Infection sequence alters disease severity—Effects of the sequential exposure of two larval trematodes to Polypedates cruciger tadpoles

Multiple pathogens coexist in nature, and hence, host species often encounter several pathogens simultaneously. The sequence in which the host encounters the parasites influences interactions between parasites and host pathology. Here, the effects of infection by two cercaria (larvae of trematodes) types, pleurolophocercous cercaria of Acanthostomum burminis and a furcocercous cercaria, on the tadpoles of common hourglass tree frog (Polypedates cruciger) were examined. Ten days posthatch, tadpoles (Gosner stage 27/28) were used for infection exposures. First, in a single infection each cercaria type was introduced to the tadpoles separately. Second, coinfection of the two cercaria was carried out by alternating the sequences of exposure. For all the experiments, appropriate controls were instituted. Tadpoles of all groups exposed to parasites had lower survival levels compared to controls. Among the four groups exposed, the highest survival was observed in the coinfection when furcocercous was introduced first (82.5%). The lowest survival was observed in the coinfection when the A. burminis cercaria was introduced first (65.0%). In the coinfections, when A. burminis was introduced prior to furcocercous, survival of the tadpoles was reduced by 17.0% compared to the exposures of furcocercous prior to A. burminis. Prior infection with A. burminis induced negative effect on the host with an increased infection severity, while prior infection with furcocercous had reduced infection severity than lone exposures. These results suggest that furcocercous infections can be beneficial for hosts challenged with A. burminis provided that A. burminis exposure occurs second. None of the treatments had an effect on the growth of the tadpoles, but lengthening of developmental period was observed in some exposures. All exposed tadpoles developed malformations which were exclusively axial—kyphosis and scoliosis. However, there was no difference in the number of malformed individuals in the single infection (19.0%–25.0%) compared to coinfection (20.0%–22.5%) or between coinfections. The results suggest that the sequence of parasite exposure affects host–parasite interactions and hence the disease outcomes. Understanding the effects of coinfection on disease outcomes for hosts provides insight into disease dynamics.     

Amphibian deformities and Ribeiroia infection: an emerging helminthiasis

Since their widespread appearance in the mid-1990s, malformed amphibians have evoked fear, as well as fascination within the scientific and public communities. Recent evidence from field and laboratory studies has implicated infection by a digenetic trematode--Ribeiroia ondatrae--as an important cause of such deformities. Ribeiroia spp. have a complex life cycle involving planorbid snails, amphibians and water birds. Under natural conditions, malformations might promote parasite transmission by increasing the susceptibility of infected amphibians to predation by definitive hosts. However, with respect to the recent outbreak of deformities, we suggest that exogenous agents (e.g. pesticides, nutrient run-off, introduced fishes) might be interacting with Ribeiroia, resulting in elevated infection levels, and we highlight the need for studies incorporating multiple stressor dynamics to further explore this problem.     

The potential for arms race and Red Queen coevolution in a protist host–parasite system

The dynamics and consequences of host–parasite coevolution depend on the nature of host genotype‐by‐parasite genotype interactions (G × G) for host and parasite fitness. G × G with crossing reaction norms can yield cyclic dynamics of allele frequencies (“Red Queen” dynamics) while G × G where the variance among host genotypes differs between parasite genotypes results in selective sweeps (“arms race” dynamics). Here, we investigate the relative potential for arms race and Red Queen coevolution in a protist host–parasite system, the dinoflagellate Alexandrium minutum and its parasite Parvilucifera sinerae. We challenged nine different clones of A. minutum with 10 clones of P. sinerae in a fully factorial design and measured infection success and host and parasite fitness. Each host genotype was successfully infected by four to ten of the parasite genotypes. There were strong G × Gs for infection success, as well as both host and parasite fitness. About three quarters of the G × G variance components for host and parasite fitness were due to crossing reaction norms. There were no general costs of resistance or infectivity. We conclude that there is high potential for Red Queen dynamics in this host–parasite system.     

Host species,and not environment,predicts variation in blood parasite prevalence,distribution, and diversity along a humidity gradient in northern South America

Environmental factors strongly influence the ecology and evolution of vector‐borne infectious diseases. However, our understanding of the influence of climatic variation on host–parasite interactions in tropical systems is rudimentary. We studied five species of birds and their haemosporidian parasites (Plasmodium and Haemoproteus) at 16 sampling sites to understand how environmental heterogeneity influences patterns of parasite prevalence, distribution, and diversity across a marked gradient in water availability in northern South America. We used molecular methods to screen for parasite infections and to identify parasite lineages. To characterize spatial heterogeneity in water availability, we used weather‐station and remotely sensed climate data. We estimated parasite prevalence while accounting for spatial autocorrelation, and used a model selection approach to determine the effect of variables related to water availability and host species on prevalence. The prevalence, distribution, and lineage diversity of haemosporidian parasites varied among localities and host species, but we found no support for the hypothesis that the prevalence and diversity of parasites increase with increasing water availability. Host species and host × climate interactions had stronger effects on infection prevalence, and parasite lineages were strongly associated with particular host species. Because climatic variables had little effect on the overall prevalence and lineage diversity of haemosporidian parasites across study sites, our results suggest that independent host–parasite dynamics may influence patterns in parasitism in environmentally heterogeneous landscapes.     

Experimental warming drives a seasonal shift in the timing of host‐parasite dynamics with consequences for disease risk

Multi‐species experiments are critical for identifying the mechanisms through which climate change influences population dynamics and community interactions within ecological systems, including infectious diseases. Using a host–parasite system involving freshwater snails, amphibians and trematode parasites, we conducted a year‐long, outdoor experiment to evaluate how warming affected net parasite production, the timing of infection and the resultant pathology. Warming of 3 °C caused snail intermediate hosts to release parasites 9 months earlier and increased infected snail mortality by fourfold, leading to decreased overlap between amphibians and parasites. As a result, warming halved amphibian infection loads and reduced pathology by 67%, despite comparable total parasite production across temperature treatments. These results demonstrate that climate–disease theory should be expanded to account for predicted changes in host and parasite phenology, which may often be more important than changes in total parasite output for predicting climate‐driven changes in disease risk.     

Genetic structure and host–parasite co‐divergence: evidence for trait‐specific local adaptation

Host–parasite co‐evolution can lead to genetic differentiation among isolated host–parasite populations and local adaptation between parasites and their hosts. However, tests of local adaptation rarely consider multiple fitness‐related traits although focus on a single component of fitness can be misleading. Here, we concomitantly examined genetic structure and co‐divergence patterns of the trematode Coitocaecum parvum and its crustacean host Paracalliope fluviatilis among isolated populations using the mitochondrial cytochrome oxidase I gene (COI). We then performed experimental cross‐infections between two genetically divergent host–parasite populations. Both hosts and parasites displayed genetic differentiation among populations, although genetic structure was less pronounced in the parasite. Data also supported a co‐divergence scenario between C. parvum and P. fluviatilis potentially related to local co‐adaptation. Results from cross‐infections indicated that some parasite lineages seemed to be locally adapted to their sympatric (home) hosts in which they achieved higher infection and survival rates than in allopatric (away) amphipods. However, local, intrinsic host and parasite characteristics (host behavioural or immunological resistance to infections, parasite infectivity or growth rate) also influenced patterns of host–parasite interactions. For example, overall host vulnerability to C. parvum varied between populations, regardless of parasite origin (local vs. foreign), potentially swamping apparent local co‐adaptation effects. Furthermore, local adaptation effects seemed trait specific; different components of parasite fitness (infection and survival rates, growth) responded differently to cross‐infections. Overall, data show that genetic differentiation is not inevitably coupled with local adaptation, and that the latter must be interpreted with caution in a multi‐trait context.     

Habitat selection by a threatened desert amphibian

Habitat degradation and fragmentation are major drivers of amphibian declines. The loss of environmental features that allow for movement between water sources may be particularly detrimental for amphibians in arid environments. Climate changes will increase the importance of microhabitats to amphibians. Enhancing areas to facilitate movement may be a necessary conservation strategy for many animal species that depend on wetlands, including federally threatened Chiricahua leopard frogs (Lithobates chiricahuensis). Habitat preferences of this frog species are not well understood. We sought to better understand fine‐scale habitat selection, to inform conservation of Chiricahua leopard frogs. We conducted our study on the Ladder Ranch, a privately owned working bison ranch in New Mexico, USA that supports a large proportion of the remaining Chiricahua leopard frogs in the state. We attached radio transmitters to 44 frogs during summer 2014. We located each frog daily for up to 8 weeks (median = 30 days). We assessed fine‐scale habitat selection by comparing characteristics at each frog location and a random location 5 m away using conditional logistic regression. Frogs preferred features that likely reduce desiccation, even after accounting for the presence of water. Frogs selected areas with more low‐lying cover, especially aquatic vegetation and woody debris, a tree overstory, and a mud substrate. We recommend managing potential movement corridors for Chiricahua leopard frogs by ensuring the presence of muddy creek bottoms, woody debris, riparian overstory, low‐lying ground cover, and pools. Microclimates created by these features seem especially valuable given warming temperatures and modified precipitation regimes, resulting in decreased surface water, soil moisture, and vegetation cover. Retaining or creating preferred habitat features and microclimates in areas between water sources may increase connectivity among isolated populations of Chiricahua leopard frogs and could improve persistence and recovery of other water‐obligate species in arid landscapes.     

Some (worms) like it hot: fish parasites grow faster in warmer water,and alter host thermal preferences

Elevated environmental temperatures associated with anthropogenic warming have the potential to impact host‐parasite interactions, with consequences for population health and ecosystem functioning. One way that elevated temperatures might influence parasite prevalence and intensity is by increasing life cycle completion rates. Here, we investigate how elevated temperatures impact a critical phase of the life cycle of the bird tapeworm Schistocephalus solidus – the growth of plerocercoid larvae in host fish (three‐spined sticklebacks Gasterosteus aculeatus). By 8 weeks post‐infection, plerocercoids recovered from experimentally infected sticklebacks held at 20 °C weighed on average 104.9 mg, with all exceeding 50 mg, the mass considered consistently infective to definitive hosts. In contrast, plerocercoids from sticklebacks held at 15 °C weighed on average 26.5 mg, with none exceeding 50 mg. As small increases in plerocercoid mass affect adult fecundity disproportionately in this species, enhanced plerocercoid growth at higher temperatures predicts dramatically increased output of infective parasite stages. Subsequent screening of thermal preferences of sticklebacks from a population with endemic S. solidus infection demonstrated that fish harbouring infective plerocercoids show significant preferences for warmer temperatures. Our results therefore indicate that parasite transmission might be affected in at least two ways under anthropogenic warming; by enhancing rates of parasite growth and development, and by increasing the likelihood of hosts being able to seek out proliferating warmer microhabitats. Furthermore, our results suggest the potential for positive feedback between parasite growth and host thermal preferences, which could dramatically increase the effects of even small temperature increases. We discuss the possible mechanisms underpinning our results, their likely ecological consequences and highlight key areas for further research.     

Extent, properties, and landscape setting of geographically isolated wetlands in urban southern New England watersheds

We assessed the extent and characteristics of geographically isolated wetlands (i.e., wetlands completely surrounded by upland) in a series of watersheds in the urban northeast US. We applied a previously developed index of urbanization to a sample of 10 watersheds selected at random from a set of 30 watersheds whose boundaries lay within the borders of Rhode Island, USA. The index of urbanization in our sample watersheds ranged over more than an order of magnitude and increased with increasing amount of urban land use in the watersheds (r ² = 0.51, F = 8.22, P = 0.02). The density of isolated wetlands in the watersheds averaged 1.93 ± 0.21 wetlands km⁻² and comprised 38.2 ± 1.77% of all wetlands. Isolated wetlands were smaller than those connected to other waters (non-isolated), and accounted for 6.01–16.5% of the total wetland area in the watersheds. The area of isolated wetlands as a percent of all wetland area significantly increased with increasing watershed urbanization (r ² = 0.62, F = 12.9, P = 0.007). Isolated wetlands were predominantly deciduous forested wetlands, and urban land cover in the 50 m buffer surrounding isolated wetlands was significantly higher than in the 50 m surrounding non-isolated wetlands. The proportion of urban land cover was greater in a 150 than a 50 m buffer surrounding the wetlands. Our results suggest that an increase in the index of urbanization of 50 will result in 7% of the watershed’s wetlands being lost from federal protection. These findings indicate that the process of urbanization, along with accompanying habitat fragmentation, may result in an increase in the vulnerability of wetlands to loss and degradation and therefore has implications for the management and conservation of geographically isolated wetlands.     

Pythons,parasites, and pests: anthropogenic impacts on Sarcocystis (Sarcocystidae) transmission in a multi‐host system

Parasites are essential components of ecosystems and can be instrumental in maintaining host diversity and populations; however, their role in trophic interactions has often been overlooked. Three apicomplexan parasite species of Sarcocystis (S. singaporensis, S. zamani, and S. villivillosi) use the reticulated python as their definitive hosts and several species within the Rattus genus as intermediate hosts, and they form a system useful for studying interactions between host–parasite and predator–prey relationships, as well as anthropogenic impacts on parasite transmission. Based on predictions from a 1998 survey, which detected an inverse relationship between urban development and Sarcocystis infection in Rattus, we tested the hypothesis that Sarcocystis transmission in Singapore will decrease over time due to anthropogenic activities. Despite a large proportion of the reticulated python diet consisting of Rattus species at all sizes of pythons, Sarcocystis infection rates decreased from 1998 to 2010. Pythons found in industrial areas had lower Sarcocystis infection rates, particularly in the western industrial area of Singapore Island. Average python size also decreased, with implications that we predict may disrupt host–parasite relationships. Anthropogenic activities such as habitat modification, fragmentation, and systematic removal and translocation of pythons have negative impacts on Sarcocystis transmission in Singapore, which in turn may augment pest rat populations. Trends observed may ultimately have negative impacts on human health and biodiversity in the region.     

Temporal Variation in Infection Prevalence by the Amphibian Chytrid Fungus in Three Species of Frogs at La Selva,Costa Rica

The emerging infectious disease chytridiomycosis, caused by the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), is implicated in widespread population declines, extirpations, and extinctions of amphibians throughout the world. In the Neotropics, most amphibian declines have occurred in cool mid‐ to high‐elevation sites (> 400 m asl), and it is hypothesized that high temperatures limit the growth of Bd in lowland tropical sites, despite few data available on the distribution of Bd in lowland forests. Here, we report the results of a 12‐mo pathogen surveillance program for three common species of frogs at a warm lowland site in northeastern Costa Rica. We combine standard non‐invasive skin swabbing techniques with a quantitative polymerase chain reaction assay to analyze the infection prevalence and Bd load across a 1‐yr period. Our data indicate an overall Bd infection rate of 6.1 percent, but prevalence varies from < 5 percent in warmer months to a peak of 34.7 percent in the coolest months of the year. Despite very little seasonal variation in temperature (< 4°C), our data indicate strong seasonal variation in the prevalence of Bd, with highest prevalence of infection in months with coolest air temperatures. While it has been suggested that Bd is primarily a riparian fungus, we find no difference in prevalence of infection among our species despite considerable differences in affiliation of these species with water. Our study provides further evidence that infection by Bd is regulated by temperature and shows that warm temperatures in lowland forests may restrict, but not prevent, infection by Bd.     

Combined effects of salinity and infectious disease on Daphnia dentifera at multiple scales

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The right response at the right time: Exploring helminth immune modulation in sticklebacks by experimental coinfection

Parasites are one of the strongest selective agents in nature. They select for hosts that evolve counter‐adaptive strategies to cope with infection. Helminth parasites are special because they can modulate their hosts’ immune responses. This phenomenon is important in epidemiological contexts, where coinfections may be affected. How different types of hosts and helminths interact with each other is insufficiently investigated. We used the three‐spined stickleback (Gasterosteus aculeatus) – Schistocephalus solidus model to study mechanisms and temporal components of helminth immune modulation. Sticklebacks from two contrasting populations with either high resistance (HR) or low resistance (LR) against S. solidus, were individually exposed to S. solidus strains with characteristically high growth (HG) or low growth (LG) in G. aculeatus. We determined the susceptibility to another parasite, the eye fluke Diplostomum pseudospathaceum, and the expression of 23 key immune genes at three time points after S. solidus infection. D. pseudospathaceum infection rates and the gene expression responses depended on host and S. solidus type and changed over time. Whereas the effect of S. solidus type was not significant after three weeks, T regulatory responses and complement components were upregulated at later time points if hosts were infected with HG S. solidus. HR hosts showed a well orchestrated immune response, which was absent in LR hosts. Our results emphasize the role of regulatory T cells and the timing of specific immune responses during helminth infections. This study elucidates the importance to consider different coevolutionary trajectories and ecologies when studying host‐parasite interactions.     

Cryptic diversity,reproductive isolation and cytoplasmic incompatibility in a classic biological control success story

Molecular genetics and symbiont diagnostics have revolutionized our understanding of insect species diversity, and the transformative effects of bacterial symbionts on host life history. Encarsia inaron is a parasitoid wasp that has been shown to harbour two bacterial endosymbionts, Wolbachia and Cardinium. Known then as E. partenopea, it was introduced to the USA in the late 1980s from populations collected in Italy and Israel for the biological control of an ornamental tree pest, the ash whitefly, Siphoninus phillyreae. We studied natural populations from sites in the USA, the Mediterranean and the Middle East as well as from a Cardinium‐infected laboratory culture established from Italy, with the aims of characterizing these populations genetically, testing reproductive isolation, determining symbiont infection status in their native and introduced range, and determining symbiont role. The results showed that the two Encarsia populations introduced to the USA are genetically distinct, reproductively isolated, have different symbionts and different host–symbiont interactions, and can be considered different biological species. One (‘E. inaron’) is doubly infected by Wolbachia and Cardinium, while only Cardinium is present in the other (‘E. partenopea’). The Cardinium strains in the two species are distinct, although closely related, and crossing tests indicate that the Cardinium infecting ‘E. partenopea’ induces cytoplasmic incompatibility. The frequency of symbiont infection found in the native and introduced range of these wasps was similar, unlike the pattern seen in some other systems. These results also lead to a retelling of a successful biological control story, with several more characters than had been initially described.     

Sitting ducklings: Timing of hatch,nest departure,and predation risk for dabbling duck broods

For ground‐nesting waterfowl, the timing of egg hatch and duckling departure from the nest may be influenced by the risk of predation at the nest and en route to wetlands and constrained by the time required for ducklings to imprint on the hen and be physically able to leave the nest. We determined the timing of hatch, nest departure, and predation on dabbling duck broods using small video cameras placed at the nests of mallard (Anas platyrhynchos; n = 26), gadwall (Mareca strepera; n = 24), and cinnamon teal (Anas cyanoptera; n = 5). Mallard eggs began to hatch throughout the day and night, whereas gadwall eggs generally started to hatch during daylight hours (mean 7.5 hr after dawn). Among all species, duckling departure from the nest occurred during daylight (98%), and 53% of hens typically left the nest with their broods 1–4 hr after dawn. For mallard and gadwall, we identified three strategies for the timing of nest departure: (a) 9% of broods left the nest the same day that eggs began to hatch (6–12 hr later), (b) 81% of broods left the nest the day after eggs began to hatch, and (c) 10% of broods waited 2 days to depart the nest after eggs began to hatch, leaving the nest just after the second dawn (27–42 hr later). Overall, eggs were depredated at 10% of nests with cameras in the 2 days prior to hatch and ducklings were depredated at 15% of nests with cameras before leaving the nest. Our results suggest that broods prefer to depart the nest early in the morning, which may best balance developmental constraints with predation risk both at the nest and en route to wetlands.     

Long‐term monitoring of tropical alpine habitat change,Andean anurans,and chytrid fungus in the Cordillera Vilcanota,Peru: Results from a decade of study

The Cordillera Vilcanota in southern Peru is the second largest glacierized range in the tropics and home to one of the largest high‐alpine lakes, Sibinacocha (4,860 m). Here, Telmatobius marmoratus (marbled water frog), Rhinella spinulosa (Andean toad), and Pleurodema marmoratum (marbled four‐eyed frog) have expanded their range vertically within the past century to inhabit newly formed ponds created by ongoing deglaciation. These anuran populations, geographically among the highest (5,200–5,400 m) recorded globally, are being impacted by the chytrid fungus Batrachochytrium dendrobatidis (Bd), and the disease it causes, chytridiomycosis. In this study, we report results from over a decade of monitoring these three anuran species, their habitat, and Bd infection status. Our observations reveal dynamic changes in habitat including ongoing rapid deglaciation (18.4 m/year widening of a corridor between retreating glaciers from 2005 to 2015), new pond formation, changes in vegetation in amphibian habitat, and widespread occurrence of Bd in amphibians in seven sites. Three of these sites have tested positive for Bd over a 9‐ to 12‐year period. In addition, we observed a widespread reduction in T. marmoratus encounters in the Vilcanota in 2008, 2009, and 2012, while encounters increased in 2013 and 2015. Despite the rapid and dynamic changes in habitat under a warming climate, continued presence of Bd in the environment for over a decade, and a reduction in one of three anuran species, we document that these anurans continue to breed and survive in this high Andean environment. High variability in anuran encounters across sites and plasticity in these populations across habitats, sites, and years are all factors that could favor repopulation postdecline. Preserving the connectivity of wetlands in the Cordillera Vilcanota is therefore essential in ensuring that anurans continue to breed and adapt as climate change continues to reshape the environment.