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Kendra Phelps

EcoHealth Alliance, Science, Senior Scientist

Texas Tech University, Biological Sciences, Employee

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My interests lie at the nexus of conservation biology, disturbance ecology, ecophysiology, and wildlife-human interactions. My research focuses on the role of human disturbance in shaping mammalian communities, ranging from assemblage composition and population demographics to individual health. I have a keen interest in applying principles of disease ecology to understand how human disturbance can promote vulnerability to pathogen transmission between hosts and potential spillover events into other wildlife, livestock, and humans. My long-term goal is to understand how human manipulation of the environment can have detrimental effects on wildlife health and the prevalence and dynamics of zoonotic diseases in wildlife species.
Supervisors: Dr. Tigga Kingston, Dr. Karen McBee, and Dr. Troy Best

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Julian D Reynolds

Trinity College Dublin

Binghamton University

Duke University

Kansas State University

University of East London

Armando Marques-Guedes

UNL - New University of Lisbon

University of New England - Australia

Swansea University

The University of Queensland, Australia

Elizabeth Jeffers

University of Oxford

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Papers by Kendra Phelps

Figure 3 from: Van der Jeucht L, Groom Q, Agosti D, Phelps K, Reeder DM, Simmons NB (2021) Using iNaturalist to monitor adherence to best practices in bat handling. Biodiversity Data Journal 9: e68052. https://doi.org/10.3897/BDJ.9.e68052

Figure 2 from: Van der Jeucht L, Groom Q, Agosti D, Phelps K, Reeder DM, Simmons NB (2021) Using iNaturalist to monitor adherence to best practices in bat handling. Biodiversity Data Journal 9: e68052. https://doi.org/10.3897/BDJ.9.e68052

Figure 1 from: Van der Jeucht L, Groom Q, Agosti D, Phelps K, Reeder DM, Simmons NB (2021) Using iNaturalist to monitor adherence to best practices in bat handling. Biodiversity Data Journal 9: e68052. https://doi.org/10.3897/BDJ.9.e68052

Using iNaturalist to monitor adherence to best practices in bat handling

Biodiversity Data Journal

A strategy to assess spillover risk of bat SARS-related coronaviruses in Southeast Asia

Emerging diseases caused by coronaviruses of likely bat origin (e.g. SARS, MERS, SADS and COVID-1... more Emerging diseases caused by coronaviruses of likely bat origin (e.g. SARS, MERS, SADS and COVID-19) have disrupted global health and economies for two decades. Evidence suggests that some bat SARS-related coronaviruses (SARSr-CoVs) could infect people directly, and that their spillover is more frequent than previously recognized. Each zoonotic spillover of a novel virus represents an opportunity for evolutionary adaptation and further spread; therefore, quantifying the extent of this "hidden" spillover may help target prevention programs. We derive biologically realistic range distributions for known bat SARSr-CoV hosts and quantify their overlap with human populations. We then use probabilistic risk assessment and data on human-bat contact, human SARSr-CoV seroprevalence, and antibody duration to estimate that ~400,000 people (median: ~50,000) are infected with SARSr-CoVs annually in South and Southeast Asia. These data on the geography and scale of spillover can be used ...

Ecological Characteristics of Small Mammal Communities at a Superfund Site

The American Midland Naturalist, 2009

Preserve a Voucher Specimen! The Critical Need for Integrating Natural History Collections in Infectious Disease Studies

mBio

Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definit... more Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definitive animal host for SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), the causal agent of COVID-19, remains unknown. Unfortunately, similar problems exist for other betacoronaviruses, and no vouchered specimens exist to corroborate host species identification for most of these pathogens. This most basic information is critical to the full understanding and mitigation of emerging zoonotic diseases. To overcome this hurdle, we recommend that host-pathogen researchers adopt vouchering practices and collaborate with natural history collections to permanently archive microbiological samples and host specimens. Vouchered specimens and associated samples provide both repeatability and extension to host-pathogen studies, and using them mobilizes a large workforce (i.e., biodiversity scientists) to assist in pandemic preparedness. We review several well-known examples that successfull...

Preserve a Voucher Specimen! The Critical Need for Integrating Natural History Collections in Infectious Disease Studies Downloaded from

mBio, 2021

Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definit... more Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definitive animal host for SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), the causal agent of COVID-19, remains unknown. Unfortunately, similar problems exist for other betacoronaviruses, and no vouchered specimens exist to corroborate host species identification for most of these pathogens. This most basic information is critical to the full understanding and mitigation of emerging zoonotic diseases. To overcome this hurdle, we recommend that host-pathogen researchers adopt vouchering practices and collaborate with natural history collections to permanently archive microbiological samples and host specimens. Vouchered specimens and associated samples provide both repeatability and extension to host-pathogen studies, and using them mobilizes a large workforce (i.e., biodiversity scientists) to assist in pandemic preparedness. We review several well-known examples that successfully integrate host-pathogen research with natural history collections (e.g., yellow fever, hantaviruses, helminths). However, vouchering remains an underutilized practice in such studies. Using an online survey, we assessed vouchering practices used by microbiologists (e.g., bacteriologists, parasitologists, virologists) in host-pathogen research. A much greater number of respondents permanently archive microbiological samples than archive host specimens, and less than half of respondents voucher host specimens from which microbiological samples were lethally collected. To foster collaborations between microbiologists and natural history collections, we provide recommendations for integrating vouchering techniques and archiving of microbiological samples into host-pathogen studies. This integrative approach exemplifies the premise underlying One Health initiatives, providing critical infrastructure for

Possibility for reverse zoonotic transmission of SARS-CoV-2 to free-ranging wildlife: A case study of bats

PLoS Pathogens, 2020

The COVID-19 pandemic highlights the substantial public health, economic, and societal consequenc... more The COVID-19 pandemic highlights the substantial public health, economic, and societal consequences of virus spillover from a wildlife reservoir. Widespread human transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) also presents a new set of challenges when considering viral spillover from people to naïve wildlife and other animal populations. The establishment of new wildlife reservoirs for SARS-CoV-2 would further complicate public health control measures and could lead to wildlife health and conservation impacts. Given the likely bat origin of SARS-CoV-2 and related beta-coronaviruses (β-CoVs), free-ranging bats are a key group of concern for spillover from humans back to PLOS PATHOGENS PLOS Pathogens | https://doi.org/10.1371/journal.ppat.

Temporal patterns of bat activity on the High Plains of Texas

by Julie Parlos, Lizette Siles, and Kendra Phelps

From field to laboratory: a memorial volume in honor of Robert J. Baker (R. D. Bradley, H. H. Genoways, D. J. Schmidly, and L. C. Bradley, eds.), Oct 11, 2019

Texas is home to more wind turbines and more bat species than any other state in the United State... more Texas is home to more wind turbines and more bat species than any other state in the United States. Insectivorous bats provide an important economical ecosystem service in this region through agricultural pest regulation. Unfortunately, bats can be impacted negatively by wind turbines, and migratory bat species particularly so. To understand how bat activity changes throughout the year in western Texas, activity was monitored through echolocation calls and opportunistic mist-netting efforts over a period of four years (2012–2015). Peaks in activity were observed from March through April, and again in September, which coincides with previously documented migratory
periods for many species native to the High Plains of Texas. Findings presented herein suggest that urban habitats are preferred stopover sites for migratory bat species while traversing arid regions such as those occurring in western Texas. In addition to human-made structures, urban habitats harbor non-native trees that provide suitable roost sites, aggregations of insect prey swarming outdoor light sources, and artificial water sources. It is important to understand bat activity in western Texas, not only for the benefit of agricultural pest suppression, but also to predict how the expansion of wind energy may affect bat populations in this region.

Poriferan abundance is negatively associated with coral health in the Mesoamerican Reef

Texas Journal of Science , 2018

The Mesoamerican Reef is the second largest coral reef in the world and has experienced a 50% los... more The Mesoamerican Reef is the second largest coral reef in the world and has experienced a 50% loss of coral coverage in recent decades. Due to the high biodiversity of marine life that depend on the Mesoamerican Reef, identifying drivers of coral loss is crucial. This study was designed to assess the relationship between the presence of yellow band disease (YBD) and white plague type-II (WPII) on stony corals with environmental (water depth) and biological stressors (abundance of sponges in close proximity) in the reef surrounding the Bay Islands, Honduras. Both radial and parallel transect survey techniques were used to quantify the abundance of seven sponge species within a one-meter radius of Orbicella species and Montastraea cavernsoa. The strongest predictor of coral health was the abundance of Callyspongia plicifera, followed by Svenzea zeai, in close proximity to diseased coral. A weak, but positive, correlation between poriferan abundance and the presence of disease lesions on coral was observed. However, no significant relationship of disease prevalence with water depth was observed. Additionally, no differences in the prevalence of disease lesions between four species of native stony corals were observed. These findings suggest coral species are equally susceptible to bacterial pathogens, but that close association with poriferans may increase the transmission and persistence of harmful bacteria in coral reef ecosystems. _________________________ The Mesoamerican Reef is the second largest coral reef in the world, extending from the northern tip of the Yucatan Peninsula to the Honduran Bay Islands, and is only second in size to the Great Barrier Reef of Australia (Gerholdt 2016). However, in recent decades, the abundance and distribution of coral reefs has been shrinking rapidly across the globe; Great Barrier Reef coral coverage has declined by 50% from 1985 to 2012 (Sweatman 2017), and an 80% loss of coral reef structures has been detected in the Mesoamerican Reef over the last 20 years (AIMS 2017). Multiple stressors have been implicated in these declines. Rising ocean temperatures, ocean acidification,

Bat Research Networks and Viral Surveillance: Gaps and Opportunities in Western Asia

by Kendra Phelps and Nisreen Alhmoud

Viruses, 2019

Bat research networks and viral surveillance are assumed to be at odds due to seemingly conflicti... more Bat research networks and viral surveillance are assumed to be at odds due to seemingly conflicting research priorities. Yet human threats that contribute to declines in bat populations globally also lead to increased transmission and spread of bat-associated viruses, which may pose a threat to global health and food security. In this review, we discuss the importance of and opportunities for multidisciplinary collaborations between bat research networks and infectious disease experts to tackle shared threats that jeopardize bat conservation as well as human and animal health. Moreover, we assess research effort on bats and bat-associated viruses globally, and demonstrate that Western Asia has limited published research and represents a gap for coordinated bat research. The lack of bat research in Western Asia severely limits our capacity to identify and mitigate region-specific threats to bat populations and detect interactions between bats and incidental hosts that promote virus spillover. We detail a regional initiative to establish the first bat research network in Western Asia (i.e., the Western Asia Bat Research Network, WAB-Net), with the aim of integrating ecological research on bats with virus surveillance to find "win-win" solutions that promote bat conservation and safeguard public and animal health across the region.

Assemblage and Species Threshold Responses to Environmental and Disturbance Gradients Shape Bat Diversity in Disturbed Cave Landscapes

Ecological thresholds represent a critical tipping point along an environmental gradient that, on... more Ecological thresholds represent a critical tipping point along an environmental gradient that, once breached, can have irreversible consequences for species persistence and assemblage structure. Thresholds can also be used to identify species with the greatest sensitivity to environmental changes. Bats are keystone species yet are under pressure from human disturbances, specifically landscape and cave disturbances (i.e., reduced forest cover, urbanization, hunting, tourism). We compared bat assemblages across environmental and disturbance gradients measured at 56 caves in the Philippines to identify species-specific thresholds and assess congruence among species responses. All species exhibited significant responses to one or more gradients, with 84% responding to more than one gradient. Yet mixed responses of sensitivity to some gradients but tolerance to others hindered identification of assemblage thresholds to all gradients except landscape disturbance. However, we identified credible indicator species that exhibit distinct thresholds to specific gradients and tested for differences in ecological and morphological traits between species groups with shared responses (i.e., negative or positive). Few traits were useful for discriminating the direction of a species response, with some exceptions. Species that responded positively to increased landscape disturbance and hunting had greater body mass, whereas species that responded negatively to mining emitted higher peak call frequencies.

Environmental and biological context modulates the physiological stress response of bats to human disturbance

by Kendra Phelps and Tigga Kingston

Environmental and biological context play significant roles in modulating physiological stress re... more Environmental and biological context play significant roles in modulating physiological stress responses of individuals in wildlife populations yet are often overlooked when evaluating consequences of human disturbance on individual health and fitness. Furthermore, most studies gauge individual stress responses based on a single physiological biomarker, typically circulating glucocorticoid concentrations, which limits interpretation of the complex, multifaceted responses of individuals to stressors. We selected four physiological biomarkers to capture short-term and prolonged stress responses in a widespread cave-roosting bat, Hipposideros diadema, across multiple gradients of human disturbance in and around caves in the Philippines. We used conditional inference trees and random forest analysis to determine the role of environmental quality (cave complexity, available roosting area), assemblage composition (intra- and interspecific associations and species richness), and intrinsic characteristics of individuals (sex and reproductive status) in modulating responses to disturbance. Direct cave disturbance (hunting pressure and human visitation) was the primary driver of neutrophil-to-lymphocyte ratios, with lower ratios associated with increased disturbance, while context-specific factors were more important in explaining total leukocyte count, body condition, and ectoparasite load. Moreover, conditional inference trees revealed complex interactions among human disturbance and modulating factors. Cave complexity often ameliorated individual responses to human disturbance, whereas conspecific abundance often compounded responses. Our study demonstrates the importance of an integrated approach that incorporates environmental and biological context when identifying drivers of physiological responses, and that assesses responses to gradients of direct and indirect disturbance using multiple complementary biomarkers.

A Comparative Analysis of Viral Richness and Viral Sharing in Cave-Roosting Bats

by Luis F. Aguirre and Kendra Phelps

Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or des... more Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or destroyed by human activities such as tourism and extractive industries. In addition to degrading the habitats of cave-roosting bats, such activities often promote contact between humans and bats, which may have potential impacts on human health. Cave-roosting bats are hosts to diverse viruses, some of which emerged in humans with severe consequences (e.g., severe acute respiratory syndrome coronavirus and Marburg virus). Characterizing patterns of viral richness and sharing among bat species are therefore important first steps for understanding bat-virus dynamics and mitigating future bat-human spillover. Here we compile a database of bat-virus associations and bat species ecological traits, and investigate the importance of roosting behavior as a determinant of viral richness and viral sharing among bat species. We show that cave-roosting species do not host greater viral richness, when accounting for publication bias, diet, body mass, and geographic range size. Our global analyses, however, show that cave-roosting bats do exhibit a greater likelihood of viral sharing, especially those documented in the literature as co-roosting in the same cave. We highlight the importance of caves as critical foci for bat conservation, as well as ideal sites for longitudinal surveillance of bat-virus dynamics.

A Comparative Analysis of Viral Richness and Viral Sharing in Cave-Roosting Bats

by Kendra Phelps, Anna Willoughby, and PREDICT Consortium

Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or des... more Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or destroyed by human activities such as tourism and extractive industries. In addition to degrading the habitats of cave-roosting bats, such activities often promote contact between humans and bats, which may have potential impacts on human health. Cave-roosting bats are hosts to diverse viruses, some of which emerged in humans with severe consequences (e.g., severe acute respiratory syndrome coronavirus and Marburg virus). Characterizing patterns of viral richness and sharing among bat species are therefore important first steps for understanding bat-virus dynamics and mitigating future bat-human spillover. Here we compile a database of bat-virus associations and bat species ecological traits, and investigate the importance of roosting behavior as a determinant of viral richness and viral sharing among bat species. We show that cave-roosting species do not host greater viral richness, when accounting for publication bias, diet, body mass, and geographic range size. Our global analyses, however, show that cave-roosting bats do exhibit a greater likelihood of viral sharing, especially those documented in the literature as co-roosting in the same cave. We highlight the importance of caves as critical foci for bat conservation, as well as ideal sites for longitudinal surveillance of bat-virus dynamics.

Correlates of cave-roosting bat diversity as an effective tool to identify priority caves

by Kendra Phelps and Tigga Kingston

Cave ecosystems are subterranean biodiversity hotspots, but limited knowledge of the distribution... more Cave ecosystems are subterranean biodiversity hotspots, but limited knowledge of the distribution of diversity among caves hampers their conservation. Surveys of surrogate taxa (e.g., keystone species) can identify hotspots of biodiversity when knowledge about an ecosystem is lacking. Bats are keystone species in cave ecosystems because their guano is the primary energy source supporting diverse assemblages of cave-dependent wildlife. However , directly measuring bat diversity is time-consuming and requires expert knowledge; instead, we suggest the use of correlates of bat diversity that can be derived from readily accessible data (e.g., land-use maps) and straightforward methods not requiring expert knowledge (e.g., cave surveys, interviews) as a foundation for prioritizing caves. To identify easily measurable correlates of bat diversity, we compared assemblage composition and species abundances of 21 bat species captured in 56 caves on Bohol Island, Philippines, along gradients in environmental factors and human disturbance. Model-and distance-based methods indicated that surface-level disturbance (i.e., percent non-forested habitat, degree of urbanization and road development) along with cave complexity (i.e., available roosting area, structural heterogeneity, number of entrances and temperature range) were the most influential factors governing cave-roosting bat assemblages, thus representing correlates of bat diversity. Prioritization schemes based on these correlates select combinations of caves with greater species richness than both random selection and selection of caves based on observed richness from intensive bat surveys. The use of easy-to-measure environmental and disturbance correlates of bat diversity is an effective tool to prioritize caves to protect cave-roosting bats and the cave-dependent wildlife they support.

Bats and Buildings: The Conservation of Synanthropic Bats

Humans have shared buildings with bats for thousands of years, probably as early as first humans ... more Humans have shared buildings with bats for thousands of years, probably as early as first humans built primitive huts. Indeed, many bat species can be defined as synanthropic, i.e., they have a strong ecological association with humans. Bats have been observed using buildings as roosting and foraging sites, temporary shelters, for reproduction and hibernation. A synanthropic lifestyle may result in direct fitness benefits owing to energetic advantages in warmer roosts, which may ultimately lead to more rapid gestation and faster development of juveniles, or by being less exposed to natural predators in urban environments. All these benefits may allow bats to use buildings as stepping stones to exploit habitats
otherwise devoid of roosting structures and may even lead to the expansion of geographic ranges. Yet, the coexistence with humans also comes with some risks. Bats may be exposed to chemical pollutants, particularly preservation chemicals
used on lumber or during pest control measures. Bats may also be at risk of direct persecution or they may die accidently if trapped within buildings. In general, eviction of bats from buildings should follow the general rule of avoidance–mitigation–compensation. When considering conservation measures for synanthropic bats, it is most important to assess the role of the building for different life stages of bats. Construction work at buildings should be conducted in a manner that minimizes disturbance of bats. Artificial roosts can replace lost roosts, yet bats will often not accept alternative roosts. Demographic changes in human populations
may lead to the abandonment of buildings, for example, in rural areas and to increased conflicts in urban areas when old buildings are replaced by new buildings or when previously unoccupied space in buildings is renovated. We advocate
maintenance and enhancement of roosts for synanthropic bats, in addition to outreach and education campaigns, to improve the tolerance of humans for synanthropic bats.

Ecological Characteristics of Small Mammal Communities Inhabiting Tar Creek Superfund Site, Oklahoma

ECOLOGICAL CHARACTERISTICS OF SMALL MAMMAL COMMUNITIES INHABITING TAR CREEK SUPERFUND SITE, OKLAH... more

Population Parameters of Peromyscus leucopus (White-footed Mice) Inhabiting a Heavy Metal Contaminated Superfund Site

We used standard mark-recapture techniques to investigate ecological characteristics of Peromyscu... more We used standard mark-recapture techniques to investigate ecological characteristics of Peromyscus leucopus (white-footed mouse) populations inhabiting two locations within a heavy metal contaminated site, Tar Creek Superfund Site, and reference sites, Lake Carl Blackwell and Oologah Wildlife Management Area, located in northeastern Oklahoma. Basic demographic parameters such as population size, survival rate, recapture rate, mean minimum longevity, number of reproductively active females, reproductive success, and incidence of botfly (Cuterebra fontinella) infestation were not significantly different between contaminated and reference sites. However, adult, non-reproductive P. leucopus inhabiting contaminated sites had, on average, a larger body mass than those from reference sites. Other indicators of overall individual health, dental condition and prevalence of botfly infestations, were significantly different among populations. Instances of extensive mottling of the upper and lower incisors, a reliable indicator of exposure to heavy metal contamination, were only noted in individuals inhabiting contaminated sites. Unfortunately, no direct link between site contamination and alterations to some population parameters could be established.

Figure 3 from: Van der Jeucht L, Groom Q, Agosti D, Phelps K, Reeder DM, Simmons NB (2021) Using iNaturalist to monitor adherence to best practices in bat handling. Biodiversity Data Journal 9: e68052. https://doi.org/10.3897/BDJ.9.e68052

Figure 2 from: Van der Jeucht L, Groom Q, Agosti D, Phelps K, Reeder DM, Simmons NB (2021) Using iNaturalist to monitor adherence to best practices in bat handling. Biodiversity Data Journal 9: e68052. https://doi.org/10.3897/BDJ.9.e68052

Figure 1 from: Van der Jeucht L, Groom Q, Agosti D, Phelps K, Reeder DM, Simmons NB (2021) Using iNaturalist to monitor adherence to best practices in bat handling. Biodiversity Data Journal 9: e68052. https://doi.org/10.3897/BDJ.9.e68052

Using iNaturalist to monitor adherence to best practices in bat handling

Biodiversity Data Journal

A strategy to assess spillover risk of bat SARS-related coronaviruses in Southeast Asia

Emerging diseases caused by coronaviruses of likely bat origin (e.g. SARS, MERS, SADS and COVID-1... more Emerging diseases caused by coronaviruses of likely bat origin (e.g. SARS, MERS, SADS and COVID-19) have disrupted global health and economies for two decades. Evidence suggests that some bat SARS-related coronaviruses (SARSr-CoVs) could infect people directly, and that their spillover is more frequent than previously recognized. Each zoonotic spillover of a novel virus represents an opportunity for evolutionary adaptation and further spread; therefore, quantifying the extent of this "hidden" spillover may help target prevention programs. We derive biologically realistic range distributions for known bat SARSr-CoV hosts and quantify their overlap with human populations. We then use probabilistic risk assessment and data on human-bat contact, human SARSr-CoV seroprevalence, and antibody duration to estimate that ~400,000 people (median: ~50,000) are infected with SARSr-CoVs annually in South and Southeast Asia. These data on the geography and scale of spillover can be used ...

Ecological Characteristics of Small Mammal Communities at a Superfund Site

The American Midland Naturalist, 2009

Preserve a Voucher Specimen! The Critical Need for Integrating Natural History Collections in Infectious Disease Studies

mBio

Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definit... more Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definitive animal host for SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), the causal agent of COVID-19, remains unknown. Unfortunately, similar problems exist for other betacoronaviruses, and no vouchered specimens exist to corroborate host species identification for most of these pathogens. This most basic information is critical to the full understanding and mitigation of emerging zoonotic diseases. To overcome this hurdle, we recommend that host-pathogen researchers adopt vouchering practices and collaborate with natural history collections to permanently archive microbiological samples and host specimens. Vouchered specimens and associated samples provide both repeatability and extension to host-pathogen studies, and using them mobilizes a large workforce (i.e., biodiversity scientists) to assist in pandemic preparedness. We review several well-known examples that successfull...

Preserve a Voucher Specimen! The Critical Need for Integrating Natural History Collections in Infectious Disease Studies Downloaded from

mBio, 2021

Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definit... more Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definitive animal host for SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), the causal agent of COVID-19, remains unknown. Unfortunately, similar problems exist for other betacoronaviruses, and no vouchered specimens exist to corroborate host species identification for most of these pathogens. This most basic information is critical to the full understanding and mitigation of emerging zoonotic diseases. To overcome this hurdle, we recommend that host-pathogen researchers adopt vouchering practices and collaborate with natural history collections to permanently archive microbiological samples and host specimens. Vouchered specimens and associated samples provide both repeatability and extension to host-pathogen studies, and using them mobilizes a large workforce (i.e., biodiversity scientists) to assist in pandemic preparedness. We review several well-known examples that successfully integrate host-pathogen research with natural history collections (e.g., yellow fever, hantaviruses, helminths). However, vouchering remains an underutilized practice in such studies. Using an online survey, we assessed vouchering practices used by microbiologists (e.g., bacteriologists, parasitologists, virologists) in host-pathogen research. A much greater number of respondents permanently archive microbiological samples than archive host specimens, and less than half of respondents voucher host specimens from which microbiological samples were lethally collected. To foster collaborations between microbiologists and natural history collections, we provide recommendations for integrating vouchering techniques and archiving of microbiological samples into host-pathogen studies. This integrative approach exemplifies the premise underlying One Health initiatives, providing critical infrastructure for

Possibility for reverse zoonotic transmission of SARS-CoV-2 to free-ranging wildlife: A case study of bats

PLoS Pathogens, 2020

The COVID-19 pandemic highlights the substantial public health, economic, and societal consequenc... more The COVID-19 pandemic highlights the substantial public health, economic, and societal consequences of virus spillover from a wildlife reservoir. Widespread human transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) also presents a new set of challenges when considering viral spillover from people to naïve wildlife and other animal populations. The establishment of new wildlife reservoirs for SARS-CoV-2 would further complicate public health control measures and could lead to wildlife health and conservation impacts. Given the likely bat origin of SARS-CoV-2 and related beta-coronaviruses (β-CoVs), free-ranging bats are a key group of concern for spillover from humans back to PLOS PATHOGENS PLOS Pathogens | https://doi.org/10.1371/journal.ppat.

Temporal patterns of bat activity on the High Plains of Texas

by Julie Parlos, Lizette Siles, and Kendra Phelps

From field to laboratory: a memorial volume in honor of Robert J. Baker (R. D. Bradley, H. H. Genoways, D. J. Schmidly, and L. C. Bradley, eds.), Oct 11, 2019

Texas is home to more wind turbines and more bat species than any other state in the United State... more Texas is home to more wind turbines and more bat species than any other state in the United States. Insectivorous bats provide an important economical ecosystem service in this region through agricultural pest regulation. Unfortunately, bats can be impacted negatively by wind turbines, and migratory bat species particularly so. To understand how bat activity changes throughout the year in western Texas, activity was monitored through echolocation calls and opportunistic mist-netting efforts over a period of four years (2012–2015). Peaks in activity were observed from March through April, and again in September, which coincides with previously documented migratory
periods for many species native to the High Plains of Texas. Findings presented herein suggest that urban habitats are preferred stopover sites for migratory bat species while traversing arid regions such as those occurring in western Texas. In addition to human-made structures, urban habitats harbor non-native trees that provide suitable roost sites, aggregations of insect prey swarming outdoor light sources, and artificial water sources. It is important to understand bat activity in western Texas, not only for the benefit of agricultural pest suppression, but also to predict how the expansion of wind energy may affect bat populations in this region.

Poriferan abundance is negatively associated with coral health in the Mesoamerican Reef

Texas Journal of Science , 2018

The Mesoamerican Reef is the second largest coral reef in the world and has experienced a 50% los... more The Mesoamerican Reef is the second largest coral reef in the world and has experienced a 50% loss of coral coverage in recent decades. Due to the high biodiversity of marine life that depend on the Mesoamerican Reef, identifying drivers of coral loss is crucial. This study was designed to assess the relationship between the presence of yellow band disease (YBD) and white plague type-II (WPII) on stony corals with environmental (water depth) and biological stressors (abundance of sponges in close proximity) in the reef surrounding the Bay Islands, Honduras. Both radial and parallel transect survey techniques were used to quantify the abundance of seven sponge species within a one-meter radius of Orbicella species and Montastraea cavernsoa. The strongest predictor of coral health was the abundance of Callyspongia plicifera, followed by Svenzea zeai, in close proximity to diseased coral. A weak, but positive, correlation between poriferan abundance and the presence of disease lesions on coral was observed. However, no significant relationship of disease prevalence with water depth was observed. Additionally, no differences in the prevalence of disease lesions between four species of native stony corals were observed. These findings suggest coral species are equally susceptible to bacterial pathogens, but that close association with poriferans may increase the transmission and persistence of harmful bacteria in coral reef ecosystems. _________________________ The Mesoamerican Reef is the second largest coral reef in the world, extending from the northern tip of the Yucatan Peninsula to the Honduran Bay Islands, and is only second in size to the Great Barrier Reef of Australia (Gerholdt 2016). However, in recent decades, the abundance and distribution of coral reefs has been shrinking rapidly across the globe; Great Barrier Reef coral coverage has declined by 50% from 1985 to 2012 (Sweatman 2017), and an 80% loss of coral reef structures has been detected in the Mesoamerican Reef over the last 20 years (AIMS 2017). Multiple stressors have been implicated in these declines. Rising ocean temperatures, ocean acidification,

Bat Research Networks and Viral Surveillance: Gaps and Opportunities in Western Asia

by Kendra Phelps and Nisreen Alhmoud

Viruses, 2019

Bat research networks and viral surveillance are assumed to be at odds due to seemingly conflicti... more Bat research networks and viral surveillance are assumed to be at odds due to seemingly conflicting research priorities. Yet human threats that contribute to declines in bat populations globally also lead to increased transmission and spread of bat-associated viruses, which may pose a threat to global health and food security. In this review, we discuss the importance of and opportunities for multidisciplinary collaborations between bat research networks and infectious disease experts to tackle shared threats that jeopardize bat conservation as well as human and animal health. Moreover, we assess research effort on bats and bat-associated viruses globally, and demonstrate that Western Asia has limited published research and represents a gap for coordinated bat research. The lack of bat research in Western Asia severely limits our capacity to identify and mitigate region-specific threats to bat populations and detect interactions between bats and incidental hosts that promote virus spillover. We detail a regional initiative to establish the first bat research network in Western Asia (i.e., the Western Asia Bat Research Network, WAB-Net), with the aim of integrating ecological research on bats with virus surveillance to find "win-win" solutions that promote bat conservation and safeguard public and animal health across the region.

Assemblage and Species Threshold Responses to Environmental and Disturbance Gradients Shape Bat Diversity in Disturbed Cave Landscapes

Ecological thresholds represent a critical tipping point along an environmental gradient that, on... more Ecological thresholds represent a critical tipping point along an environmental gradient that, once breached, can have irreversible consequences for species persistence and assemblage structure. Thresholds can also be used to identify species with the greatest sensitivity to environmental changes. Bats are keystone species yet are under pressure from human disturbances, specifically landscape and cave disturbances (i.e., reduced forest cover, urbanization, hunting, tourism). We compared bat assemblages across environmental and disturbance gradients measured at 56 caves in the Philippines to identify species-specific thresholds and assess congruence among species responses. All species exhibited significant responses to one or more gradients, with 84% responding to more than one gradient. Yet mixed responses of sensitivity to some gradients but tolerance to others hindered identification of assemblage thresholds to all gradients except landscape disturbance. However, we identified credible indicator species that exhibit distinct thresholds to specific gradients and tested for differences in ecological and morphological traits between species groups with shared responses (i.e., negative or positive). Few traits were useful for discriminating the direction of a species response, with some exceptions. Species that responded positively to increased landscape disturbance and hunting had greater body mass, whereas species that responded negatively to mining emitted higher peak call frequencies.

Environmental and biological context modulates the physiological stress response of bats to human disturbance

by Kendra Phelps and Tigga Kingston

Environmental and biological context play significant roles in modulating physiological stress re... more Environmental and biological context play significant roles in modulating physiological stress responses of individuals in wildlife populations yet are often overlooked when evaluating consequences of human disturbance on individual health and fitness. Furthermore, most studies gauge individual stress responses based on a single physiological biomarker, typically circulating glucocorticoid concentrations, which limits interpretation of the complex, multifaceted responses of individuals to stressors. We selected four physiological biomarkers to capture short-term and prolonged stress responses in a widespread cave-roosting bat, Hipposideros diadema, across multiple gradients of human disturbance in and around caves in the Philippines. We used conditional inference trees and random forest analysis to determine the role of environmental quality (cave complexity, available roosting area), assemblage composition (intra- and interspecific associations and species richness), and intrinsic characteristics of individuals (sex and reproductive status) in modulating responses to disturbance. Direct cave disturbance (hunting pressure and human visitation) was the primary driver of neutrophil-to-lymphocyte ratios, with lower ratios associated with increased disturbance, while context-specific factors were more important in explaining total leukocyte count, body condition, and ectoparasite load. Moreover, conditional inference trees revealed complex interactions among human disturbance and modulating factors. Cave complexity often ameliorated individual responses to human disturbance, whereas conspecific abundance often compounded responses. Our study demonstrates the importance of an integrated approach that incorporates environmental and biological context when identifying drivers of physiological responses, and that assesses responses to gradients of direct and indirect disturbance using multiple complementary biomarkers.

A Comparative Analysis of Viral Richness and Viral Sharing in Cave-Roosting Bats

by Luis F. Aguirre and Kendra Phelps

Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or des... more Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or destroyed by human activities such as tourism and extractive industries. In addition to degrading the habitats of cave-roosting bats, such activities often promote contact between humans and bats, which may have potential impacts on human health. Cave-roosting bats are hosts to diverse viruses, some of which emerged in humans with severe consequences (e.g., severe acute respiratory syndrome coronavirus and Marburg virus). Characterizing patterns of viral richness and sharing among bat species are therefore important first steps for understanding bat-virus dynamics and mitigating future bat-human spillover. Here we compile a database of bat-virus associations and bat species ecological traits, and investigate the importance of roosting behavior as a determinant of viral richness and viral sharing among bat species. We show that cave-roosting species do not host greater viral richness, when accounting for publication bias, diet, body mass, and geographic range size. Our global analyses, however, show that cave-roosting bats do exhibit a greater likelihood of viral sharing, especially those documented in the literature as co-roosting in the same cave. We highlight the importance of caves as critical foci for bat conservation, as well as ideal sites for longitudinal surveillance of bat-virus dynamics.

A Comparative Analysis of Viral Richness and Viral Sharing in Cave-Roosting Bats

by Kendra Phelps, Anna Willoughby, and PREDICT Consortium

Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or des... more Caves provide critical roosting habitats for bats globally, but are increasingly disturbed or destroyed by human activities such as tourism and extractive industries. In addition to degrading the habitats of cave-roosting bats, such activities often promote contact between humans and bats, which may have potential impacts on human health. Cave-roosting bats are hosts to diverse viruses, some of which emerged in humans with severe consequences (e.g., severe acute respiratory syndrome coronavirus and Marburg virus). Characterizing patterns of viral richness and sharing among bat species are therefore important first steps for understanding bat-virus dynamics and mitigating future bat-human spillover. Here we compile a database of bat-virus associations and bat species ecological traits, and investigate the importance of roosting behavior as a determinant of viral richness and viral sharing among bat species. We show that cave-roosting species do not host greater viral richness, when accounting for publication bias, diet, body mass, and geographic range size. Our global analyses, however, show that cave-roosting bats do exhibit a greater likelihood of viral sharing, especially those documented in the literature as co-roosting in the same cave. We highlight the importance of caves as critical foci for bat conservation, as well as ideal sites for longitudinal surveillance of bat-virus dynamics.

Correlates of cave-roosting bat diversity as an effective tool to identify priority caves

by Kendra Phelps and Tigga Kingston

Cave ecosystems are subterranean biodiversity hotspots, but limited knowledge of the distribution... more Cave ecosystems are subterranean biodiversity hotspots, but limited knowledge of the distribution of diversity among caves hampers their conservation. Surveys of surrogate taxa (e.g., keystone species) can identify hotspots of biodiversity when knowledge about an ecosystem is lacking. Bats are keystone species in cave ecosystems because their guano is the primary energy source supporting diverse assemblages of cave-dependent wildlife. However , directly measuring bat diversity is time-consuming and requires expert knowledge; instead, we suggest the use of correlates of bat diversity that can be derived from readily accessible data (e.g., land-use maps) and straightforward methods not requiring expert knowledge (e.g., cave surveys, interviews) as a foundation for prioritizing caves. To identify easily measurable correlates of bat diversity, we compared assemblage composition and species abundances of 21 bat species captured in 56 caves on Bohol Island, Philippines, along gradients in environmental factors and human disturbance. Model-and distance-based methods indicated that surface-level disturbance (i.e., percent non-forested habitat, degree of urbanization and road development) along with cave complexity (i.e., available roosting area, structural heterogeneity, number of entrances and temperature range) were the most influential factors governing cave-roosting bat assemblages, thus representing correlates of bat diversity. Prioritization schemes based on these correlates select combinations of caves with greater species richness than both random selection and selection of caves based on observed richness from intensive bat surveys. The use of easy-to-measure environmental and disturbance correlates of bat diversity is an effective tool to prioritize caves to protect cave-roosting bats and the cave-dependent wildlife they support.

Bats and Buildings: The Conservation of Synanthropic Bats

Humans have shared buildings with bats for thousands of years, probably as early as first humans ... more Humans have shared buildings with bats for thousands of years, probably as early as first humans built primitive huts. Indeed, many bat species can be defined as synanthropic, i.e., they have a strong ecological association with humans. Bats have been observed using buildings as roosting and foraging sites, temporary shelters, for reproduction and hibernation. A synanthropic lifestyle may result in direct fitness benefits owing to energetic advantages in warmer roosts, which may ultimately lead to more rapid gestation and faster development of juveniles, or by being less exposed to natural predators in urban environments. All these benefits may allow bats to use buildings as stepping stones to exploit habitats
otherwise devoid of roosting structures and may even lead to the expansion of geographic ranges. Yet, the coexistence with humans also comes with some risks. Bats may be exposed to chemical pollutants, particularly preservation chemicals
used on lumber or during pest control measures. Bats may also be at risk of direct persecution or they may die accidently if trapped within buildings. In general, eviction of bats from buildings should follow the general rule of avoidance–mitigation–compensation. When considering conservation measures for synanthropic bats, it is most important to assess the role of the building for different life stages of bats. Construction work at buildings should be conducted in a manner that minimizes disturbance of bats. Artificial roosts can replace lost roosts, yet bats will often not accept alternative roosts. Demographic changes in human populations
may lead to the abandonment of buildings, for example, in rural areas and to increased conflicts in urban areas when old buildings are replaced by new buildings or when previously unoccupied space in buildings is renovated. We advocate
maintenance and enhancement of roosts for synanthropic bats, in addition to outreach and education campaigns, to improve the tolerance of humans for synanthropic bats.

Ecological Characteristics of Small Mammal Communities Inhabiting Tar Creek Superfund Site, Oklahoma

ECOLOGICAL CHARACTERISTICS OF SMALL MAMMAL COMMUNITIES INHABITING TAR CREEK SUPERFUND SITE, OKLAH... more

Population Parameters of Peromyscus leucopus (White-footed Mice) Inhabiting a Heavy Metal Contaminated Superfund Site

We used standard mark-recapture techniques to investigate ecological characteristics of Peromyscu... more We used standard mark-recapture techniques to investigate ecological characteristics of Peromyscus leucopus (white-footed mouse) populations inhabiting two locations within a heavy metal contaminated site, Tar Creek Superfund Site, and reference sites, Lake Carl Blackwell and Oologah Wildlife Management Area, located in northeastern Oklahoma. Basic demographic parameters such as population size, survival rate, recapture rate, mean minimum longevity, number of reproductively active females, reproductive success, and incidence of botfly (Cuterebra fontinella) infestation were not significantly different between contaminated and reference sites. However, adult, non-reproductive P. leucopus inhabiting contaminated sites had, on average, a larger body mass than those from reference sites. Other indicators of overall individual health, dental condition and prevalence of botfly infestations, were significantly different among populations. Instances of extensive mottling of the upper and lower incisors, a reliable indicator of exposure to heavy metal contamination, were only noted in individuals inhabiting contaminated sites. Unfortunately, no direct link between site contamination and alterations to some population parameters could be established.