Papers by Marshall D McCue
Oecologia, 2018
Predators often feed on a wide range of prey that can vary in behavior, morphology, and physiolog... more Predators often feed on a wide range of prey that can vary in behavior, morphology, and physiology. The net benefits that predators gain from prey are likely related to both prey nutrient content and prey morphology or defenses. For invertebrates, the exoskeleton is a morphological trait that varies widely among species and during ontogeny and could affect nutrient extraction by predators. The goal of this study was to determine how prey exoskeleton content affected predator nutrient intake, assimilation, and excretion by comparing spiders feeding on either larval or adult mealworms of similar size. We found that the proportion of prey energy invested in digestion was greatest in spiders consuming adult mealworm beetles which had higher amounts of exoskeleton than larvae. Further, spiders extracted a greater proportion of elements, macronutrients, and energy from the larval mealworms, which had lower amounts of exoskeleton. Interestingly, total nitrogen content of prey was not a predictor of nitrogen assimilation as spiders assimilated more nitrogen from the larval mealworms, which had lower total nitrogen content. While adult beetles had higher total nitrogen content, their discarded remains of prey had large amounts of nitrogen that was nutritionally unavailable for spiders (i.e., exoskeleton). These results suggest that prey exoskeleton can affect assimilation efficiency by predators, and that a combination of macronutrient and elemental analyses may be needed to examine the quality of prey for predators and the potential consequences of predation for nutrient flows (e.g., consumer assimilation, egestion, and excretion) in ecosystems.
Oxidation rates of glucose and leucine tracers before, during and after cold exposure for cold-ha... more Oxidation rates of glucose and leucine tracers before, during and after cold exposure for cold-hardy and -susceptible flies
Integrative Zoology, 2020
Individuals that inhabit broad elevational ranges may experience unique environmental challenges.... more Individuals that inhabit broad elevational ranges may experience unique environmental challenges. Because temperature decreases with increased elevation the ectotherms living at high elevations have to manage limited activity time and high thermoregulatory effort. The resting metabolic rate (RMR) of a postabsorptive animal is related to its total energy requirements as well as many other fitness traits. Mesquite lizards (Sceloporus grammicus, Wiegmann 1828) living on La Malinche Volcano, Mexico inhabit a wide elevational range with some populations apparently thriving above the tree line. We measured the RMR of lizards from different elevations (i.e., 2600 m, 3200 m, and 4100 m) at four ecologically relevant temperatures (i.e., 15, 25, 30, and 35°C) and found that RMR of mesquite lizards increased with temperature and body mass. More importantly, lizards from the high-elevation population had mass specific RMR that was higher at all temperatures. While the higher RMRs of high-elevation populations imply higher metabolic costs at a given temperature This article is protected by copyright. All rights reserved. 2 these lizards were also smaller. Both of these traits may allow these high elevation populations to thrive in the face of the thermal challenges imposed by their environment.
Journal of Experimental Biology, 2019
Processing food (e.g. ingestion, digestion, assimilation) requires energy referred to as specific... more Processing food (e.g. ingestion, digestion, assimilation) requires energy referred to as specific dynamic action (SDA) and is at least partially fuelled by oxidation of the nutrients (e.g. proteins and lipids) within the recently ingested meal. In ectotherms, environmental temperature can affect the magnitude and/or duration of the SDA, but is likely to also alter the mixture of nutrients that are oxidized to cover these costs. Here, we examined metabolic rate, gut passage time, assimilation efficiency and fuel use in the lizard Agama atra digesting cricket meals at three ecologically relevant temperatures (20, 25 and 32°C). Crickets were isotopically enriched with 13C-leucine or 13C-palmitic-acid tracers to distinguish between protein and lipid oxidation, respectively. Our results show that higher temperatures increased the magnitude of the SDA peak (by 318% between 32 and 20°C) and gut passage rate (63%), and decreased the duration of the SDA response (by 20% for males and 48% for...
The Journal of experimental biology, Dec 1, 2017
Starvation is common among wild animal populations, and many individuals experience repeated bout... more Starvation is common among wild animal populations, and many individuals experience repeated bouts of starvation over the course of their lives. Although much information has been gained through laboratory studies of acute starvation, little is known about how starvation affects an animal once food is again available (i.e. during the refeeding and recovery phases). Many animals exhibit a curious phenomenon - some seem to 'get better' at starving following exposure to one or more starvation events - by this we mean that they exhibit potentially adaptive responses, including reduced rates of mass loss, reduced metabolic rates, and lower costs of digestion. During subsequent refeedings they may also exhibit improved digestive efficiency and more rapid mass gain. Importantly, these responses can last until the next starvation bout or even be inherited and expressed in the subsequent generation. Currently, however, little is known about the molecular regulation and physiological ...
Journal of Comparative Physiology B, 2015
The carbon isotope values in the exhaled breath of an animal mirror the carbon isotope values of ... more The carbon isotope values in the exhaled breath of an animal mirror the carbon isotope values of the metabolic fuels being oxidized. The measurement of stable carbon isotopes in carbon dioxide is called (13)C-breath testing and offers a minimally invasive method to study substrate oxidation in vivo. (13)C-breath testing has been broadly used to study human exercise, nutrition, and pathologies since the 1970s. Owing to reduced use of radioactive isotopes and the increased convenience and affordability of (13)C-analyzers, the past decade has witnessed a sharp increase in the use of breath testing throughout comparative physiology-especially to answer questions about how and when animals oxidize particular nutrients. Here, we review the practical aspects of (13)C-breath testing and identify the strengths and weaknesses of different methodological approaches including the use of natural abundance versus artificially-enriched (13)C tracers. We critically compare the information that can be obtained using different experimental protocols such as diet-switching versus fuel-switching. We also discuss several factors that should be considered when designing breath testing experiments including extrinsic versus intrinsic (13)C-labelling and different approaches to model nutrient oxidation. We use case studies to highlight the myriad applications of (13)C-breath testing in basic and clinical human studies as well as comparative studies of fuel use, energetics, and carbon turnover in multiple vertebrate and invertebrate groups. Lastly, we call for increased and rigorous use of (13)C-breath testing to explore a variety of new research areas and potentially answer long standing questions related to thermobiology, locomotion, and nutrition.
Annals of the New York Academy of Sciences, 2015
Almost half a century ago, researchers demonstrated that the ratio of stable carbon isotopes in e... more Almost half a century ago, researchers demonstrated that the ratio of stable carbon isotopes in exhaled breath of rats and humans could reveal the oxidation of labeled substrates in vivo, opening a new chapter in the study of fuel use, the fate of ingested substrates, and aerobic metabolism. Until recently, the combined use of respirometry and stable-isotope tracer techniques had not been broadly employed to study fuel use in other animal groups. In this review, we summarize the history of this approach in human and animal research and define best practices that maximize its utility. We also summarize several case studies that use stable-isotope measurements of breath to explore the limits of aerobic metabolism and substrate turnover among several species and various physiological states. We highlight the importance of a comparative approach in revealing the profound effects that phylogeny, ecology, and behavior can have in shaping aerobic metabolism and energetics as well as the fundamental biological principles that underlie fuel use and metabolic function across taxa. New analytical equipment and refinement of methodology make the combined use of respirometry and stable-isotope tracer techniques simpler to perform, less costly, and more field ready than ever before.
FEMS Microbiology Ecology, 2014
Many animals face unpredictable food sources and periods of prolonged fasting, which likely prese... more Many animals face unpredictable food sources and periods of prolonged fasting, which likely present significant challenges to gut microorganisms. While several studies have demonstrated that fasting impacts the gut microbiota, experiments have not been carried out in a comparative context. We used 16S rRNA gene sequencing to document changes in colonic and cecal microbiomes of animals representing five classes of vertebrates at four time points through prolonged fasting: tilapia, toads, geckos, quail, and mice. We found differences in the starvation-induced changes in the microbiome across host species and across gut regions. Microbial phylogenetic diversity increased as a result of fasting in the colons of fish, toads, and mice, while quail exhibited a decrease in diversity; geckos exhibited no change. Microbial diversity in the cecum decreased in fish and exhibited no change in mice. Alterations in relative abundances of microbial taxa varied across hosts. Fish exhibited the most significant changes due to fasting, while geckos maintained a stable community over 28 days of fasting. We uncovered several shared responses of the microbiota across hosts. For example, all tetrapods exhibited decreases in the abundances of Coprobacillus and Ruminococcus in response to fasting. We also discuss hostmediated physiological mechanisms that may underlie these community changes.
Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 2014
During acclimatization to winter, changes in morphology and physiology combined with changes in d... more During acclimatization to winter, changes in morphology and physiology combined with changes in diet may affect how animals use the nutrients they ingest. To study (a) how thermal acclimation and (b) nutritional history affect the rates at which Siberian hamsters (Phodopus sungorus) oxidize different classes of dietary nutrients, we conducted two trials in which we fed hamsters one of three 13 C-labeled compounds, that is, glucose, leucine, or palmitic acid. We predicted that under acute cold stress (3 hr at 2°C) hamsters previously acclimated to cold temperatures (10°C) for 3 weeks would have higher resting metabolic rate (RMR) and would oxidize a greater proportion of dietary fatty acids than animals acclimated to 21°C. We also investigated how chronic nutritional stress affects how hamsters use dietary nutrients. To examine this, hamsters were fed four different diets (control, low protein, low lipid, and low-glycemic index) for 2 weeks. During cold challenges, hamsters previously acclimated to cold exhibited higher thermal conductance and RMR, and also oxidized more exogenous palmitic acid during the postprandial phase than animals acclimated to 21°C. In the nutritional stress trial, hamsters fed the low protein diet oxidized more exogenous glucose, but not more exogenous palmitic acid than the control group. The use of 13 C-labeled metabolic tracers combined with breath testing demonstrated that both thermal and nutritional history results in significant changes in the extent to which animals oxidize dietary nutrients during the postprandial period.
Clinicians and researchers studying protein metabolism in vivo, typically use isotopically-labele... more Clinicians and researchers studying protein metabolism in vivo, typically use isotopically-labeled free amino acids as metabolic tracers rather than isotopically-labeled proteins because such proteins are commercially unavailable. However, the use of free amino acids in lieu of protein tracers violates the critical assumption that tracer molecules undergo the identical biochemical reactions as the tracee molecules of interest. To address this problem we synthesized 13 C-labeled proteins using egg laying hens and investigated the relationship between tracer dose and method of delivery on 13 C-protein production. We enriched hens with one of two isotope tracers (13 C-1-leucine or a uniformly labeled 13 C-amino acid mixture) mixed in their food or dissolved in their drinking water at different dosing levels (86-432 mg day-1). The recovery of 13 C in egg white proteins of the hen fed 13 C-leucine ranged from 14% to 21%; recovery rates were highest at the lowest dosing level. At the highest dosing level egg whites were enriched more than 150‰ above background levels of 13 C. The time required for half maximal 13 C enrichment depended chiefly on the mode of tracer administration, and ranged from 2.5 days for 13 C-leucine dissolved in water to 4.9 days for 13 C-leucine mixed in food. Relative rates of 13 C recovery in the egg protein were lowest for hens fed the uniformly 13 C labeled amino acid mixture, presumably because of the high proportion of nonessential amino acids. The time required for the 13 C-enrichment in eggs to return to background levels at the end of the enrichment period was about twice that required to initially reach isotopic equilibrium with the diet, indicating significant biochemical discrimination of endogenous 13 C amino acids. We conclude that delivering small amounts of 13 C amino acid tracers in the drinking water of hens is the most effective way to produce 13 C-enriched proteins to for tracer studies that do not require δ 13 C-enrichment above 200‰.
Physiological and Biochemical Zoology, 2014
Hosts can manage parasitic infections using an array of tactics, which are likely to vary conting... more Hosts can manage parasitic infections using an array of tactics, which are likely to vary contingent on coevolutionary history between the host and the parasite. Here we asked whether coping ability of congeners that differ in host-parasite coevolutionary history differed in response to experimental infections with a coccidian parasite. House sparrows (Passer domesticus) and gray-headed sparrows (Passer griseus) are sympatric and ecologically similar, but house sparrows are recent colonizers of Kenya, the site of our comparison, whereas gray-headed sparrows are native. We evaluated three variables as barometers of infection coping ability: vertical flight, pectoral muscle size, and fat score. We also measured routing of a dose of 13 C-labeled leucine, an essential amino acid, among tissues to compare resource allocation strategies in response to infection. We found that burden effects on performance were minimal in both species, but house sparrows maintained considerably higher burdens than gray-headed sparrows regardless of exposure. House sparrows also had more exogeneous leucine tracer in all tissues after 24 h, demonstrating a difference in the way the two species allocate or distribute resources. We argue that house sparrows may be maintaining larger resource reserves to mitigate costs associated with exposure and infection. Additionally, in response to increased parasite exposure, gray-headed sparrows had less leucine tracer in their spleens and more in their gonads, whereas house sparrows did not change allocation, perhaps indicating a trade-off that is not experienced by the introduced species.
Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2015
Due to various biochemical fractionation processes during lipid synthesis, the lipid molecules in... more Due to various biochemical fractionation processes during lipid synthesis, the lipid molecules in the body contain substantially lower concentrations of 13 C than the nonlipid molecules. Because of the isotopic differences between these two endogenous nutrient pools, any shift toward nonlipid fuel oxidation would be expected to increase in the δ 13 C of the exhaled breath. Interestingly, the possibility of whether or not an exercise-induced change actually occurs has been debated in literature for over two decades and researchers have still not reached a consensus. We measured ventilatory and metabolic variables before, during, and after exercise in forty-eight adults (n = 25 females, n = 23 males; 20.1 ± 1.9 years) assigned to either a resting treatment or one of three exercising treatments where they maintained a heart rate of 130, 150, or 170 bpm for 56 min. We found that the mean metabolic rates of the exercising groups increased 4.4-fold, 6.1-fold, and 7.7-fold above resting values, respectively. Exercise caused small increases in respiratory exchange ratios (e.g., from 0.83 ± 0.08 to 0.86 ± 0.10) indicative of increased carbohydrate oxidation, but these changes were too variable to be reliably correlated with exercise intensity. In contrast, the δ 13 C of the exhaled breath increased by 0.62 ± 0.19‰, 1.14 ± 0.29‰, and 1.79 ± 0.50‰, respectively, for the three groups and was significantly correlated with the intensity of exercise. We also show that the isotopic difference of the lipid and nonlipids of the body is similar (~2.7‰) even when consuming bulk diets that are isotopically distinct (N 8‰). If not corrected for, these exerciseinduced changes in δ 13 C of the breath would be sufficiently large to skew the results of studies investigating the oxidative fates of exogenous nutritional supplements.
Experimental Gerontology, 2011
Dietary restriction (DR) and reduced reproduction each extend life span in many species. Females ... more Dietary restriction (DR) and reduced reproduction each extend life span in many species. Females undergoing DR typically experience a reduction in their fecundity, which raises the question of whether the two treatments are actually extending life span in overlapping ways. Life span in lubber grasshoppers has been shown to be increased by DR, and separately by ovariectomy (OVX). Here, we test the combination of these on life span. If life extension by the two treatments are additive, it would suggest that they likely act through separate pathways. The experimental groups were: fully reproductive and fully fed (ShamFD); ovariectomized and fully fed (OVX FD); fully reproductive and restricted diet (ShamDR); and ovariectomized and restricted diet (OVX DR). The median life spans of these groups were: ShamFD = 245 d, OVX FD = 285 d, ShamDR = 286 d, and OVX DR = 322 d. Feeding rate for the OVX FD group was 64% of ad libitum, not significantly different from the 70% of ad libitum that was used for ShamDR. We also measured hemolymph parameters of physiology in these same individuals. Hemolymph levels of vitellogenin (the egg yolk-precursor protein) were increased 5-fold by OVX, but were not affected by DR. In addition, hemolymph total anti-oxidant activity (per μg protein) was significantly reduced by OVX, but was not affected by DR. We show that OVX and DR produce different physiological responses in grasshoppers, despite life extensions and feeding levels that were not significantly different. These data suggest that OVX and DR might extend life span via distinct pathways.
This study was conducted to investigate spatio-temporal patterns of exogenous nutrient allocation... more This study was conducted to investigate spatio-temporal patterns of exogenous nutrient allocation in three sympatric North American pit-vipers. Snakes were fed mouse meals artificially labeled with 15N L-Leucine and 1-13C D-glucose. At various time periods following ingestion of labeled mice (i.e. 0, 48, 96, and 144 hours), snakes were sacrificed and the isotope signatures of several tissues were quantified using isotoperatio mass-spectrometry. The results of this study revealed that the three snake species demonstrated similar patterns in background isotope signatures. Cardiac muscle exhibited the highest 15N enrichment whereas skeletal muscle was the most deplete in 15N. Adipose tissue showed the lowest enrichment of 13C whereas skeletal muscle had the greatest 13C enrichment. Tissues of postprandial snakes consuming labeled meals exhibited increases in 15N and 13C over time, but no changes in C:N ratios of postprandial tissues were observed. Exogenous amino acids were found at the greatest levels in hepatic and lower gastrointestinal tissues followed by cardiac muscle and upper gastrointestinal tissues. Absorbed amino acids were allocated at the lowest rates to skeletal muscle and blood cells. Interestingly, the two rattlesnake species preferentially allocated 13C-glucose to hepatic stores whereas copperheads apparently allocated 13C to adipose stores. This study illustrates the potential utility of isotopically labeled physiological fuels to examine dietary allocation strategies in animals and promises to benefit forthcoming investigations into the dietary physiology of animals as well as those quantifying stable isotope flux among ecological food webs.
The Journal of experimental biology, 2015
Pythons digesting rodent meals exhibit up to 10-fold increases in their resting metabolic rate (R... more Pythons digesting rodent meals exhibit up to 10-fold increases in their resting metabolic rate (RMR); this increase in RMR is termed specific dynamic action (SDA). Studies have shown that SDA is partially fueled by oxidizing dietary nutrients, yet it remains unclear whether the proteins and the lipids in their meals contribute equally to this energy demand. We raised two populations of mice on diets labeled with either [(13)C]leucine or [(13)C]palmitic acid to intrinsically enrich the proteins and lipids in their bodies, respectively. Ball pythons (Python regius) were fed whole mice (and pureed mice 3 weeks later), after which we measured their metabolic rates and the δ(13)C in the breath. The δ(13)C values in the whole bodies of the protein- and lipid-labeled mice were generally similar (i.e. 5.7±4.7‰ and 2.8±5.4‰, respectively) but the oxidative kinetics of these two macronutrient pools were quite different. We found that the snakes oxidized 5% of the protein and only 0.24% of the...
PLOS ONE, 2015
Most of our understanding about the physiology of fasting and starvation comes from studies of ve... more Most of our understanding about the physiology of fasting and starvation comes from studies of vertebrates; however, for ethical reasons, studies that monitor vertebrates through the lethal endpoint are scant. Insects are convenient models to characterize the comparative strategies used to cope with starvation because they have diverse life histories and have evolved under the omnipresent challenge of food limitation. Moreover, we can study the physiology of starvation through its natural endpoint. In this study we raised populations of five species of insects (adult grasshoppers, crickets, cockroaches, and larval beetles and moths) on diets labeled with either 13 C-palmitic acid or 13 C-leucine to isotopically enrich the lipids or the proteins in their bodies, respectively. The insects were allowed to become postabsorptive and then starved. We periodically measured the δ 13 C of the exhaled breath to characterize how each species adjusted their reliance on endogenous lipids and proteins as energy sources. We found that starving insects employ a wide range of strategies for regulating lipid and protein oxidation. All of the insects except for the beetle larvae were capable of sharply reducing reliance on protein oxidation; however, this protein sparing strategy was usually unsustainable during the entire starvation period. All insects increased their reliance on lipid oxidation, but while some species (grasshoppers, cockroaches, and beetle larvae) were still relying extensively on lipids at the time of death, other species (crickets and moth larvae) allowed rates of lipid oxidation to return to prestarvation levels. Although lipids and proteins are critical metabolic fuels for both vertebrates and insects, insects apparently exhibit a much wider range of strategies for rationing these limited resources during starvation.
The Journal of Experimental Biology, 2016
The energetics of processing a meal is crucial for understanding energy budgets of animals in the... more The energetics of processing a meal is crucial for understanding energy budgets of animals in the wild. Given that digestion and its associated costs may be dependent on environmental conditions, it is crucial to obtain a better understanding of these costs under diverse conditions and identify resulting behavioural or physiological trade-offs. This study examines the speed and metabolic costs - in cumulative, absolute, and relative energetic terms - of processing a bloodmeal for a major zoonotic disease vector, the tsetse fly Glossina brevipalpis, across a range of ecologically-relevant temperatures (25°C, 30°C & 35°C). Respirometry showed that flies used less energy digesting meals faster at higher temperatures but that their starvation tolerance was reduced supporting the prediction that warmer temperatures are optimal for bloodmeal digestion while cooler temperatures should be preferred for unfed or post-absorptive flies. 13C-Breath testing revealed that the flies oxidized dieta...
Uploads
Papers by Marshall D McCue
mortality. This book summarizes state of the art of starvation biology from the ecological
causes of food limitation to the physiological and evolutionary consequences of
prolonged fasting. It is written for an audience with an understanding of general
principles in animal physiology, yet offers a level of analysis and interpretation that will
engage seasoned scientists. Each chapter is written by active researchers in the field of
comparative physiology and draws on the primary literature of starvation both in nature
and the laboratory. The chapters are organized among broad taxonomic categories, such
as protists, arthropods, fishes, reptiles, birds, and flying, aquatic, and terrestrial mammals
including humans; particularly well-studied animal models, e.g. endotherms are further
organized by experimental approaches, such as analyses of blood metabolites, stable
isotopes, thermobiology, and modeling of body composition.
Research highlights
► Under salinity salt-tolerant olive trees have an higher fine root biomass than salt-sensitive trees. ► Under salinity salt-resistant olive trees sustain an higher root sap-flow density than salt-sensitive trees. ► Salt-sensitive olive trees possess a lower root biomass:necromass ratio under salinity than salt-tolerant ones. ► The ability of fine roots to resist the deleterious effects of NaCl affects the salt resistance of mature olives varieties.