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

Urban specialization reduces habitat connectivity by a highly mobile wading bird

Figure 2. Observed and simulated ibis networks Claire used in her analysis.
Provided by Claire Teitelbaum.

Background

Mobile animals transport nutrients and propagules across habitats, and are crucial for the functioning of food webs and for ecosystem services. Human activities such as urbanization can alter animal movement behavior, including site fidelity and resource use. Because many urban areas are adjacent to natural sites, mobile animals might connect natural and urban habitats. More generally, understanding animal movement patterns in urban areas can help predict how urban expansion will affect the roles of highly mobile animals in ecological processes.

Methods

Here, we examined movements by a seasonally nomadic wading bird, the American white ibis (Eudocimus albus), in South Florida, USA. White ibis are colonial wading birds that forage on aquatic prey; in recent years, some ibis have shifted their behavior to forage in urban parks, where they are fed by people. We used a spatial network approach to investigate how individual movement patterns influence connectivity between urban and non-urban sites. We built a network of habitat connectivity using GPS tracking data from ibis during their non-breeding season and compared this network to simulated networks that assumed individuals moved indiscriminately with respect to habitat type.

Results

We found that the observed network was less connected than the simulated networks, that urban-urban and natural-natural connections were strong, and that individuals using urban sites had the least-variable habitat use. Importantly, the few ibis that used both urban and natural habitats contributed the most to connectivity.

Conclusions

Habitat specialization in urban-acclimated wildlife could reduce the exchange of propagules and nutrients between urban and natural areas, which has consequences both for beneficial effects of connectivity such as gene flow and for detrimental effects such as the spread of contaminants or pathogens.

Claire S. Teitelbaum, Jeffrey Hepinstall-Cymerman, Anjelika Kidd-Weaver, Sonia M. Hernandez, Sonia Altizer, Richard J. Hall. Urban specialization reduces habitat connectivity by a highly mobile wading bird. Movement Ecology 8, 49 (2020). https://doi.org/10.1186/s40462-020-00233-7

Identifying correlates of Guinea worm (Dracunculus medinensis) infection in domestic dog populations

Figure 1. Map of spatial hotspots of Dmedinensis infection in dogs.

The eradication of human infectious diseases has proven remarkably difficult. The world has only succeeded once, in the case of the smallpox virus. However, international efforts have driven the debilitating Guinea worm parasite closer to the brink of eradication than nearly any other parasite. Coordinated efforts by the Ministries of Health in endemic countries, the U.S. Centers for Disease Control, The Carter Center, and the World Health Organization have reduced the number of annual Guinea worm cases from millions in the 1980s to hundreds in the early 2010s, but recently a new threat has emerged. Guinea worm infections have been diagnosed in domestic dogs, particularly in the Republic of Chad, and numbers of infections have continued to increase. As in many countries where dracunculiasis is endemic, the campaign for eradication in Chad has focused intervention measures on interrupting transmission among humans, so infection in dogs jeopardizes eradication efforts. In this study, we used machine learning methods to identify demographic, geographic, and climatic factors associated with the presence of Guinea worm-infected dogs at the village level, and spatial clustering of dog cases regionally. A combination of demographic, geographic and climatic factors were important correlates of infection at the village level, but the importance of these factors varied between northern and southern populations of the parasite. At the larger village cluster level, the geographic position and climate of a village were most important. Some of our findings, including the importance of fishing villages and the difference in correlates between northern and southern villages can be used by researchers to guide additional data collection and by public health workers to better target eradication efforts. More generally, this work contributes to a broader understanding of the spatial patterning of multi-host infectious diseases of humans and animals.

Richards RL, Cleveland CA, Hall RJ, Tchindebet Ouakou P, Park AW, Ruiz-Tiben E, Weiss A, Yabsley MJ, Ezenwa VO. Identifying correlates of Guinea worm (Dracunculus medinensis) infection in domestic dog populations. PLOS Neglected Tropical Diseases. 2020 Sep 14;14(9):e0008620. https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0008620

Freshwater crabs (Decapoda: Pseudothelphusidae) increase rates of leaf breakdown in a neotropical headwater stream

  1. Freshwater crabs are the largest macroconsumers in many neotropical headwater streams, but few studies have examined their roles in ecosystem processes such as leaf litter breakdown. As omnivorous macroconsumers, freshwater crabs affect multiple trophic levels. They may directly increase leaf breakdown through fragmentation and consumption or indirectly decrease breakdown by consuming other macroinvertebrates, including shredders and detritivores.
  2. In a headwater stream in Monteverde, Costa Rica, we conducted an in‐stream experiment with 40 enclosures to quantify the effects of pseudothelphusid crabs on both leaf breakdown and macroinvertebrate colonisation of leaves. Half of the enclosures were randomly selected to contain two crabs (mean carapace width = 30 mm) and half were controls without crabs. We sampled mixed leaf packs from the enclosures on days 11, 19, 28, 34, and 42. We found the leaves of one species (Koanophyllon pittieri) almost completely decomposed by day 28 in both treatments (crab versus no crab). The other two leaf species (Meliosma idiopoda, Quercus brenesii) composed the remaining leaf mass at the end of the experiment.
  3. At 42 days, enclosures with crabs had faster rates of leaf breakdown than those without crabs (with crabs: k = −0.020; without crabs: k = −0.016; p = 0.034). This suggests that the magnitude of direct leaf breakdown by crabs, due to fragmentation, consumption, or manipulation of leaves, was greater than any indirect effects on leaf breakdown via crab consumption of other leaf‐consuming species.
  4. Macroinvertebrate composition based on taxa abundances or biomasses did not significantly differ between treatments (ANOSIM; p = 0.73 and p = 0.65, respectively). Shredder and detritivore abundances and biomasses increased significantly through time (ANOVA; p ≤ 0.001), but there was no evidence of an effect of crab presence (p > 0.2), nor were there significant interactions between crab presence and time (p > 0.3).
  5. This is one of the first studies to quantify the effects of pseudothelphusid freshwater crabs on leaf breakdown rates. Our results suggest that these crabs can play a significant role in detrital processing in neotropical headwater streams. This study has also demonstrated that short‐term enclosure experiments are useful in measuring in‐stream effects of crab activity on leaf breakdown.

Yang C, Wenger SJ, Rugenski AT, Wehrtmann IS, Connelly S, Freeman MC. Freshwater crabs (Decapoda: Pseudothelphusidae) increase rates of leaf breakdown in a neotropical headwater stream. Freshwater Biology. 2020;00:1–12. https://doi.org/10.1111/fwb.13524