Caroline Glidden
Basic Life Res Scientist
Biology
Academic Appointments
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Basic Life Research Scientist, Biology
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Postdoctoral Fellow, Institute for Human-Centered Artificial Intelligence (HAI)
All Publications
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Distinct life history strategies underpin clear patterns of succession in microparasite communities infecting a wild mammalian host.
Molecular ecology
2023
Abstract
Individual animals in natural populations tend to host diverse parasite species concurrently over their lifetimes. In free-living ecological communities, organismal life histories shape interactions with their environment, which ultimately forms the basis of ecological succession. However, the structure and dynamics of mammalian parasite communities have not been contextualized in terms of primary ecological succession, in part because few datasets track occupancy and abundance of multiple parasites in wild hosts starting at birth. Here, we studied community dynamics of twelve subtypes of protozoan microparasites (Theileria spp.) in a herd of African buffalo. We show that Theileria communities followed predictable patterns of succession underpinned by four different parasite life-history strategies. In contrast to many free-living communities, network complexity decreased with host age. Examining parasite communities through the lens of succession may better inform the effect of complex within host eco-evolutionary dynamics on infection outcomes, including parasite co-existence through the lifetime of the host.
View details for DOI 10.1111/mec.16949
View details for PubMedID 37009964
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Human footprint is associated with shifts in the assemblages of major vector-borne diseases
NATURE SUSTAINABILITY
2023
View details for DOI 10.1038/s41893-023-01080-1
View details for Web of Science ID 000948642200003
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Data-driven predictions of potential Leishmania vectors in the Americas.
PLoS neglected tropical diseases
2023; 17 (2): e0010749
Abstract
The incidence of vector-borne diseases is rising as deforestation, climate change, and globalization bring humans in contact with arthropods that can transmit pathogens. In particular, incidence of American Cutaneous Leishmaniasis (ACL), a disease caused by parasites transmitted by sandflies, is increasing as previously intact habitats are cleared for agriculture and urban areas, potentially bringing people into contact with vectors and reservoir hosts. Previous evidence has identified dozens of sandfly species that have been infected with and/or transmit Leishmania parasites. However, there is an incomplete understanding of which sandfly species transmit the parasite, complicating efforts to limit disease spread. Here, we apply machine learning models (boosted regression trees) to leverage biological and geographical traits of known sandfly vectors to predict potential vectors. Additionally, we generate trait profiles of confirmed vectors and identify important factors in transmission. Our model performed well with an average out of sample accuracy of 86%. The models predict that synanthropic sandflies living in areas with greater canopy height, less human modification, and within an optimal range of rainfall are more likely to be Leishmania vectors. We also observed that generalist sandflies that are able to inhabit many different ecoregions are more likely to transmit the parasites. Our results suggest that Psychodopygus amazonensis and Nyssomia antunesi are unidentified potential vectors, and should be the focus of sampling and research efforts. Overall, we found that our machine learning approach provides valuable information for Leishmania surveillance and management in an otherwise complex and data sparse system.
View details for DOI 10.1371/journal.pntd.0010749
View details for PubMedID 36809249
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Human-mediated impacts on biodiversity and the consequences for zoonotic disease spillover.
Current biology : CB
2021; 31 (19): R1342-R1361
Abstract
Human-mediated changes to natural ecosystems have consequences for both ecosystem and human health. Historically, efforts to preserve or restore 'biodiversity' can seem to be in opposition to human interests. However, the integration of biodiversity conservation and public health has gained significant traction in recent years, and new efforts to identify solutions that benefit both environmental and human health are ongoing. At the forefront of these efforts is an attempt to clarify ways in which biodiversity conservation can help reduce the risk of zoonotic spillover of pathogens from wild animals, sparking epidemics and pandemics in humans and livestock. However, our understanding of the mechanisms by which biodiversity change influences the spillover process is incomplete, limiting the application of integrated strategies aimed at achieving positive outcomes for both conservation and disease management. Here, we review the literature, considering a broad scope of biodiversity dimensions, to identify cases where zoonotic pathogen spillover is mechanistically linked to changes in biodiversity. By reframing the discussion around biodiversity and disease using mechanistic evidence - while encompassing multiple aspects of biodiversity including functional diversity, landscape diversity, phenological diversity, and interaction diversity - we work toward general principles that can guide future research and more effectively integrate the related goals of biodiversity conservation and spillover prevention. We conclude by summarizing how these principles could be used to integrate the goal of spillover prevention into ongoing biodiversity conservation initiatives.
View details for DOI 10.1016/j.cub.2021.08.070
View details for PubMedID 34637744
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A systematic review of climate-change driven range shifts in mosquito vectors.
bioRxiv : the preprint server for biology
2025
Abstract
As global temperatures rise, concerns about shifting mosquito ranges-and accompanying changes in the transmission of malaria, dengue, and other diseases-are mounting. However, systematic evidence for climate-driven changes in mosquito ranges remains limited. We conducted a systematic review of studies documenting expansions or contractions in medically important mosquito species. In total, 178 studies on six continents identified range expansions in 118 mosquito species. While over a third of these studies cited warming as a driver, fewer than 10% performed statistical tests of the role of climate. Instead, most expansions were linked to human-aided dispersal (e.g., trade, travel), land-use changes, and urbanization. Although several studies reported poleward or upward expansions consistent with climate warming, none demonstrated warm-edge contractions driven by rising temperatures, which are theoretically predicted in some settings. Rather than expanding into newly suitable areas, many expansions appear to be filling preexisting thermally suitable habitats. Our findings highlight the need for long-term mosquito monitoring, rigorous climate-attribution methods, and better documentation of confounding factors like land-use change and vector control efforts to disentangle climate-driven changes from other anthropogenic factors.
View details for DOI 10.1101/2025.03.25.645279
View details for PubMedID 40196676
View details for PubMedCentralID PMC11974840
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Mapping schistosomiasis risk landscapes and implications for disease control: A case study for low endemic areas in the Middle Paranapanema river basin, São Paulo, Brazil.
PLoS neglected tropical diseases
2024; 18 (11): e0012582
Abstract
Schistosomiasis, a chronic parasitic disease, remains a public health issue in tropical and subtropical regions, especially in low and moderate-income countries lacking assured access to safe water and proper sanitation. A national prevalence survey carried out by the Brazilian Ministry of Health from 2011 to 2015 found a decrease in human infection rates to 1%, with 19 out of 26 states still classified as endemic areas. There is a risk of schistosomiasis reemerging as a public health concern in low-endemic regions. This study proposes an integrated landscape-based approach to aid surveillance and control strategies for schistosomiasis in low-endemic areas.In the Middle Paranapanema river basin, specific landscapes linked to schistosomiasis were identified using a comprehensive methodology. This approach merged remote sensing, environmental, socioeconomic, epidemiological, and malacological data. A team of experts identified ten distinct landscape categories associated with varying levels of schistosomiasis transmission potential. These categories were used to train a supervised classification machine learning algorithm, resulting in a 92.5% overall accuracy and a 6.5% classification error. Evaluation revealed that 74.6% of collected snails from water collections in five key municipalities within the basin belonged to landscape types with higher potential for S. mansoni infection. Landscape connectivity metrics were also analysed.This study highlights the role of integrated landscape-based analyses in informing strategies for eliminating schistosomiasis. The methodology has produced new schistosomiasis risk maps covering the entire basin. The region's low endemicity can be partly explained by the limited connectivity among grouped landscape-units more prone to triggering schistosomiasis transmission. Nevertheless, changes in social, economic, and environmental landscapes, especially those linked to the rising pace of incomplete urbanization processes in the region, have the potential to increase risk of schistosomiasis transmission. This study will help target interventions to bring the region closer to schistosomiasis elimination.
View details for DOI 10.1371/journal.pntd.0012582
View details for PubMedID 39495810
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Temperature dependence of mosquitoes: Comparing mechanistic and machine learning approaches.
PLoS neglected tropical diseases
2024; 18 (9): e0012488
Abstract
Mosquito vectors of pathogens (e.g., Aedes, Anopheles, and Culex spp. which transmit dengue, Zika, chikungunya, West Nile, malaria, and others) are of increasing concern for global public health. These vectors are geographically shifting under climate and other anthropogenic changes. As small-bodied ectotherms, mosquitoes are strongly affected by temperature, which causes unimodal responses in mosquito life history traits (e.g., biting rate, adult mortality rate, mosquito development rate, and probability of egg-to-adult survival) that exhibit upper and lower thermal limits and intermediate thermal optima in laboratory studies. However, it remains unknown how mosquito thermal responses measured in laboratory experiments relate to the realized thermal responses of mosquitoes in the field. To address this gap, we leverage thousands of global mosquito occurrences and geospatial satellite data at high spatial resolution to construct machine-learning based species distribution models, from which vector thermal responses are estimated. We apply methods to restrict models to the relevant mosquito activity season and to conduct ecologically plausible spatial background sampling centered around ecoregions for comparison to mosquito occurrence records. We found that thermal minima estimated from laboratory studies were highly correlated with those from the species distributions (r = 0.87). The thermal optima were less strongly correlated (r = 0.69). For most species, we did not detect thermal maxima from their observed distributions so were unable to compare to laboratory-based estimates. The results suggest that laboratory studies have the potential to be highly transportable to predicting lower thermal limits and thermal optima of mosquitoes in the field. At the same time, lab-based models likely capture physiological limits on mosquito persistence at high temperatures that are not apparent from field-based observational studies but may critically determine mosquito responses to climate warming. Our results indicate that lab-based and field-based studies are highly complementary; performing the analyses in concert can help to more comprehensively understand vector response to climate change.
View details for DOI 10.1371/journal.pntd.0012488
View details for PubMedID 39283940
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Climate and urbanization drive changes in the habitat suitability of Schistosoma mansoni competent snails in Brazil.
Nature communications
2024; 15 (1): 4838
Abstract
Schistosomiasis is a neglected tropical disease caused by Schistosoma parasites. Schistosoma are obligate parasites of freshwater Biomphalaria and Bulinus snails, thus controlling snail populations is critical to reducing transmission risk. As snails are sensitive to environmental conditions, we expect their distribution is significantly impacted by global change. Here, we used machine learning, remote sensing, and 30 years of snail occurrence records to map the historical and current distribution of forward-transmitting Biomphalaria hosts throughout Brazil. We identified key features influencing the distribution of suitable habitat and determined how Biomphalaria habitat has changed with climate and urbanization over the last three decades. Our models show that climate change has driven broad shifts in snail host range, whereas expansion of urban and peri-urban areas has driven localized increases in habitat suitability. Elucidating change in Biomphalaria distribution-while accounting for non-linearities that are difficult to detect from local case studies-can help inform schistosomiasis control strategies.
View details for DOI 10.1038/s41467-024-48335-9
View details for PubMedID 38898012
View details for PubMedCentralID PMC11186836
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Species distribution modeling for disease ecology: A multi-scale case study for schistosomiasis host snails in Brazil.
PLOS global public health
2024; 4 (8): e0002224
Abstract
Species distribution models (SDMs) are increasingly popular tools for profiling disease risk in ecology, particularly for infectious diseases of public health importance that include an obligate non-human host in their transmission cycle. SDMs can create high-resolution maps of host distribution across geographical scales, reflecting baseline risk of disease. However, as SDM computational methods have rapidly expanded, there are many outstanding methodological questions. Here we address key questions about SDM application, using schistosomiasis risk in Brazil as a case study. Schistosomiasis is transmitted to humans through contact with the free-living infectious stage of Schistosoma spp. parasites released from freshwater snails, the parasite's obligate intermediate hosts. In this study, we compared snail SDM performance across machine learning (ML) approaches (MaxEnt, Random Forest, and Boosted Regression Trees), geographic extents (national, regional, and state), types of presence data (expert-collected and publicly-available), and snail species (Biomphalaria glabrata, B. straminea, and B. tenagophila). We used high-resolution (1km) climate, hydrology, land-use/land-cover (LULC), and soil property data to describe the snails' ecological niche and evaluated models on multiple criteria. Although all ML approaches produced comparable spatially cross-validated performance metrics, their suitability maps showed major qualitative differences that required validation based on local expert knowledge. Additionally, our findings revealed varying importance of LULC and bioclimatic variables for different snail species at different spatial scales. Finally, we found that models using publicly-available data predicted snail distribution with comparable AUC values to models using expert-collected data. This work serves as an instructional guide to SDM methods that can be applied to a range of vector-borne and zoonotic diseases. In addition, it advances our understanding of the relevant environment and bioclimatic determinants of schistosomiasis risk in Brazil.
View details for DOI 10.1371/journal.pgph.0002224
View details for PubMedID 39093879
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Human footprint is associated with shifts in the assemblages of major vector-borne diseases.
Nature sustainability
2023; 6 (6): 652-661
Abstract
Predicting how increasing intensity of human-environment interactions affects pathogen transmission is essential to anticipate changing disease risks and identify appropriate mitigation strategies. Vector-borne diseases (VBDs) are highly responsive to environmental changes, but such responses are notoriously difficult to isolate because pathogen transmission depends on a suite of ecological and social responses in vectors and hosts that may differ across species. Here we use the emerging tools of cumulative pressure mapping and machine learning to better understand how the occurrence of six medically important VBDs, differing in ecology from sylvatic to urban, respond to multidimensional effects of human pressure. We find that not only is human footprint-an index of human pressure, incorporating built environments, energy and transportation infrastructure, agricultural lands and human population density-an important predictor of VBD occurrence, but there are clear thresholds governing the occurrence of different VBDs. Across a spectrum of human pressure, diseases associated with lower human pressure, including malaria, cutaneous leishmaniasis and visceral leishmaniasis, give way to diseases associated with high human pressure, such as dengue, chikungunya and Zika. These heterogeneous responses of VBDs to human pressure highlight thresholds of land-use transitions that may lead to abrupt shifts in infectious disease burdens and public health needs.
View details for DOI 10.1038/s41893-023-01080-1
View details for PubMedID 37538395
View details for PubMedCentralID PMC10399301
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Phylogenetic and biogeographical traits predict unrecognized hosts of zoonotic leishmaniasis.
PLoS neglected tropical diseases
2023; 17 (5): e0010879
Abstract
The spatio-temporal distribution of leishmaniasis, a parasitic vector-borne zoonotic disease, is significantly impacted by land-use change and climate warming in the Americas. However, predicting and containing outbreaks is challenging as the zoonotic Leishmania system is highly complex: leishmaniasis (visceral, cutaneous and muco-cutaneous) in humans is caused by up to 14 different Leishmania species, and the parasite is transmitted by dozens of sandfly species and is known to infect almost twice as many wildlife species. Despite the already broad known host range, new hosts are discovered almost annually and Leishmania transmission to humans occurs in absence of a known host. As such, the full range of Leishmania hosts is undetermined, inhibiting the use of ecological interventions to limit pathogen spread and the ability to accurately predict the impact of global change on disease risk. Here, we employed a machine learning approach to generate trait profiles of known zoonotic Leishmania wildlife hosts (mammals that are naturally exposed and susceptible to infection) and used trait-profiles of known hosts to identify potentially unrecognized hosts. We found that biogeography, phylogenetic distance, and study effort best predicted Leishmania host status. Traits associated with global change, such as agricultural land-cover, urban land-cover, and climate, were among the top predictors of host status. Most notably, our analysis suggested that zoonotic Leishmania hosts are significantly undersampled, as our model predicted just as many unrecognized hosts as unknown hosts. Overall, our analysis facilitates targeted surveillance strategies and improved understanding of the impact of environmental change on local transmission cycles.
View details for DOI 10.1371/journal.pntd.0010879
View details for PubMedID 37256857
View details for PubMedCentralID PMC10231829
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Strategies for managing marine disease
ECOLOGICAL APPLICATIONS
2022: e2643
Abstract
The incidence of emerging infectious diseases (EIDs) has increased in wildlife populations in recent years and is expected to continue to increase with global environmental change. Marine diseases are relatively understudied compared with terrestrial diseases but warrant parallel attention as they can disrupt ecosystems, cause economic loss, and threaten human livelihoods. Although there are many existing tools to combat the direct and indirect consequences of EIDs, these management strategies are often insufficient or ineffective in marine habitats compared with their terrestrial counterparts, often due to fundamental differences between marine and terrestrial systems. Here, we first illustrate how the marine environment and marine organism life histories present challenges and opportunities for wildlife disease management. We then assess the application of common disease management strategies to marine versus terrestrial systems to identify those that may be most effective for marine disease outbreak prevention, response, and recovery. Finally, we recommend multiple actions that will enable more successful management of marine wildlife disease emergencies in the future. These include prioritizing marine disease research and understanding its links to climate change, improving marine ecosystem health, forming better monitoring and response networks, developing marine veterinary medicine programs, and enacting policy that addresses marine and other wildlife diseases. Overall, we encourage a more proactive rather than reactive approach to marine wildlife disease management and emphasize that multidisciplinary collaborations are crucial to managing marine wildlife health.
View details for DOI 10.1002/eap.2643
View details for Web of Science ID 000828498100001
View details for PubMedID 35470930
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EXPLORING THE USE OF THE ERYTHROCYTE SEDIMENTATION RATE AS AN INFLAMMATORY MARKER FOR FREE-RANGING WILDLIFE: A CASE STUDY IN AFRICAN BUFFALO (SYNCERUS CAFFER)
JOURNAL OF WILDLIFE DISEASES
2022; 58 (2): 298-308
Abstract
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.
View details for DOI 10.7589/JWD-D-21-001I4
View details for Web of Science ID 000787191700005
View details for PubMedID 35276000
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Corrigendum: Global Patterns of the Fungal Pathogen Batrachochytrium dendrobatidis Support Conservation Urgency.
Frontiers in veterinary science
2022; 9: 825058
Abstract
[This corrects the article DOI: 10.3389/fvets.2021.685877.].
View details for DOI 10.3389/fvets.2022.825058
View details for PubMedID 35211542
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Global Patterns of the Fungal Pathogen Batrachochytrium dendrobatidis Support Conservation Urgency.
Frontiers in veterinary science
2021; 8: 685877
Abstract
The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) is a skin pathogen that can cause the emerging infectious disease chytridiomycosis in susceptible species. It has been considered one of the most severe threats to amphibian biodiversity. We aimed to provide an updated compilation of global Bd occurrences by host taxon and geography, and with the larger global Bd dataset we reanalyzed Bd associations with environmental metrics at the world and regional scales. We also compared our Bd data compilation with a recent independent assessment to provide a more comprehensive count of species and countries with Bd occurrences. Bd has been detected in 1,375 of 2,525 (55%) species sampled, more than doubling known species infections since 2013. Bd occurrence is known from 93 of 134 (69%) countries at this writing; this compares to known occurrences in 56 of 82 (68%) countries in 2013. Climate-niche space is highly associated with Bd detection, with different climate metrics emerging as key predictors of Bd occurrence at regional scales; this warrants further assessment relative to climate-change projections. The accretion of Bd occurrence reports points to the common aims of worldwide investigators to understand the conservation concerns for amphibian biodiversity in the face of potential disease threat. Renewed calls for better mitigation of amphibian disease threats resonate across continents with amphibians, especially outside Asia. As Bd appears to be able to infect about half of amphibian taxa and sites, there is considerable room for biosecurity actions to forestall its spread using both bottom-up community-run efforts and top-down national-to-international policies. Conservation safeguards for sensitive species and biodiversity refugia are continuing priorities.
View details for DOI 10.3389/fvets.2021.685877
View details for PubMedID 34336978