Mammal responses to global changes in human activity vary by trophic group and landscape.

Wildlife must adapt to human presence to survive in the Anthropocene, so it is critical to understand species responses to humans in different contexts. We used camera trapping as a lens to view mammal responses to changes in human activity during the COVID-19 pandemic. Across 163 species sampled in 102 projects around the world, changes in the amount and timing of animal activity varied widely. Under higher human activity, mammals were less active in undeveloped areas but unexpectedly more active in developed areas while exhibiting greater nocturnality. Carnivores were most sensitive, showing the strongest decreases in activity and greatest increases in nocturnality. Wildlife managers must consider how habituation and uneven sensitivity across species may cause fundamental differences in human-wildlife interactions along gradients of human influence.

Stepping stones to extirpation: Puma patch occupancy thresholds in an urban-wildland matrix.

Habitat loss and fragmentation are the leading causes of species range contraction and extirpation, worldwide. Factors that predict sensitivity to fragmentation include high trophic level, large body size, and extensive spatial requirements. Pumas (Puma concolor) exemplify these qualities, making them particularly susceptible to fragmentation and subsequent reductions in demographic connectivity. The chaparral-dominated ecosystems surrounding the greater San Francisco Bay Area encompass over 10,000 km2 of suitable puma habitat, but inland waterways, croplands, urban land uses, and extensive transportation infrastructure have resulted in widespread habitat fragmentation. Pumas in this region now exist as a metapopulation marked by loss of genetic diversity, collisions with vehicles, and extensive human-puma conflict. Given these trends, we conducted a photo survey from 2017 to 2021 across 19 patches of predicted habitat and compiled a dataset of >6584 puma images. We used a logistic regression analytical framework to evaluate the hypothesis that puma patch occupancy would exhibit a threshold response explained by patch size, isolation, and habitat quality. Contrary to predictions, only variables related to patch size demonstrated any power to explain occupancy. On average, occupied patches were 18× larger than those where they were not detected (825 ± 1238 vs. 46 ± 101 km2). Although we observed pumas in patches as small as 1 km2, logistic regression models indicated a threshold occupancy probability between 300 and 400 km2, which is remarkably close to the mean male puma home range size in coastal California (~381 km2). Puma populations dependent on habitats below this value may be susceptible to inbreeding depression and human-wildlife conflict, and therefore vulnerable to extirpation. For species conservation, we suggest conflicts might be ameliorated by identifying the largest, isolated patches for public education campaigns with respect to management of domestic animals, and remaining connective parcels be identified, mapped, and prioritized for targeted mitigation.

EXPLORING THE USE OF THE ERYTHROCYTE SEDIMENTATION RATE AS AN INFLAMMATORY MARKER FOR FREE-RANGING WILDLIFE: A CASE STUDY IN AFRICAN BUFFALO (SYNCERUS CAFFER).

Measuring inflammatory markers is critical to evaluating both recent infection status and overall human and animal health; however, there are relatively few techniques that do not require specialized equipment or personnel for detecting inflammation among wildlife. Such techniques are useful in that they help determine individual and population-level inflammatory status without the infrastructure and reagents that many more-specific assays require. One such technique, known as the erythrocyte sedimentation rate (ESR), is a measure of how quickly erythrocytes (red blood cells) settle in serum, with a faster rate indicating a general, underlying inflammatory process is occurring. The technique is simple, inexpensive, and can be performed in the field without specialized equipment. We took advantage of a population of African buffalo (Syncerus caffer), well studied from June 2014 to May 2017, to understand the utility of ESR in an important wildlife species. When ESR was compared with other markers of immunity in African buffalo, it correlated to known measures of inflammation. We found that a faster ESR was significantly positively correlated with increased total globulin levels and significantly negatively correlated with increased red blood cell count and albumin levels. We then evaluated if ESR correlated to the incidence of five respiratory pathogens and infection with two tick-borne pathogens in African buffalo. Our results suggest that elevated ESR is associated with the incidence of bovine viral diarrhea virus infection, parainfluenza virus, and Mannheimia haemolytica infections as well as concurrent Anaplasma marginale and Anaplasma centrale coinfection. These findings suggest that ESR is a useful field test as an inflammatory marker in individuals and herds, helping us better monitor overall health status in wild populations.

Co-infection best predicts respiratory viral infection in a wild host.

The dynamics of directly transmitted pathogens in natural populations are likely to result from the combined effects of host traits, pathogen biology, and interactions among pathogens within a host. Discovering how these factors work in concert to shape variation in pathogen dynamics in natural host-multi-pathogen systems is fundamental to understanding population health. Here, we describe temporal variation in incidence and then elucidate the effect of hosts trait, season and pathogen co-occurrence on host infection risk using one of the most comprehensive studies of co-infection in a wild population: a suite of seven directly transmitted viral and bacterial respiratory infections from a 4-year study of 200 free-ranging African buffalo Syncerus caffer. Incidence of upper respiratory infections was common throughout the study-five out of the seven pathogens appeared to be consistently circulating throughout our study population. One pathogen exhibited clear outbreak dynamics in our final study year and another was rarely detected. Co-infection was also common in this system: The strongest indicator of pathogen occurrence for respiratory viruses was in fact the presence of other viral respiratory infections. Host traits had minimal effects on odds of pathogen occurrence but did modify pathogen-pathogen associations. In contrast, only season predicted bacterial pathogen occurrence. Though a combination of environmental, behavioural, and physiological factors work together to shape disease dynamics, we found pathogen associations best determined infection risk. Our study demonstrates that, in the absence of very fine-scale data, the intricate changes among these factors are best represented by co-infection.

Immune stability predicts tuberculosis infection risk in a wild mammal.

Immunity is one of the most variable phenotypic traits in animals; however, some individuals may show less fluctuation in immune traits, resulting in stable patterns of immune variation over time. It is currently unknown whether immune variation has consequences for infectious disease risk. In this study, we identified moderately stable immune traits in wild African buffalo and asked whether the stability of these traits affected bovine tuberculosis (TB) infection risk. We found that adaptive immune traits such as the level of interferon-γ (IFN-γ) released after white blood cell stimulation, the number of circulating lymphocytes and the level of antibodies against bovine adenovirus-3 were moderately repeatable (i.e. stable) over time, whereas parameters related to innate immunity either had low repeatability (circulating eosinophil numbers) or were not repeatable (e.g. neutrophil numbers, plasma bacteria killing capacity). Intriguingly, individuals with more repeatable IFN-γ and lymphocyte levels were at a significantly higher risk of acquiring TB infection. In stark contrast, average IFN-γ and lymphocyte levels were poor predictors of TB risk, indicating that immune variability rather than absolute response level better captured variation in disease susceptibility. This work highlights the important and under-appreciated role of immune variability as a predictor of infection risk.

Bovine tuberculosis disturbs parasite functional trait composition in African buffalo.

Novel parasites can have wide-ranging impacts, not only on host populations, but also on the resident parasite community. Historically, impacts of novel parasites have been assessed by examining pairwise interactions between parasite species. However, parasite communities are complex networks of interacting species. Here we used multivariate taxonomic and trait-based approaches to determine how parasite community composition changed when African buffalo (Syncerus caffer) acquired an emerging disease, bovine tuberculosis (BTB). Both taxonomic and functional parasite richness increased significantly in animals that acquired BTB than in those that did not. Thus, the presence of BTB seems to catalyze extraordinary shifts in community composition. There were no differences in overall parasite taxonomic composition between infected and uninfected individuals, however. The trait-based analysis revealed an increase in direct-transmitted, quickly replicating parasites following BTB infection. This study demonstrates that trait-based approaches provide insight into parasite community dynamics in the context of emerging infections.

Introduced and native congeners use different resource allocation strategies to maintain performance during infection.

Abstract 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.

Surveillance for microbes and range expansion in house sparrows.

Interactions between hosts and parasites influence the success of host introductions and range expansions post-introduction. However, the physiological mechanisms mediating these outcomes are little known. In some vertebrates, variation in the regulation of inflammation has been implicated, perhaps because inflammation imparts excessive costs, including high resource demands and collateral damage upon encounter with novel parasites. Here, we tested the hypothesis that variation in the regulation of inflammation contributed to the spread of house sparrows (Passer domesticus) across Kenya, one of the world's most recent invasions of this species. Specifically, we asked whether inflammatory gene expression declines with population age (i.e. distance from Mombasa (dfM), the site of introduction around 1950). We compared expression of two microbe surveillance molecules (Toll-like receptors, TLRs-2 and 4) and a proinflammatory cytokine (interleukin-6, IL-6) before and after an injection of an immunogenic component of Gram-negative bacteria (lipopolysaccharide, LPS) among six sparrow populations. We then used a best-subset model selection approach to determine whether population age (dfM) or other factors (e.g. malaria or coccidian infection, sparrow density or genetic group membership) best-explained gene expression. For baseline expression of TLR-2 and TLR-4, population age tended to be the best predictor with expression decreasing with population age, although other factors were also important. Induced expression of TLRs was affected by LPS treatment alone. For induced IL-6, only LPS treatment reliably predicted expression; baseline expression was not explained by any factor. These data suggest that changes in microbe surveillance, more so than downstream control of inflammation via cytokines, might have been important to the house sparrow invasion of Kenya.

Does immune suppression during stress occur to promote physical performance?

Two adaptationist hypotheses have been proposed to explain why stress, particularly elevation of stress hormones (i.e. glucocorticoids), tends to suppress immune functions. One is that immune suppression represents efforts to minimize autoimmune responses to self-antigens released as organisms cope with stressors (i.e. the autoimmune-avoidance hypothesis). The other is that immune suppression occurs to promote a shunting of resources to life processes more conducive to survival of the stressor (i.e. the re-allocation hypothesis). Here in wild-caught house sparrows (Passer domesticus), we tested the second hypothesis, asking whether sustained elevation of baseline glucocorticoids, due to captivity, caused a greater rate of decline in immune functions than flight performance. A greater decline in immune functions than flight performance would support the re-allocation hypothesis. As in previous studies, we found that captivity tended to alter baseline corticosterone, suggesting that house sparrows experience captivity as a stressor. Captivity also affected several constitutive and induced innate immune metrics: bacterial (Escherichia coli) killing activity of blood and oxidative burst of leukocytes both changed in a manner consistent with immune disregulation. In contrast, breast muscle size and vertical flight (hovering) duration improved over captivity. Collectively, these changes provide indirect support for the re-allocation hypothesis, although within individuals, changes in immune and physical performance were unrelated.

Epigenetic Variation May Compensate for Decreased Genetic Variation with Introductions: A Case Study Using House Sparrows (Passer domesticus) on Two Continents.

Epigenetic mechanisms impact several phenotypic traits and may be important for ecology and evolution. The introduced house sparrow (Passer domesticus) exhibits extensive phenotypic variation among and within populations. We screened methylation in populations from Kenya and Florida to determine if methylation varied among populations, varied with introduction history (Kenyan invasion <50 years old, Florida invasion ~150 years old), and could potentially compensate for decrease genetic variation with introductions. While recent literature has speculated on the importance of epigenetic effects for biological invasions, this is the first such study among wild vertebrates. Methylation was more frequent in Nairobi, and outlier loci suggest that populations may be differentiated. Methylation diversity was similar between populations, in spite of known lower genetic diversity in Nairobi, which suggests that epigenetic variation may compensate for decreased genetic diversity as a source of phenotypic variation during introduction. Our results suggest that methylation differences may be common among house sparrows, but research is needed to discern whether methylation impacts phenotypic variation.

The effect of exogenous corticosterone on West Nile virus infection in Northern Cardinals (Cardinalis cardinalis).

The relationship between stress and disease is thought to be unambiguous: chronic stress induces immunosuppression, which likely increases the risk of infection. However, this link has not been firmly established in wild animals, particularly whether stress hormones affect host responses to zoonotic pathogens, which can be transmitted to domesticated animal, wildlife and human populations. Due to the dynamic effects of stress hormones on immune functions, stress hormones may make hosts better or poorer amplifying hosts for a pathogen contingent on context and the host species evaluated. Using an important zoonotic pathogen, West Nile virus (WNV) and a competent host, the Northern Cardinal (Cardinalis cardinalis), we tested the effects of exogenous corticosterone on response to WNV infection. Corticosterone was administered at levels that individuals enduring chronic stressors (i.e., long-term inclement weather, food shortage, anthropogenic pollution) might experience in the wild. Corticosterone greatly impacted mortality: half of the corticosterone-implanted cardinals died between five - 11 days post-inoculation whereas only one of nine empty-implanted (control) birds died. No differences were found in viral titer between corticosterone- and empty-implanted birds. However, cardinals that survived infections had significantly higher average body temperatures during peak infection than individuals that died. In sum, this study indicates that elevated corticosterone could affect the survival of WNV-infected wild birds, suggesting that populations may be disproportionately at-risk to disease in stressful environments.

Captivity induces hyper-inflammation in the house sparrow (Passer domesticus).

Some species thrive in captivity but others exhibit extensive psychological and physiological deficits, which can be a challenge to animal husbandry and conservation as well as wild immunology. Here, we investigated whether captivity duration impacted the regulation of a key innate immune response, inflammation, of a common wild bird species, the house sparrow (Passer domesticus). Inflammation is one of the most commonly induced and fast-acting immune responses animals mount upon exposure to a parasite. However, attenuation and resolution of inflammatory responses are partly coordinated by glucocorticoid hormones, hormones that can be disregulated in captivity. Here, we tested whether captivity duration alters corticosterone regulation and hence the inflammatory response by comparing the following responses to lipopolysaccharide (LPS; a Gram-negative bacteria component that induces inflammation) of birds caught wild and injected immediately versus those held for 2 or 4 weeks in standard conditions: (1) the magnitude of leukocyte immune gene expression [the cytokines, interleukin 1ß and interleukin 6, and Toll-like receptor 4 (TLR4)], (2) the rate of clearance of endotoxin, and (3) the release of corticosterone (CORT) in response to endotoxin (LPS). We predicted that captivity duration would increase baseline CORT and thus suppress gene expression and endotoxin clearance rate. However, our predictions were not supported: TLR4 expression increased with time in captivity irrespective of LPS, and cytokine expression to LPS was stronger the longer birds remained captive. Baseline CORT was not affected by captivity duration, but CORT release post-LPS occurred only in wild birds. Lastly, sparrows held captive for 4 weeks maintained significantly higher levels of circulating endotoxin than other groups, perhaps due to leakage of microbes from the gut, but exogenous LPS did not increase circulating levels over the time scale samples were collected. Altogether, captivity appears to have induced a hyper-inflammatory state in house sparrows, perhaps due to disregulation of glucocorticoids, natural microflora or both.

Acute-phase responses vary with pathogen identity in house sparrows (Passer domesticus).

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.