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  1. Abstract

    Monitoring the health of wildlife populations is essential in the face of increased agricultural expansion and forest fragmentation. Loss of habitat and habitat degradation can negatively affect an animal’s physiological state, possibly resulting in immunosuppression and increased morbidity or mortality. We sought to determine how land conversion may differentially impact cellular immunity and infection risk in Neotropical bats species regularly infected with bloodborne pathogens, and to evaluate how effects may vary over time and by dietary habit. We studied common vampire bats (Desmodus rotundus), northern yellow-shouldered bats (Sturnira parvidens) and Mesoamerican mustached bats (Pteronotus mesoamericanus), representing the dietary habits of sanguivory, frugivory and insectivory respectively, in northern Belize. We compared estimated total white blood cell count, leukocyte differentials, neutrophil to lymphocyte ratio and infection status with two bloodborne bacterial pathogens (Bartonella spp. and hemoplasmas) of 118 bats captured in a broadleaf, secondary forest over three years (2017–2019). During this period, tree cover decreased by 14.5% while rangeland expanded by 14.3%, indicating increasing habitat loss and fragmentation. We found evidence for bat species-specific responses of cellular immunity between years, with neutrophil counts significantly decreasing in S. parvidens from 2017 to 2018, but marginally increasing in D. rotundus. However, the odds of infection with Bartonella spp. and hemoplasmas between 2017 and 2019 did not differ between bat species, contrary to our prediction that pathogen prevalence may increase with land conversion. We conclude that each bat species invested differently in cellular immunity in ways that changed over years of increasing habitat loss and fragmentation. We recommend further research on the interactions between land conversion, immunity and infection across dietary habits of Neotropical bats for informed management and conservation.

     
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  2. Free, publicly-accessible full text available December 1, 2024
  3. Synopsis

    Comparative analyses in biology rely on the quality of available data. Methodological differences among studies may introduce variation in results that obscure patterns. In the field of eco-immunology, functional immune assays such as antimicrobial capacity assays are widely used for among-species applications. Sample storage time and animal handling time can influence assay results in some species, but how sample holding time prior to freezing influences assay results is unknown. Sample holding time can vary widely in field studies on wild animals, prompting the need to understand the implications of such variation on assay results. We investigated the hypothesis that sample holding time prior to freezing influences assay results in six species (Leiocephalus carinatus, Iguana iguana, Loxodonta africana, Ceratotherium simum, Columba livia, and Buteo swainsoni) by comparing antibacterial capacity of serum with varying processing times prior to snap-freezing. Blood was collected once from each individual and aliquots were placed on ice and assigned different holding times (0, 30, 60, 180, and 240 min), after which each sample was centrifuged, then serum was separated and snap-frozen on dry ice and stored at −80ºC for 60 days prior to assaying. For each aliquot, we conducted antibacterial capacity assays with serial dilutions of serum inoculated with E. coli and extracted the dilution at 50% antibacterial capacity for analysis. We found a decrease in antibacterial capacity with increased holding time in one of the six species tested (B. swainsoni), driven in part by complete loss of antibacterial capacity in some individuals at the 240-min time point. While the majority of species’ antibacterial capacity were not affected, our results demonstrate the need to conduct pilot assays spanning the anticipated variation in sample holding times to develop appropriate field protocols.

     
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  4. The immune system undergoes marked changes during aging characterized by a state of chronic, low-grade inflammation, so called inflammaging. Domestic dogs are the most morphological and physiological diverse group of mammals, with the widest range in body masses for a single species. Additionally, smaller dogs tend to live significantly longer than larger dogs across all breeds. Body mass is intricately linked to mass-specific metabolism and aging rates, thus, dogs are exemplary for studies in inflammaging. Dermal fibroblasts cells play an important role in skin inflammation, and as such, are a good cell type to determine inflammatory patterns in dogs. Here, we examine aerobic and glycolytic cellular metabolism, and IL-6 concentrations in primary fibroblast cells isolated from small and large, young and old dogs when treated with lipopolysaccharide (LPS) from Escherichia coli to stimulate an inflammatory phenotype. We found no differences in cellular metabolism of any group when treated with LPS. Unlike mice and humans, there was a less drastic amplification of IL-6 concentration after LPS treatment in the geriatric population of dogs compared with puppies. We also found evidence that large breed puppies have significantly less background or control IL-6 concentrations compared with small breed puppies. This implies that the patterns of inflammaging in dogs may be distinct and different from other mammals commonly studied. 
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  5. ABSTRACT Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints probably have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells – lymphocytes and granulocytes (neutrophils/heterophils) – across 63 bat species, 400 bird species and 251 non-volant mammal species. By using phylogenetically informed statistical models on field-collected data from wild Neotropical bats and from captive bats, non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Our inability to distinguish bat lymphocyte scaling from birds and bat granulocyte scaling from all other taxa suggests there may be other ecological explanations (i.e. not flight related) for the cell proportion scaling patterns. Future comparative studies of wild bats, birds and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense and its role in the tolerance of (zoonotic) infections. 
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  6. null (Ed.)
    Canids are a morphological and physiological diverse group of animals, with the most diversity found within one species, the domestic dog. Underlying observed morphological differences, there must also be differences at other levels of organization that could lead to elucidating aging rates and life span disparities between wild and domestic canids. Furthermore, small-breed dogs live significantly longer lives than large-breed dogs, while having higher mass-specific metabolic rates and faster growth rates. At the cellular level, a clear mechanism underlying whole animal traits has not been fully elucidated, although oxidative stress has been implicated as a potential culprit of the disparate life spans of domestic dogs. We used plasma and red blood cells from known aged domestic dogs and wild canids, and measured several oxidative stress variables: total antioxidant capacity (TAC), lipid damage, and enzymatic activities of catalase, superoxide dismutase, and glutathione peroxidase (GPx). We used phylogenetically informed general linear mixed models and nonphylogenetically corrected linear regression analysis. We found that lipid damage increases with age in domestic dogs, whereas TAC increases with age and TAC and GPx activity increases as a function of age/maximum life span in wild canids, which may partly explain longer potential life spans in wolves. As body mass increases, TAC and GPx activity increase in wild canids, but not domestic dogs, highlighting that artificial selection may have decreased antioxidant capacity in domestic dogs. We found that small-breed dogs have significantly higher circulating lipid damage compared with large-breed dogs, concomitant to their high mass-specific metabolism and higher growth rates, but in opposition to their long life spans. 
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  7. null (Ed.)
    Body mass affects many biological traits, but its impacts on immune defences are fairly unknown. Recent research on mammals found that neutrophil concentrations disproportionately increased (scaled hypermetrically) with body mass, a result not predicted by any existing theory. Although the scaling relationship for mammals might predict how leucocyte concentrations scale with body mass in other vertebrates, vertebrate classes are distinct in many ways that might affect their current and historic interactions with parasites and hence the evolution of their immune systems. Subsequently, here, we asked which existing scaling hypothesis best-predicts relationships between body mass and lymphocyte, eosinophil and heterophil concentrations—the avian functional equivalent of neutrophils—among more than 100 species of birds. We then examined the predictive power of body mass relative to life-history variation, as extensive literature indicates that the timing of key life events has influenced immune system variation among species. Finally, we ask whether avian scaling patterns differ from the patterns we observed in mammals. We found that an intercept-only model best explained lymphocyte and eosinophil concentrations among birds, indicating that the concentrations of these cell types were both independent of body mass. For heterophils, however, body mass explained 31% of the variation in concentrations among species, much more than life-history variation (4%). As with mammalian neutrophils, avian heterophils scaled hypermetrically ( b = 0.19 ± 0.05), but more steeply than mammals (approx. 1.5 ×; 0.11 ± 0.03). As such, we discuss why birds might require more broadly protective cells compared to mammals of the same body size. Overall, body mass appears to have strong influences on the architecture of immune systems. 
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  8. Abstract

    Body size affects many traits, but often in allometric, or disproportionate ways. For example, large avian and mammalian species circulate far more of some immune cells than expected for their size based on simple geometric principles. To date, such hypermetric immune scaling has mostly been described in zoo‐dwelling individuals, so it remains obscure whether immune hyper‐allometries have any natural relevance. Here, we asked whether granulocyte and lymphocyte allometries in wild birds differ from those described in captive species. Our previous allometric studies of avian immune cell concentrations were performed on animals kept for their lifetimes in captivity where conditions are benign and fairly consistent. In natural conditions, infection, stress, nutrition, climate, and myriad other forces could alter immune traits and hence mask any interspecific scaling relationships between immune cells and body size. Counter to this expectation, we found no evidence that immune cell allometries differed between captive and wild species, although we had to rely on cell proportion data, as insufficient concentration data were available for wild species. Our results indicate that even in variable and challenging natural contexts, immune allometries endure and might affect disease ecology and evolution.

     
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