ring deposition, only four case studies had sufficient data to indicate that a consistent number of rings was added each year. In this paper, we illustrate how the widespread use of this technique ultimately has led to its acceptance without the rigor of tests of its validity or accuracy. We conclude that (a) studies attempting to calibrate the relationship between growth rings and age are few, (b) a majority of the papers that we surveyed referenced other papers that did not themselves include a test justifying growth ring counts as an estimate of turtle age, (c) aging turtles from counts of growth rings might be feasible in some types of studies, for some species at some locations, but only after calibrating the relationship between ring counts and age for each circumstance, and (d) there is currently no justification for generalizing the use of growth rings to estimate turtle age for many species.

Not just small, wet, and cold: effects of body size and skin resistance on thermoregulation and arboreality of frogs

We used simulations from a biophysical model that integrates interlinked exchanges of energy and water between frogs and their environments to address questions about the limits to thermoregulation and about adaptations for arboreality. Body size and cutaneous resistance (Rc) both significantly affected body temperature (Tb) and the time to desiccate to 70% of standard mass (an ecologically relevant metric of desiccation). Cutaneous resistances < 25 s/cm allow basking frogs to elevate their Tb several degrees above ambient, but Rc above 25 had little additional effect on Tb. Small frogs (<10 g) are able to elevate their Tb above ambient while basking, even with small Rc. Large frogs must have greater skin resistances to be able to elevate body temperatures above ambient, yet large frogs take longer to desiccate to 70% of their standard mass. Frogs can avoid rapid desiccation with high Rc, a large body size, or some combination of these traits. Our literature survey indicates that frogs with a combination of Rc and body size that would result in long times to desiccate to 70% of standard mass tend to be arboreal, suggesting that those species may be selectively favored in a niche that often requires frogs to be away from water sources for extended periods of time.

Absorption of sugars in the Egyptian fruit bat (Rousettus aegyptiacus): a paradox explained

SUMMARY Two decades ago D. J. Keegan reported results on Egyptian fruit bats (Rousettus aegyptiacus, Megachiroptera) that were strangely at odds with the prevailing understanding of how glucose is absorbed in the mammalian intestine. Keegans in vitro tests for glucose transport against a concentration gradient and with phloridzin inhibition in fruit bat intestine were all negative, although he used several different tissue preparations and had positive control results with laboratory rats. Because glucose absorption by fruit bats is nonetheless efficient, Keegan postulated that the rapid glucose absorption from the fruit bat intestine is not through the enterocytes, but must occur via spaces between the cells. Thus, we hypothesized that absorption of water-soluble compounds that are not actively transported would be extensive in these bats, and would decline with increasing molecular mass in accord with sieve-like paracellular absorption. We did not presume from Keegans studies that there is no Na+-coupled, mediated sugar transport in these bats, and our study was not designed to rule it out, but rather to quantify the level of possible non-mediated absorption. Using a standard pharmacokinetic technique, we fed, or injected intraperitonealy, the metabolically inert carbohydrates l-rhamnose (molecular mass=164 Da) and cellobiose (molecular mass=342 Da), which are absorbed by paracellular uptake, and 3-O-methyl-d-glucose (3OMd-glucose), a d-glucose analog that is absorbed via both mediated (active) and paracellular uptake. As predicted, the bioavailability of paracellular probes declined with increasing molecular mass (rhamnose, 62±4%; cellobiose, 22±4%) and was significantly higher in bats than has been reported for rats and other mammals. In addition, fractional absorption of 3OMd-glucose was high (91±2%). We estimated that Egyptian fruit bats rely on passive, paracellular absorption for the majority of their glucose absorption (at least 55% of 3OMd-glucose absorption), much more than in non-flying mammals.

Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia.

Hypolithic microbes, primarily cyanobacteria, inhabit the highly specialized microhabitats under translucent rocks in extreme environments. Here we report findings from hypolithic cyanobacteria found under three types of translucent rocks (quartz, prehnite, agate) in a semiarid region of tropical Australia. We investigated the photosynthetic responses of the cyanobacterial communities to light, temperature and moisture in the laboratory, and we measured the microclimatic variables of temperature and soil moisture under rocks in the field over an annual cycle. We also used molecular techniques to explore the diversity of hypolithic cyanobacteria in this community and their phylogenetic relationships within the context of hypolithic cyanobacteria from other continents. Based on the laboratory experiments, photosynthetic activity required a minimum soil moisture of 15% (by mass). Peak photosynthetic activity occurred between approximately 8 degrees C and 42 degrees C, though some photosynthesis occurred between -1 degrees C and 51 degrees C. Maximum photosynthesis rates also occurred at light levels of approximately 150-550 micromol m(-2) s(-1). We used the field microclimatic data in conjunction with these measurements of photosynthetic efficiency to estimate the amount of time the hypolithic cyanobacteria could be photosynthetically active in the field. Based on these data, we estimated that conditions were appropriate for photosynthetic activity for approximately 942 h (approximately 75 days) during the year. The hypolithic cyanobacteria community under quartz, prehnite and agate rocks was quite diverse both within and between rock types. We identified 115 operational taxonomic units (OTUs), with each rock hosting 8-24 OTUs. A third of the cyanobacteria OTUs from northern Australia grouped with Chroococcidiopsis, a genus that has been identified from hypolithic and endolithic communities from the Gobi, Mojave, Atacama and Antarctic deserts. Several OTUs identified from northern Australia have not been reported to be associated with hypolithic communities previously.

Ecology of Aestivation in a Cocoon-forming Frog, Cyclorana Australis (Hylidae)

Abstract We examined burrow microclimate and cocoon formation of the burrowing frog, Cyclorana australis, from northern Australia, during the dormancy season by monitoring frogs in burrows in the field. At the beginning of the dry season, while the soils were still quite moist, frogs dug shallow burrows, with 2–8 cm of soil above the top of the burrow chamber. The frogs spent 2–3 months underground without cocoons, but they began to form cocoons once the soils dried to water potentials that would dehydrate the frogs (as determined by laboratory experiments on water exchange). Frogs remained underground for up to six months, and then emerged when soil water potentials were great enough to permit water absorption, although it is unclear whether this was the primary cue for emergence. Soil temperatures adjacent to burrows were intermediate to those in full sun and full shade at 10-cm depth and increased throughout the dormancy period. Frogs removed from burrows after 2–4 months underground had a body mass 136% of their standard mass, indicating that burrowed frogs store a considerable amount of water in the bladder while in the burrows in the early weeks of aestivation. Because C. australis absorb water during the first part of aestivation (or at least maintain water they absorbed prior to burrowing), and construct a relatively impermeable cocoon during the latter part of aestivation, when they could lose water, these frogs may never experience water stress, despite being underground in the dry season for 5–6 months.

Evaluating Thermoregulation in Reptiles: An Appropriate Null Model

Established indexes of thermoregulation in ectotherms compare body temperatures of real animals with a null distribution of operative temperatures from a physical or mathematical model with the same size, shape, and color as the actual animal but without mass. These indexes, however, do not account for thermal inertia or the effects of inertia when animals move through thermally heterogeneous environments. Some recent models have incorporated body mass, to account for thermal inertia and the physiological control of warming and cooling rates seen in most reptiles, and other models have incorporated movement through the environment, but none includes all pertinent variables explaining body temperature. We present a new technique for calculating the distribution of body temperatures available to ectotherms that have thermal inertia, random movements, and different rates of warming and cooling. The approach uses a biophysical model of heat exchange in ectotherms and a model of random interaction with thermal environments over the course of a day to create a null distribution of body temperatures that can be used with conventional thermoregulation indexes. This new technique provides an unbiased method for evaluating thermoregulation in large ectotherms that store heat while moving through complex environments, but it can also generate null models for ectotherms of all sizes.

Regulation of Gut Function Varies with Life‐History Traits in Chuckwallas (Sauromalus obesus: Iguanidae)

We examined the effects of hibernation and fasting on intestinal glucose and proline uptake rates of chuckwallas (Sauromalus obesus) and on the size of organs directly or indirectly related to digestion. These lizards show geographic variation in body size and growth rate that parallels an elevational gradient in our study area. At low elevation, food is available only for a short time during the spring; at high elevation, food may also be available during summer and autumn, depending on rainfall conditions in a given year. We hypothesized that low‐elevation lizards with a short season of food availability would show more pronounced regulation of gut size and function than high‐elevation lizards with prolonged or bimodal food availability. Hibernating lizards from both elevations had significantly lower uptake rates per milligram intestine for both nutrients, and lower small intestine mass, than active lizards. The combination of these two effects resulted in significantly lower total nutrient uptake in hibernating animals compared to active ones. The stomach, large intestine, and cecum showed lower masses in hibernators, but these results were not statistically significant. The heart, kidney, and liver showed no difference in mass between hibernating and nonhibernating animals. Lizards from low elevations with a short growing season also showed a greater increase in both uptake rates and small intestine mass from the hibernating to the active state, compared to those from high elevations with longer growing seasons. Thus, compared to those from long growing season areas, lizards from short growing season areas have equal uptake capacity during hibernation but much higher uptake capacity while active and feeding. This pattern of regulation of gut function may or may not be an adaptive response, but it is consistent with variation in life‐history characteristics among populations. In areas with a short season, those lizards that can extract nutrients quickly and then reduce the gut will be favored; in areas where food may be available later in the year, those lizards that maintain an active gut would be favored. While other researchers have found much greater magnitudes of gut regulation when making comparisons among species, we find the different patterns of change in gut function between different populations of chuckwallas particularly intriguing because they occur within a single species.