OSE Students & Grads Present at EEID 2021

In an *UNPRECEDENTED* year, a delayed Ecology and Evolution of Infectious Diseases meeting reformulated into an “Animal Crossing”-esque virtual conference extravaganza. Check out the amazing work OSE students and graduates presented while navigating a complex map full of disease experts, habitat boundaries, and french paraphernalia.

Aedes aegypti outcompetes Anopheles stephensi across a range of larval temperatures
MV Evans, JM Drake, L Jones, CC Murdock

Anopheles stephensi, the primary vector of malaria in urban centers in India, has recently expanded its range across the Middle East and North Africa, raising concern it may become established and contribute to urban malaria transmission in sub-Saharan Africa. In its invasive range, An. stephensi interacts with resident mosquito species, and understanding how these interactions can affect An. stephensi population dynamics is necessary to predict transmission risk at the species’ invasive edge.  Further, mosquito life-history traits are extremely sensitive to temperature and competition between mosquito species may be dependent on temperature as well. Here, we explored temperature-dependent competition between An. stephensi and Ae. aegypti across five temperatures (16 –  32 C). We measured traits relevant for population growth from which we estimated each species’ per capita growth rates and derived each species’ competitive ability at each temperature. Ae. aegypti emerged as the dominant competitor at all temperatures, primarily due to differences in larval survival and development times across the two species. Our results suggest that competitive interactions with resident mosquito species, such as Ae. aegypti, could shape the distribution of An. stephensi, and therefore the human population at risk of urban malaria, across its invasive range.


Community composition, abundance, and environmental coditions may synergistically enhance transmission of a ranavirus in larval amphibian communities

Daniel Suh and Andrew Park

Communities of hosts can change through space and time, altering the transmission potential of parasites. We investigated how changes in host composition, total host abundance, and environmental conditions affect a ranavirus in larval amphibian communities. We developed a dynamical model for ranavirus in a 2-species community and manipulated this model in terms of community composition, host abundance, and viral half-life. Next, we measured community competence, diversity (richness, evenness, phylogeny), and overall composition using previously collected amphibian community data. Community competence is the propensity for a community of hosts to support a parasite and was calculated as the sum of the products of each species’ mean viral load and their relative abundance in a community. After calculating these metrics, we used data visualization and correlation tests to detect patterns between our variables of interest (composition, abundance, and environment) and transmission potential of ranavirus. 

Our transmission model showed that manipulations of community composition, host abundance, and viral half-life can all enhance a community’s ability to support a parasite, and that when combined, the effects of these variables resulted in communities highly susceptible to ranavirus. Analysis of real host communities confirmed that similar host compositions (according to PCA ordination) had similar community competence, but dissimilar compositions could still result in similar community competence. In our diversity analysis, we found patterns across an evenness gradient but not across richness. We also saw that high competence species appeared intermediately dispersed throughout the phylogeny. Further analysis showed that communities with high community competence were often the most abundant and occurred in months with lower temperatures, resulting in communities highly susceptible to ranavirus. Finally, in univariate correlation tests, community competence, host abundance, and water temperature were all significantly correlated with infection prevalence in host communities.


Parasite and host traits predict the zoonotic risk of protozoa

Joy Vaz, Barbara A. Han, John M. Drake

Protozoan zoonoses such Chagas disease and leishmaniasis remain endemic in large parts of the world, exacerbating social inequity and contributing heavily to the global burden of infectious disease. Novel protozoa species which have emerged from wildlife to humans in the recent decades (e.g., Plasmodium knowlesi, a causal agent of malaria) have proven difficult to control. Our ability to anticipate and prevent future emerging disease threats relies on identifying the characteristics of zoonotic pathogens and targeting surveillance efforts accordingly. While several studies have profiled the traits of zoonotic viruses, protozoa have received limited attention. We compiled a dataset of protozoa species which incorporates both parasite and host traits, including information on community structure and importance within a host-parasite bipartite network. Using a machine learning algorithm, extreme gradient boosting, we distinguished zoonotic from non-zoonotic protozoa with 85% accuracy. Our model found that traits of generalist protozoa (e.g., broad tissue tropism, high network centrality, multiple transmission modes) were most useful for predicting zoonotic status, compared to intrinsic biological traits (e.g., morphology), environmental traits (e.g., temperature), or host-related traits (e.g., life history). We ranked the zoonotic potential of protozoa species currently not known to be zoonotic based on their trait similarity to known zoonotic protozoa. Here we report parasitic protozoa species of wild mammals which are most likely to be undiscovered sources of current or future zoonoses, identifying them as priority targets for surveillance.


Urbanization, food provisioning, and transmission-relevant behaviors in Florida white ibis

Cali A. Wilson, Julia N. Weil, Sonia M. Hernandez, Sonia Altizer, Richard J. Hall.

As urban areas expand and natural habitats shrink, many wildlife species have shifted into cities. In urban areas, animals often aggregate at higher density, move less, encounter anthropogenic stressors, and alter their diets by consuming human-provided food, all of which can affect the transmission of infectious diseases. American white ibis (Eudocimus albus) in South Florida are well-suited for studying the consequences of urbanization on pathogen transmission. Ibis naturally reside in wetlands but now commonly forage in urban parks and consume human-provided food. In this study, we investigate how transmission-relevant ibis behaviors change between urban and natural sites, across urban sites along a gradient of provisioning, and when urban ibis are fed. We find that ibis in urban parks spent less time actively foraging relative to those in natural wetlands. Within urban sites, foraging, preening, and vigilance behaviors differed across the sites observed. Ibis at two urban sites foraged less, on average, than those at other sites, but spent significantly more time preening or being vigilant. Lastly, during feeding intervals, ibis density increased by over 20 times each time food was thrown. These results suggest that urbanization and provisioning alter wildlife behavior in ways that can influence exposure to parasites. Specifically, in ibis, food provisioning can increase local density and contact rates for transmission of directly-transmitted parasites, while decreasing exposure to environmentally-transmitted parasites due to lower active foraging time. Further studies of how urbanization and recreational feeding influences wildlife behavior can inform management strategies to benefit both wildlife and human health.

Field and Laboratory Evaluation of the Microsporidian Parasite Heterosporis sutherlandae: Prevalence, Severity, and Transmission

Heterosporis sutherlandae is an invasive microsporidian parasite in the Great Lakes region of North America that infects the skeletal muscle of numerous fish species, rendering the fillet unfit for human consumption. Although H. sutherlandae has been identified as a pathogen of concern by state management agencies, there is little information to inform regulation and intervention. We sampled fishes over 1 year from three lakes in northern Minnesota with known infected populations to determine the importance of host demographic and environmental variables for influencing H. sutherlandae infection prevalence. Heterosporis sutherlandae was present during all sampling periods, ranging in prevalence from 1% to 11%. The prevalence of Hsutherlandae among Yellow Perch Perca flavescens varied significantly according to season, with winter having the lowest prevalence (1%) and summer having the highest prevalence (11%). For other fish species, the prevalence of H. sutherlandae also varied significantly with season: the lowest prevalence occurred during spring (1%) and the highest prevalence occurred in fall (9%). Rates of pathogen transmission were estimated by exposing Fathead Minnows Pimephales promelas in the laboratory. Transmission rates were 23% when naïve fish were fed infected tissues and only 2% when naïve fish were held in cohabitation with tissue-fed fish. Exposure method and exposure duration (d) increased the probability that a fish was infected with H. sutherlandae. These findings suggest that H. sutherlandae transmission is greater when a susceptible host consumes infected tissue than when the fish is exposed to spores present in the water column. The current rates of infection in wild fishes are in stark contrast to the prevalence documented in 2004 (28%), suggesting a reduction in H. sutherlandae prevalence within at least one Yellow Perch population in the Laurentian Great Lakes region since the early 2000s.

Tomamichel MM, Venturelli PA, Phelps NB. Field and Laboratory Evaluation of the Microsporidian Parasite Heterosporis sutherlandae: Prevalence, Severity, and Transmission. Journal of Aquatic Animal Health. 2020 Dec 28. https://afspubs.onlinelibrary.wiley.com/doi/full/10.1002/aah.10122

Measuring spatial co-occurrences of species potentially involved in Leishmania transmission cycles through a predictive and fieldwork approach

A CDC Miniature Light Trap used in the fieldwork for López et al. 2021. Photo provided by Juliana Hoyos.

The Leishmaniases are a group of neglected tropical diseases caused by different species of the protozoan parasite Leishmania, transmitted to its mammalian hosts by the bites of several species of female Phlebotominae sand flies. Many factors have contributed to shifts in the disease distribution and eco epidemiological outcomes, resulting in the emergence of Cutaneous Leishmaniasis outbreaks and the incrimination of vectors in unreported regions. New research development is vital for establishing the new paradigms of the present transmission cycles, hoping to facilitate new control strategies to reduce parasite transmission. Hereafter, this work aims to model and infer the current transmission cycles of Cutaneous Leishmaniasis in Colombia defined by vector and mammal species distributed and interacting in the different regions and validate them by performing sand fly and mammal collections. Vector-host co-occurrences were computed considering five ecoregions of the Colombian territory defined by the World Wide Fund for Nature (WWF) and downloaded from The Nature Conservancy TNC Maps website. Four validation sites were selected based on Cutaneous Leishmaniasis prevalence reports. Sand flies and mammals captured in the field were processed, and species were defined using conventional taxonomic guidelines. Detection of infection by Leishmania was performed to identify transmission cycles in the selected areas. This study uses predictive models based on available information from international gazetteers and fieldwork to confirm sand fly and mammalian species’ sustaining Leishmania transmission cycles. Our results show an uneven distribution of mammal samples in Colombia, possibly due to sampling bias, since only two departments contributed 50% of the available samples. Bats were the vertebrates with the highest score values, suggesting substantial spatial overlap with sand flies than the rest of the vertebrates evaluated. Fieldwork allowed identifying three circulating Leishmania species, isolated from three sand fly species. In the Montane Forest ecosystem, one small marsupial, Gracilinanus marica, was found infected with Leishmania panamensis, constituting the first record of this species infected with Leishmania. In the same locality, an infected sand fly, Pintomyia pia, was found. The overall results could support the understanding of the current transmission cycles of Leishmaniasis in Colombia.

López, M., Erazo, D., Hoyos, Jet al. Measuring spatial co-occurrences of species potentially involved in Leishmania transmission cycles through a predictive and fieldwork approach. Sci Rep 11, 6789 (2021). https://doi.org/10.1038/s41598-021-85763-9.

Mosquito- virus interactions

Check out the new book chapter on mosquito virus development by OSE students Mike Newberry and Nikki Solano-Asamoah, and recent OSE graduate Dr. Michelle Evans!

Reitmayer CM, Evans MV, Miazgowicz KL, Newberry PM, Solano-Asamoah N, Tesla B, and CC Murdock. Mosquito- virus interactions. In Population Biology of Vector-Borne Diseases. Drake JM, Bonsall M, Strand M, editors. Oxford University Press; 2020 Dec 30. Section 3; Chapter 11.

Thermal tolerance and environmental persistence of a protozoan parasite in monarch butterflies

Figure 2 from the paper. Predicted probabilities of OE infection are plotted over the range of experimental temperatures for the three exposure durations: 2 weeks (purple), 35 weeks (blue), and 93 weeks (green). Provided by Isabella Ragonese.

Many parasites have external transmission stages that persist in the environment prior to infecting a new host. Understanding how long these stages can persist, and how abiotic conditions such as temperature affect parasite persistence, is important for predicting infection dynamics and parasite responses to future environmental change. In this study, we explored environmental persistence and thermal tolerance of a debilitating protozoan parasite that infects monarch butterflies. Parasite transmission occurs when dormant spores, shed by adult butterflies onto host plants and other surfaces, are later consumed by caterpillars. We exposed parasite spores to a gradient of ecologically-relevant temperatures for 2, 35, or 93 weeks. We tested spore viability by feeding controlled spore doses to susceptible monarch larvae, and examined relationships between temperature, time, and resulting infection metrics. We also examined whether distinct parasite genotypes derived from replicate migratory and resident monarch populations differed in their thermal tolerance. Finally, we examined evidence for a trade-off between short-term within-host replication and long-term persistence ability. Parasite viability decreased in response to warmer temperatures over moderate-to-long time scales. Individual parasite genotypes showed high heterogeneity in viability, but differences did not cluster by migratory vs. resident monarch populations. We found no support for a negative relationship between environmental persistence and within-host replication, as might be expected if parasites invest in short-term reproduction at the cost of longer-term survival. Findings here indicate that dormant spores can survive for many months under cooler conditions, and that heat dramatically shortens the window of transmission for this widespread and virulent butterfly parasite.

Ophryocystis elektroscirrha, the brown football shapes depicted above, is an obligate, neogregarine protozoan parasite that infects monarch butterflies
Sánchez CA, Ragonese IG, de Roode JC, Altizer S. Thermal tolerance and environmental persistence of a protozoan parasite in monarch butterflies. Journal of Invertebrate Pathology. 2021 Feb 11:107544. https://doi.org/10.1016/j.jip.2021.107544

Read more on the Center for Ecology of Infectious Diseases website.

Carry-over Effects of the Larval Environment in Mosquito-Borne Disease Symptoms

Figure 9.1 Life-cycle of a mosquito, from egg to larvae to pupae to adult. Environmental carry-over effects of the larval environment and the
relevant adult life history traits discussed in this chapter are labeled.
Source: Eric Marty.

Check out the new book chapter by OSE student Mike Newberry and recent OSE graduate Dr. Michelle Evans!

Evans, M., Newberry, Philip M., and Courtney C. Murdock. “Carry-over Effects of the Larval Environment” in Population Biology of Vector-Borne Diseases. Editors: Drake JM, Bonsall M, Strand M. Oxford University Press; 2020 Dec 30. 155-174.

Habitat use as indicator of adaptive capacity to climate change

A male moose lounges in the grass. Image by David Mark from Pixabay.

Aim

Populations of cold‐adapted species at the trailing edges of geographic ranges are particularly vulnerable to the negative effects of climate change from the combination of exposure to warm temperatures and high sensitivity to heat. Many of these species are predicted to decline under future climate scenarios, but they could persist if they can adapt to warming climates either physiologically or behaviourally. We aim to understand local variation in contemporary habitat use and use this information to identify signs of adaptive capacity. We focus on moose (Alces alces), a charismatic species of conservation and public interest.

Location

The northeastern United States, along the trailing edge of the moose geographic range in North America.

Methods

We compiled data on occurrences and habitat use of moose from remote cameras and GPS collars across the northeastern United States. We use these data to build habitat suitability models at local and regional spatial scales and then to predict future habitat suitability under climate change. We also use fine‐scale GPS data to model relationships between habitat use and temperature on a daily temporal scale and to predict future habitat use.

Results

We find that habitat suitability for moose will decline under a range of climate change scenarios. However, moose across the region differ in their use of climatic and habitat space, indicating that they could exhibit adaptive capacity. We also find evidence for behavioural responses to weather, where moose increase their use of forested wetland habitats in warmer places and/or times.

Main conclusions

Our results suggest that there will be significant shifts in moose distribution due to climate change. However, if there is spatial variation in thermal tolerance, trailing‐edge populations could adapt to climate change. We highlight that prioritizing certain habitats for conservation (i.e., thermal refuges) could be crucial for this adaptation.

Teitelbaum CS, Sirén AP, Coffel E, Foster JR, Frair JL, Hinton JW, Horton RM, Kramer DW, Lesk C, Raymond C, Wattles DW. Habitat use as indicator of adaptive capacity to climate change. Diversity and Distributions. 2021. https://doi.org/10.1111/ddi.13223

Climate, Fire Regime, Geomorphology, and Conspecifics Influence the Spatial Distribution of Chinook Salmon Redds

Image of a portion of the Middle Salmon Fork stream taken by helicopter. Photo provided by Greg Jacobs.

Pacific salmon spawning and rearing habitats result from dynamic interactions among geomorphic processes, natural disturbances, and hydro‐climatological factors acting across a range of spatial and temporal scales. We used a 21‐year record of redd locations in a wilderness river network in central Idaho, USA, to examine which covariates best predict the spawning occurrence of Chinook Salmon Oncorhynchus tshawytscha and how shifts under a changing climate might affect habitat availability. We quantified geomorphic characteristics (substrate size, channel slope, and valley confinement), climatic factors (stream temperature and summer discharge), wildfire, and conspecific abundance (as inferred by the number of redds) throughout the network. We then built and compared logistic regression models that estimated redd occurrence probability as a function of these covariates in 1‐km reaches throughout the network under current and projected climate change scenarios. Redd occurrence was strongly affected by nearly all of the covariates examined. The best models indicated that climate‐driven changes in redd occurrence probabilities will be relatively small but spatially heterogeneous, with warmer temperatures increasing occurrence probabilities in cold, high‐elevation reaches and decreasing probabilities in warm, low‐elevation reaches. Furthermore, positive effects of wildfire on redd occurrence may be more important than climate‐driven effects on stream temperature and summer discharge, although climate‐related changes in temperature and scour regime during the egg incubation period may influence survival to emergence. Our results identify where favorable spawning habitats are likely to exist under climate change, how future habitat distributions may differ from contemporary conditions, and where habitat conservation might be prioritized. Furthermore, the positive occurrence–abundance relationship we observed indicates that the study site is underseeded, and effective management actions are needed for increasing the recruitment of spawning adults to take advantage of available habitat.

Figure 3 from the paper showing (A) Observed salmon occurrence, (B) model-predicted contemporary occurence, (C) model-predicted change in salmon occurrence in 2040 and (D) 2080 under climate change scenarios.

Jacobs GR, Thurow RF, Buffington JM, Isaak D, Wenger SJ. Climate, Fire Regime, Geomorphology, and Conspecifics Influence the Spatial Distribution of Chinook Salmon Redds. Transactions of the American Fisheries Society. 2020.

https://afspubs.onlinelibrary.wiley.com/doi/10.1002/tafs.10270

Dead litter of resident species first facilitates and then inhibits sequential life stages of range‐expanding species

  1. Resident species can facilitate invading species (biotic assistance) or inhibit their expansion (biotic resistance). Species interactions are often context‐dependent and the relative importance of biotic assistance versus resistance could vary with abiotic conditions or the life stage of the invading species, as invader stress tolerances and resource requirements change with ontogeny. In northeast Florida salt marshes, the abundant dead litter (wrack) of the native marsh cordgrass, Spartina alterniflora, could influence the expansion success of the black mangrove, Avicennia germinans, a tropical species that is expanding its range northward.
  2. We used two field experiments to examine how S. alterniflora wrack affects A. germinans success during (a) propagule establishment and (b) subsequent seedling survival. We also conducted laboratory feeding assays to identify propagule consumers and assess how wrack presence influences herbivory on mangrove propagules.
  3. Spartina alterniflora wrack facilitated A. germinans establishment by promoting propagule recruitment, retention and rooting; the tidal regime influenced the magnitude of these effects. However, over time S. alterniflora wrack inhibited A. germinans seedling success by smothering seedlings and attracting herbivore consumers. Feeding assays identified rodents—which seek refuge in wrack—as consumers of A. germinans propagules.
  4. Synthesis. Our results suggest that the deleterious effects of S. alterniflora wrack on A. germinans seedling survival counterbalance the initial beneficial effects of wrack on A. germinans seed establishment. Such seed‐seedling conflicts can arise when species stress tolerances and resource requirements change throughout development and vary with abiotic conditions. In concert with the tidal conditions, the relative importance of positive and negative interactions with wrack at each life stage can influence the rate of local and regional mangrove expansion. Because interaction strengths can change in direction and magnitude with ontogeny, it is essential to examine resident–invader interactions at multiple life stages and across environmental gradients to uncover the mechanisms of biotic assistance and resistance during invasion.

Smith RS, Blaze JA, Byers JE. Dead litter of resident species first facilitates and then inhibits sequential life stages of range‐expanding species. Journal of Ecology. https://doi.org/10.1111/1365-2745.13586

Graduate Student Symposium Schedule 2021

Here is the Zoom Link (Meeting ID: 917 3821 1238, Passcode: 674466). You will need to be registered via this link.

Friday, February 5

Welcoming Remarks

10:00-10:15Dean John Gittleman, Jeffrey Beauvais, Nate Tomczyk

Session I (Moderator: Rebecca Atkins)

10:15-10:30Claire TeitelbaumUrbanization and habitat specialization interact to drive infection outcomes for mobile wildlife
10:30-10:45Laura NaslundThe effects of ecosystem modification and network position on contaminant fluxes from a mountaintop mining-impacted river network
10:45-11:00Amy A. BriggsLocal vs. site-level effects of algae on coral microbial communities
11:00-11:15William WhiteDams and fried green tomatoes: Natural history and sense of place in conservation decisions
11:15 – 11:30 Break

Session II (Moderator: Rebecca Atkins)

11:30-11:45Kelsey J. SolomonSmall decreases in total canopy cover can significantly affect algal communities in southern Appalachian headwater streams
11:45-12:00Robert L. RichardsThe macro-ecology of predator-prey-parasite interactions
12:00-12:15Kyle ConnellyGetting pumped: Spatial, temporal, and economic drivers of septic tank maintenance intervals in Athens-Clarke County, Georgia
12:15–2:00LunchGraduate student lunch with Dr. Ethell Vereen

Rapid Fire Session I (Moderator: TJ Odom)

2:00-2:35Daniel C. SuhPatterns in host abundance, species richness, and species evenness reveal amphibian communities highly susceptible to Ranavirus
 Christopher R. SmagaEffects of precocious estrogen on alligator ovarian development
 Carolyn CumminsWhere will carbon go when it enters warmer streams? A test of temperature effects on shredder physiology
 Ashley BallewMonarch butterflies: Diet and infection
 Q&A
2:35 – 3:00 Break
Session III (Moderator: TJ Odom)
3:00-3:15Doreen ChaussadasImpacts of bio-loggers’ weight on their carrier: is 5% of the body mass an acceptable charge to put on a birds’ back?
3:15-3:30Kristen J. ZemaitisEcotoxicology and diet of the American alligator as a function of ontogenetic shift and prey selection
3:30-3:45Anna R. WilloughbyTourist-provided resources impact park wildlife and their parasite communities
3:45 – 4:00 Break

Poster Session
4:00 – 5:30 Virtual Poster Session (Zoom link)
Breakout Room 1:  
Corinna HazelrigBatrachochytriunm dendrobatidis prevalence throughout amphibian species and life stages of varying skin keratin richness

Christopher Brandon – Walking while parasitized: Effects of a nematode parasite on locomotion activity of horned passalus beetles

Breakout Room 2:
Caroline Aikins – Inferring diet of ringtails (Bassariscus astutus) from latrines in human-impacted park habitats

Mikey Fager – Tipping streams: Does increased temperature change the balance of carbon and nutrients in food resources?

Amelia Foley – Plastic in the urban environment: An exploratory study of microplastics in the Athens, GA community

Breakout Room 3:
Will Ellis – How parasites influence ecosystems: Studying the varied effects of a trematode parasite on its environment

Jessica Mitchell – Assessing the response of aquatic detritivore insects to experimental warming

Niki Gajjar – Morphological root traits and phylogenetic signals in Southern Africa trees and grasses

Saturday, February 6

Session IV (Moderator: Carolyn Cummins)

10:00-10:15Laura V. KojimaAssessing the consumption risk of American alligators on the Savannah River Site
10:15-10:30Jeffrey BeauvaisDemographic drivers of coastal water access in South Carolina
10:30-10:45Kate SabeyAntibiotic treatment alters gut microbiota plasticity in a wild mammal
10:45 – 11:00 Break

Rapid Fire Session II (Moderator: Carolyn Cummins)

11:00-11:40Emily M. BertucciIntrinsic and extrinsic factors interact during development to influence telomere dynamics in a long-lived apex predator
 Anna Y. BaynesFish habitat preference with changes in flow pattern in the Conasauga River, GA
 Cece WorkingHost and environment predict nematode development across temperatures
 Corinne M SweeneyRadiocesium transfer between aquatic and terrestrial environments
 Q & A
11:40 – 12:00 Break

Keynote Address

12:00-12:10Dr. Erin LippIntroduction
12:10-1:10Dr. Ethell Vereen Jr.Life in Flowing Water