Title: Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus
Abstract
Elevations >2,000 m represent consistently harsh environments for small endotherms because of abiotic stressors such as cold temperatures and hypoxia.
These environmental stressors may limit the ability of populations living at these elevations to respond to biotic selection pressures—such as parasites or pathogens—that in other environmental contexts would impose only minimal energetic‐ and fitness‐related costs.
We studied deer mice (Peromyscus maniculatus rufinus) living along two elevational transects (2,300–4,400 m) in the Colorado Rockies and found that infection prevalence by botfly larvae (Cuterebridae) declined at higher elevations. We found no evidence of infections at elevations >2,400 m, but that 33.6% of all deer mice, and 52.2% of adults, were infected at elevations <2,400 m.
Botfly infections were associated with reductions in haematocrit levels of 23%, haemoglobin concentrations of 27% and cold‐induced VO2maxmeasures of 19% compared to uninfected individuals. In turn, these reductions in aerobic performance appeared to influence fitness, as infected individuals exhibited 19‐34% lower daily survival rates.
In contrast to studies at lower elevations, we found evidence indicating that botfly infections influence the aerobic capabilities and fitness of deer mice living at elevations between 2,000 and 2,400 m. Our results therefore suggest that the interaction between botflies and small rodents is likely highly context‐dependent and that, more generally, high‐elevation populations may be susceptible to additional biotic selection pressures.
Aplain language summaryis available for this article.
Will, Ian; Linehan, Sara; Jenkins, David G.; de Bekker, Charissa(
, Functional Ecology)
Abstract
Ophiocordycepsfungi manipulate the behaviour of their ant hosts to produce a summit disease phenotype, thereby establishing infected ant cadavers onto vegetation at elevated positions suitable for fungal growth and transmission. Multiple environmental and ecological factors have been proposed to shape the timing, positioning and outcome of these manipulations.
We conducted a long‐term field study ofOphiocordyceps camponoti‐floridaniinfections ofCamponotus floridanusants—the Florida zombie ants. We propose and refine hypotheses on the factors that shape infection outcomes by tracking the occurrence of and fungal growth from hundreds of ant cadavers. We modelled and report these data in relation to weather, light, vegetation and attack by hyperparasites.
We investigated environmental factors that could affect the occurrence and location of newly manipulated ant cadavers. New cadaver occurrence was preferentially biased towards epiphyticTillandsiabromeliads, canopy openness and summer weather conditions (an interactive effect of temperature, humidity and precipitation). Furthermore, we suggest that incident light at the individual cadaver level reflects microhabitat choice by manipulated ants or selective pressure on cadaver maintenance for conditions that improve fungal survival.
We also asked which environmental conditions affect fungal fitness. Continued fungal development of reproductive structures and putative transmission increased with moist weather conditions (interaction of humidity and precipitation) and canopy openness, while being reduced by hyperparasitic mycoparasite infections. Moreover, under the most open canopy conditions, we found an atypicalOphiocordycepsgrowth morphology that could represent a plastic response to conditions influenced by high light levels.
Taken together, we explore general trends and the effects of various ecological conditions on host and parasite disease outcomes in the Florida zombie ant system. These insights from the field can be used to inform experimental laboratory setups that directly test the effects of biotic and abiotic factors on fungus–ant interactions or aim to uncover underlying molecular mechanisms.
Read the freePlain Language Summaryfor this article on the Journal blog.
Williams, Terrie M.; Peter‐Heide Jørgensen, Mads; Pagano, Anthony M.; Bryce, Caleb M.; Crocker, ed., Daniel(
, Functional Ecology)
Abstract
Global biotic and abiotic threats, particularly from pervasive human activities, are progressively pushing large, apex carnivorous mammals into the functional role of mesopredator. Hunters are now becoming the hunted. Despite marked impacts on these animals and the ecosystems in which they live, little is known about the physiological repercussions of this role downgrading from ultimate to penultimate predator.
Here we examine how such ecological role reversals alter the physiological processes associated with energy expenditure, and ultimately the cost of survival during peak performance.
Taxonomic group, preferred habitat and domestication affected the capacity of the oxygen pathway to support high levels of aerobic performance by carnivorous mammals. Fear responses associated with anthropogenic threats also impacted aerobic performance.
Allometric trends for three energetic metrics [maximum oxygen consumption, field metabolic rates (FMRs) and the cost per stride or stroke], showed distinct trends in aerobic capacity for different evolutionary lineages of mammalian predators. Cursorial canids that chase down prey demonstrated the highest relative maximum oxygen consumption rates (10–25 times resting levels) and FMRs, while ambush predators (i.e. felids) and diving marine mammals had aerobic capacities that were similar to or lower than sedentary domestic mammals of comparable size.
The maximum energetic cost of performance for apex predators depended on whether the animals were hunters or the hunted. Escape responses were exceptionally costly for marine (narwhalMonodon monoceros) and terrestrial (mountain lionPuma concolor) locomotor specialists, as well as semi‐aquatic (polar bearUrsus maritimus) species; all showed a nearly two‐fold increase in peak energy expenditure when avoiding threats.
As the duration and frequency of threats to wild species continue to grow, cumulative energetic costs are becoming more apparent. In view of this, attention to the energy demands of apex predators will provide vital predictive power to anticipate mismatches between a species' functional design and human‐induced pressures, and allow for the development of conservation strategies based on how species are built to survive.
A freePlain Language Summarycan be found within the Supporting Information of this article.
Zimmer, Cedric; Taff, Conor C.; Ardia, Daniel R.; Ryan, Thomas A.; Winkler, David W.; Vitousek, Maren N.; Angelier, ed., Frédéric(
, Functional Ecology)
Abstract
Individuals often vary markedly in their ability to cope with stressors, but the drivers of this variation remain poorly understood. Many studies have tested relationships among individual variation in glucocorticoid levels and the response to challenges—often finding inconsistent patterns; however, few have addressed whether variation in the capacity to terminate the stress response through negative feedback is associated with stress resilience.
While conceptual models predict that interactions among different components of hypothalamic–pituitary–adrenal (HPA) axis regulation may be important predictors of the phenotypic and fitness effects of stress, we are aware of no previous experimental tests of this hypothesis.
We investigate whether individual variation in HPA axis regulation is related to resilience to experimental challenges in free‐living tree swallows (Tachycineta bicolor). We mimicked salient natural challenges by temporarily reducing flight efficiency or increasing perceived predation risk during incubation, and determined whether HPA axis responsiveness prior to treatments predicted resilience.
Females that exhibited both a robust HPA axis activation and strong negative feedback were less likely to abandon nests during incubation.
Our results suggest that exhibiting a strong HPA axis activation coupled with effective negative feedback may predict stress resilience. Therefore, the ability to turn on and then off the HPA axis efficiently may be important for fitness.
Our results also suggest that the interactions between different components of the HPA axis may provide greater insight into differences in stress coping capacity.
Aplain language summaryis available for this article.
Global climate change and shifting land‐use are increasing plant stress due to abiotic factors such as drought, heat, salinity and cold, as well as via the intensification of biotic stressors such as herbivores and pathogens. The ability of plants to tolerate such stresses is modulated by the bacteria and fungi that live on or inside of plant tissues and comprise the plant microbiome. However, the impacts of diverse classes of beneficial members of the microbiome and the contrasting stresses that impact plants are most commonly studied independently of each other.
Our meta‐analysis of 288 experiments across 89 studies moves beyond previous studies in that we simultaneously compare the roles of bacterial versus fungal microbiome members that live within plant tissues and colonize plant surfaces in ameliorating biotic versus abiotic sources of plant stress.
The magnitude of microbial stress amelioration can be measured as the greater proportional impact of beneficial microbes on plant performance in more stressful environments. In the plant experiments we examine, the magnitude of microbial stress amelioration is substantial: it is 23% of the effect size of the typical impact of stress and 56% of the effect size of beneficial microbiome members in the absence of stress.
The amount of benefit microbiome members confer to plants differs among classes of microbes, depending on whether plants are grown in stressful or non‐stressful environments. In the absence of stress, beneficial bacteria tend to confer greater plant benefits than do fungi. However, symbiotic fungi, especially arbuscular mycorrhizal fungi, more strongly ameliorate plant stress than do bacteria. In particular, beneficial microbes ameliorate salinity, foliar herbivory and fungal pathogen stress.
These results highlight the fact that the impacts of beneficial and antagonistic components of the microbiome on plant performance depend on biotic and abiotic environmental contexts. Furthermore, beneficial microbes are especially critical for plant health in stressful environments and thus present opportunities to mitigate negative consequences of global change.
A freeplain language summarycan be found within the Supporting Information of this article.
Mahalingam, Sajeni; Cheviron, Zachary A.; Storz, Jay F.; McClelland, Grant B.; Scott, Graham R.(
, The Journal of Physiology)
Key points
Small mammals native to high altitude must sustain high rates of thermogenesis to cope with cold. Skeletal muscle is a key site of shivering and non‐shivering thermogenesis, but the importance of mitochondrial plasticity in cold hypoxic environments remains unresolved.
We examined high‐altitude deer mice, which have evolved a high capacity for aerobic thermogenesis, to determine the mechanisms of mitochondrial plasticity during chronic exposure to cold and hypoxia, alone and in combination.
Cold exposure in normoxia or hypoxia increased mitochondrial leak respiration and decreased phosphorylation efficiency and OXPHOS coupling efficiency, which may serve to augment non‐shivering thermogenesis. Cold also increased muscle oxidative capacity, but reduced the capacity for mitochondrial respiration via complex II relative to complexes I and II combined.
High‐altitude mice had a more oxidative muscle phenotype than low‐altitude mice.
Therefore, both plasticity and evolved changes in muscle mitochondria contribute to thermogenesis at high altitude.
Abstract
Small mammals native to high altitude must sustain high rates of thermogenesis to cope with cold and hypoxic environments. Skeletal muscle is a key site of shivering and non‐shivering thermogenesis, but the importance of mitochondrial plasticity in small mammals at high altitude remains unresolved. High‐altitude deer mice (Peromyscus maniculatus) and low‐altitude white‐footed mice (P. leucopus) were born and raised in captivity, and chronically exposed as adults to warm (25°C) normoxia, warm hypoxia (12 kPa O2), cold (5°C) normoxia, or cold hypoxia. We then measured oxidative enzyme activities, oxidative fibre density and capillarity in the gastrocnemius, and used a comprehensive substrate titration protocol to examine the function of muscle mitochondria by high‐resolution respirometry. Exposure to cold in both normoxia or hypoxia increased the activities of citrate synthase and cytochrome oxidase. In lowlanders, this was associated with increases in capillary density and the proportional abundance of oxidative muscle fibres, but in highlanders, these traits were unchanged at high levels across environments. Environment had some distinct effects on mitochondrial OXPHOS capacity between species, but the capacity of complex II relative to the combined capacity of complexes I and II was consistently reduced in both cold environments. Both cold environments also increased leak respiration and decreased phosphorylation efficiency and OXPHOS coupling efficiency in both species, which may serve to augment non‐shivering thermogenesis. These cold‐induced changes in mitochondrial function were overlaid upon the generally more oxidative phenotype of highlanders. Therefore, both plasticity and evolved changes in muscle mitochondria contribute to thermogenesis at high altitudes.
Wilde, Luke R., Wolf, Cole J., Porter, Stephanie M., Stager, Maria, Cheviron, Zachary A., Senner, Nathan R., and White, ed., Craig. Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus. Functional Ecology 33.4 Web. doi:10.1111/1365-2435.13276.
Wilde, Luke R., Wolf, Cole J., Porter, Stephanie M., Stager, Maria, Cheviron, Zachary A., Senner, Nathan R., & White, ed., Craig. Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus. Functional Ecology, 33 (4). https://doi.org/10.1111/1365-2435.13276
Wilde, Luke R., Wolf, Cole J., Porter, Stephanie M., Stager, Maria, Cheviron, Zachary A., Senner, Nathan R., and White, ed., Craig.
"Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus". Functional Ecology 33 (4). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/1365-2435.13276.https://par.nsf.gov/biblio/10461685.
@article{osti_10461685,
place = {Country unknown/Code not available},
title = {Botfly infections impair the aerobic performance and survival of montane populations of deer mice, Peromyscus maniculatus rufinus},
url = {https://par.nsf.gov/biblio/10461685},
DOI = {10.1111/1365-2435.13276},
abstractNote = {Abstract Elevations >2,000 m represent consistently harsh environments for small endotherms because of abiotic stressors such as cold temperatures and hypoxia.These environmental stressors may limit the ability of populations living at these elevations to respond to biotic selection pressures—such as parasites or pathogens—that in other environmental contexts would impose only minimal energetic‐ and fitness‐related costs.We studied deer mice (Peromyscus maniculatus rufinus) living along two elevational transects (2,300–4,400 m) in the Colorado Rockies and found that infection prevalence by botfly larvae (Cuterebridae) declined at higher elevations. We found no evidence of infections at elevations >2,400 m, but that 33.6% of all deer mice, and 52.2% of adults, were infected at elevations <2,400 m.Botfly infections were associated with reductions in haematocrit levels of 23%, haemoglobin concentrations of 27% and cold‐induced VO2maxmeasures of 19% compared to uninfected individuals. In turn, these reductions in aerobic performance appeared to influence fitness, as infected individuals exhibited 19‐34% lower daily survival rates.In contrast to studies at lower elevations, we found evidence indicating that botfly infections influence the aerobic capabilities and fitness of deer mice living at elevations between 2,000 and 2,400 m. Our results therefore suggest that the interaction between botflies and small rodents is likely highly context‐dependent and that, more generally, high‐elevation populations may be susceptible to additional biotic selection pressures. Aplain language summaryis available for this article.},
journal = {Functional Ecology},
volume = {33},
number = {4},
publisher = {Wiley-Blackwell},
author = {Wilde, Luke R. and Wolf, Cole J. and Porter, Stephanie M. and Stager, Maria and Cheviron, Zachary A. and Senner, Nathan R. and White, ed., Craig},
}
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