[Show abstract][Hide abstract] ABSTRACT: While global amphibian declines are associated with the spread of Batrachochytrium dendrobatidis (Bd), undetected concurrent co-infection by other pathogens may be little recognized threats to amphibians. Emerging viruses in the genus Ranavirus (Rv) also cause die-offs of amphibians and other ectotherms, but the extent of their distribution globally, or how co-infections with Bd impact amphibians are poorly understood. We provide the first report of Bd and Rv co-infection in South America, and the first report of Rv infections in the amphibian biodiversity hotspot of the Peruvian Andes, where Bd is associated with extinctions. Using these data, we tested the hypothesis that Bd or Rv parasites facilitate co-infection, as assessed by parasite abundance or infection intensity within individual adult frogs. Co-infection occurred in 30% of stream-dwelling frogs; 65% were infected by Bd and 40% by Rv. Among terrestrial, direct-developing Pristimantis frogs 40% were infected by Bd, 35% by Rv, and 20% co-infected. In Telmatobius frogs harvested for the live-trade 49% were co-infected, 92% were infected by Bd, and 53% by Rv. Median Bd and Rv loads were similar in both wild (Bd = 101.2 Ze, Rv = 102.3 viral copies) and harvested frogs (Bd = 103.1 Ze, Rv = 102.7 viral copies). While neither parasite abundance nor infection intensity were associated with co-infection patterns in adults, these data did not include the most susceptible larval and metamorphic life stages. These findings suggest Rv distribution is global and that co-infection among these parasites may be common. These results raise conservation concerns, but greater testing is necessary to determine if parasite interactions increase amphibian vulnerability to secondary infections across differing life stages, and constitute a previously undetected threat to declining populations. Greater surveillance of parasite interactions may increase our capacity to contain and mitigate the impacts of these and other wildlife diseases.
[Show abstract][Hide abstract] ABSTRACT: Diverse biomarkers including stable isotope, hormonal, and ecoimmunological assays are powerful tools to assess animal condition. However, an integrative approach is necessary to provide the context essential to understanding how biomarkers reveal animal health in varied ecological conditions. A barrier to such integration is a general lack of awareness of how shared extraction methods from across fields can provide material from the same animal tissues for diverse biomarker assays. In addition, the use of shared methods for extracting differing tissue fractions can also provide biomarkers for how animal health varies across time. Specifically, no study has explicitly illustrated the depth and breadth of spacial and temporal information that can be derived from coupled biomarker assessments on two easily collected tissues: blood and feathers or hair. This study used integrated measures of glucocorticoids, stable isotopes, and parasite loads in the feathers and blood of fall-migrating Northern saw-whet owls (Aegolius acadicus) to illustrate the wealth of knowledge about animal health and ecology across both time and space. In feathers, we assayed deuterium (δD) isotope and corticosterone (CORT) profiles, while in blood we measured CORT and blood parasite levels. We found that while earlier migrating owls had elevated CORT levels relative to later migrating birds, there was also a disassociation between plasma and feather CORT, and blood parasite loads. These results demonstrate how these tissues integrate time periods from weeks to seasons and reflect energetic demands during differing life stages. Taken together, these findings illustrate the potential for integrating diverse biomarkers to assess interactions between environmental factors and animal health across varied time periods without the necessity of continually recapturing and tracking individuals. Combining biomarkers from diverse research fields into an integrated framework hold great promise for advancing our understanding of environmental effects on animal health.
No preview · Article · Feb 2015 · Ecology and Evolution
[Show abstract][Hide abstract] ABSTRACT: During the past decade, we have gained new insights into the profound effects that essential micronutrients and macronutrients have on biological processes ranging from cellular function, to whole-organism performance, to dynamics in ecological communities, as well as to the structure and function of ecosystems. For example, disparities between intake and organismal requirements for specific nutrients are known to strongly affect animal physiological performance and impose trade-offs in the allocations of resources. However, recent findings have demonstrated that life-history allocation trade-offs and even microevolutionary dynamics may often be a result of molecular-level constraints on nutrient and metabolic processing, in which limiting reactants are routed among competing biochemical pathways. In addition, recent work has shown that complex ecological interactions between organismal physiological states such as exposure to environmental stressors and infectious pathogens can alter organismal requirements for, and, processing of, nutrients, and even alter subsequent nutrient cycling in ecosystems. Furthermore, new research is showing that such interactions, coupled with evolutionary and biogeographical constraints on the biosynthesis and availability of essential nutrients and micronutrients play an important, but still under-studied role in the structuring and functioning of ecosystems. The purpose of this introduction to the symposium "The Micro and Macro of Nutrient Effects in Animal Physiology and Ecology" is to briefly review and highlight recent research that has dramatically advanced our understanding of how nutrients in their varied forms profoundly affect and shape ecological and evolutionary processes.
No preview · Article · Jun 2014 · Integrative and Comparative Biology
[Show abstract][Hide abstract] ABSTRACT: Size variance among similarly aged individuals within populations is a pattern common to many organisms that is a result of interactions between intrinsic and extrinsic traits of individuals. While genetic and maternal effects, as well as physiological and behavioral traits have been shown to contribute to size variation in animal populations, teasing apart the influence of such factors on individual growth rates remain a challenge. Furthermore, tracing the effects of these interactions across life stages and in shaping adult phenotypes also requires further exploration. In this study we investigated the relationship between genetics, hatching patterns, behaviors, neuroendocrine stress axis activity and variance in growth and metamorphosis among same-aged larval amphibians. Through parallel experiments we found that in the absence of conspecific interactions, hatch time and to a lesser extent egg clutch identity (i.e. genetics and maternal effects) influenced the propensity for growth and development in individual tadpoles and determined metamorphic traits. Within experimental groups we found that variance in growth rates was associated with size-dependent foraging behaviors and responses to food restriction. We also found an inverse relationship between glucocorticoid (GC) hormone levels and body mass and developmental stage among group-reared tadpoles, which suggests that GC expression plays a role in regulating differing within-population growth trajectories in response to density-dependent conditions. Taken together these findings suggest that factors that influence hatching conditions can have long-term effects on growth and development. These results also raise compelling questions regarding the extent to which maternal and genetic factors influence physiological and behavioral profiles in amphibians.
[Show abstract][Hide abstract] ABSTRACT: Exposure to adverse environmental conditions during early development can shape life-history traits and have lasting effects on physiological function in later life. Although findings within the biomedical literature have shown that environmentally induced elevations in glucocorticoids (GCs) during critical developmental windows can cause persistent carry-over effects (i.e., developmental programming), little is known about whether such effects of GCs can be generalized to wildlife species. Using wood frogs as a study species, we conducted an experiment with a split-plot design to assess the short-term and the long-term physiological consequences of availability of food, hydroperiod length (i.e., pond drying), and the interaction between these two environmental conditions. In outdoor experimental ponds, we reared tadpoles in chronically high or low-food conditions, and tadpoles from each pond experienced either high water until metamorphosis or a reduction in water volume during late developmental stages (after Gosner stage 38). After metamorphosis, animals were housed individually and fed ad libitum for 10 weeks, and growth rate, fat content, and resting and acute stress-induced GC levels were measured. We found that tadpoles experiencing low availability of food and reduced water volume had elevated GC levels, reduced mass, and body condition as they approached metamorphosis. At 10 weeks after metamorphosis, we found that these two conditions also had persistent interactive effects on post-metamorphic allocation of resources to growth, energy storage, and responsiveness of GCs to a novel stressor. Of individuals that experienced reduced water volume, only those that experienced high food as tadpoles were able to catch up to individuals that did not experience reduced water volume in terms of body mass, femur length, and body condition, and they allocated more resources to fat storage. By contrast, 10-week old frogs with low-food and that experienced low water volume and low-food levels as tadpoles allocated fewer resources to mass-specific growth, stored less fat, and exhibited blunted GC response to a novel stressor relative to those that did not experience water-reduction. Our findings demonstrate that environmental conditions experienced prior to and during important developmental transitions shape resource allocation and the ability to physiologically respond to future stressors in juvenile and potentially adult animals. These results suggest that chronic and acute environmental stressors experienced during early life stages can have cumulative and interactive effects that need to be considered when modeling the ecological and evolutionary consequences of environmental change on populations.
Preview · Article · Aug 2013 · Integrative and Comparative Biology
[Show abstract][Hide abstract] ABSTRACT: The use of stored resources to fuel reproduction, growth, and self-maintenance in the face of uncertain nutrient availability is a tactic common to many organisms. The degree to which organisms rely on stored resources in response to varied nutrients, however, is not well quantified. In this study, we used stable isotope methods to quantify the use of stored versus incoming nutrients to fuel growth and egg and fat body development in lizards under differing nutrient regimes. We found that the degree of capital breeding is a function of an individual's body condition. Furthermore, given sufficient income, lizards in poor condition can allocate simultaneously to storage, growth, and reproduction and "catch up" in body size and reproductive allocation to better-conditioned animals. Using natural variation in the δ(13)C of environmental nutrient pulses, we also found a high degree of variation in capital breeding in a lizard community. These findings demonstrate that capital breeding in lizards is not simply a one-way flow of endogenous stores to eggs but is a function of the condition state of individuals and seasonal nutrient availability. We use our findings to comment on capital breeding in lizards and the utility of the capital-income concept in general.
Full-text · Article · Jul 2012 · The American Naturalist
[Show abstract][Hide abstract] ABSTRACT: Pathogens may induce different immune responses in hosts contingent on pathogen characteristics, host characteristics, or interactions between the two. We investigated whether the broadly effective acute-phase response (APR), a whole body immune response that occurs in response to constitutive immune receptor activation and includes fever, secretion of immune peptides, and sickness behaviors such as anorexia and lethargy, varies with pathogen identity in the house sparrow (Passer domesticus). Birds were challenged with a subcutaneous injection of either a glucan at 0.7 mg/kg (to simulate fungal infection), a synthetic double-stranded RNA at 25 mg/kg (to simulate viral infection), or LPS at 1 mg/kg (to simulate a gram-negative bacterial infection), and then body mass, core body temperature changes, sickness behaviors, and secretion of an acute-phase protein, haptoglobin, were compared. Despite using what are moderate-to-high pyrogen doses for other vertebrates, only house sparrows challenged with LPS showed measurable APRs. Febrile, behavioral, and physiological responses to fungal and viral mimetics had minimal effects.
Full-text · Article · Feb 2011 · AJP Regulatory Integrative and Comparative Physiology
[Show abstract][Hide abstract] ABSTRACT: 1. Animal populations exhibit considerable variation in their susceptibility to infection by emerging diseases, yet it is poorly understood how environmental and intrinsic factors contribute to these patterns. Considering that intrinsic factors (e.g. life history stage, nutritional state) can impact immune function, knowledge of the physiological mechanisms that mediate susceptibility to infection may improve our understanding of the emergence of disease in natural populations.
2. Ranavirus outbreaks have been associated with die-offs of amphibians worldwide. While the ecological factors associated with epidemics have been widely studied, little is known about how physiological factors mediate amphibian responses to ranavirus infection.
3. The neuroendocrine hypothalamus-pituitary-interrenal axis (HPI) is a physiological system central to coordinating energy balance and development. It is known to both stimulate and inhibit immune function in vertebrates in different contexts. We hypothesized that the HPI axis would also mediate responses to ranavirus infection. We used wood frog (Rana sylvatica) larvae and ranavirus isolated from recent die-offs of local wood frog populations to examine the physiological responses to infection.
4. In addition to increasing odds of death with increasing doses of virus in an LD50 study, we saw a 1·7-fold increase in the odds of death with each increase in Gosner stage at the time of infection.
5. We then examined the HPI stress response of prometamorphic tadpoles exposed to a lethal dose of ranavirus. Infected tadpoles exhibited significantly elevated corticosterone levels, more rapid developmental changes, and a greater decrease in body weight relative to controls over 6 days after exposure.
6. Although elevated corticosterone mobilizes resources and enhances immunity, its acceleration of metamorphosis may be maladaptive in response to ranavirus infection, because it can draw energy away from expensive immune responses. These findings provide insight into how the balance of energy between development and immune function may contribute to patterns of ranavirus infection in pre-metamorphic amphibians.
Full-text · Article · Jan 2011 · Functional Ecology
[Show abstract][Hide abstract] ABSTRACT: Carbon stable isotope (delta(13)C) analysis can be used to infer the origin and to estimate the flow of nutrient resources through animals and across ecological compartments. These applications require knowledge of the rates at which carbon is incorporated into animal tissues and diet-to-tissue discrimination factors (Delta(13)C). Studies of carbon dynamics in terrestrial vertebrates to date have focused almost solely on endothermic animals; ectotherms such as reptiles have received little attention. Here we determined carbon incorporation rates and Delta(13)C in tissues of prairie lizards (Sceloporus undulatus consobrinus) and collared lizards (Crotaphytus collaris). The smaller lizard, S. undulatus, had carbon retention times of 25 and 61 d in plasma and red blood cells (RBC), respectively, compared with 44 and 311 d for the larger C. collaris. Liver, muscle, and skin carbon retention times for S. undulatus were 21, 81, and 94 d. Growth contributed 9%-19% of the carbon incorporated into these tissues. This contribution is similar to endotherms measured at comparable developmental stages. Mean Delta(13)C for plasma (-0.2 per thousand +/- 0.4 per thousand Vienna Pee Dee Belemnite Standard) and RBCs (-1.3 per thousand +/- 0.8 per thousand) were similar to values reported for other vertebrates. Carbon incorporation rates for these ectotherms, however, are seven times slower than in similarly sized adult endotherms. Although a limited comparison with data for warm-water fishes suggests comparable incorporation rates between aquatic and terrestrial ectotherms, this study highlights the lack of experimental data for isotope dynamics in ectotherms across a range of temperatures, body sizes, and developmental stages.
[Show abstract][Hide abstract] ABSTRACT: In many ecosystems, seasonal shifts in temperature and precipitation induce pulses of primary productivity that vary in phenology, abundance, and nutritional quality. Variation in these resource pulses could strongly influence community composition and ecosystem function, because these pervasive bottom-up forces play a primary role in determining the biomass, life cycles, and interactions of organisms across trophic levels. The focus of this research is to understand how consumers across trophic levels alter resource use and assimilation over seasonal and interannual timescales in response to climatically driven changes in pulses of primary productivity. We measured the carbon isotope ratios (delta(13)C) of plant, arthropod, and lizard tissues in the northern Chihuahuan Desert to quantify the relative importance of primary production from plants using C3 and C4 photosynthesis for consumers. Summer monsoonal rains on the Sevilleta Long Term Ecological Research (LTER) site in New Mexico support a pulse of C4 plant production that has tissue delta(13)C values distinct from C3 plants. During a year when precipitation patterns were relatively normal, delta(13)C measurements showed that consumers used and assimilated significantly more C4-derived carbon over the course of a summer, tracking the seasonal increase in abundance of C4 plants. In the following spring, after a failure in winter precipitation and the associated failure of spring C3 plant growth, consumers showed elevated assimilation of C4-derived carbon relative to a normal rainfall regime. These findings provide insight into how climate, pulsed resources, and temporal trophic dynamics may interact to shape semiarid grasslands such as the Chihuahuan Desert in the present and future.
[Show abstract][Hide abstract] ABSTRACT: Fundamental to life-history theory is the assumed inverse proportionality between the number of offspring and the resource allocation per offspring. Lizards have been model organisms for empirical tests of this theory for decades; however, the expected negative relationship between clutch size and offspring size is often not detected. Here we use the approach developed by Charnov and Ernest to demonstrate that this often concealed trade-off can be made apparent in an interspecific comparison by correcting for size-dependent resource allocation. Our data set also shows a tight allometry for annual production that is consistent with life-history models for indeterminate growers. To account for nonindependence of species data we also compare the fit of nonphylogenetic and phylogenetic regression models to test for phylogenetic signal in these allometry and trade-off patterns. When combined, these results demonstrate that the offspring size/clutch size trade-off is not isolated to a single clutch but is shaped by the resource investment made over an entire year. We conclude that, across diverse lizard species, there is strong evidence for the predicted trade-off between offspring size and the annual number of eggs produced.
Preview · Article · Oct 2008 · The American Naturalist
[Show abstract][Hide abstract] ABSTRACT: In a 1966 American Naturalist article, G. C. Williams initiated the study of reproductive effort (RE) with the prediction that longer-lived organisms ought to expend less in reproduction per unit of time. We can multiply RE, often measured in fractions of adult body mass committed to reproduction per unit time, by the average adult life span to get lifetime reproductive effort (LRE). Williams's hypothesis (across species, RE decreases as life span increases) can then be refined to read "LRE will be approximately constant for similar organisms." Here we show that LRE is a key component of fitness in nongrowing populations, and thus its value is central to understanding life-history evolution. We then develop metabolic life-history theory to predict that LRE ought to be approximately 1.4 across organisms despite extreme differences in production and growth rates. We estimate LRE for mammals and lizards that differ in growth and production by five- to tenfold. The distributions are approximately normal with means of 1.43 and 1.41 for lizards and mammals, respectively (95% confidence intervals: 1.3-1.5 and 1.2-1.6). Ultimately, therefore, a female can only produce a mass of offspring approximately equal to 1.4 times her own body mass during the course of her life.
Preview · Article · Jan 2008 · The American Naturalist