Related to this, another key component was his demonstration that high levels of aquatic eutrophication promoted a greater intensity and prevalence of Ribeiroia infection in amphibians, thereby ...identifying a potential environmental perturbation contributing to malformation increases. Since beginning his faculty position at the University of Colorado Boulder in 2007, Pieter has continued to explore many aspects of parasite ecology in freshwater habitats, particularly employing amphibians and trematodes as a highly successful model system with which to push forward our understanding of fundamental processes at the level of the individual, population, community, and ecosystem. ... Pieter and his lab have provided estimates of those too, but I can barely highlight work from 2013, let alone other years! In support of his wide-ranging research program that has employed laboratory, mesocosm, and field approaches (including the sampling of ~400 unique ponds in California for over 20 years now for >1,000 distinct pond by year combinations), Pieter has also been highly successful at securing funding, garnering almost 3 million dollars as the lead P.I. from a variety of sources that include the National Science Foundation (NSF), the National Fish and Wildlife Foundation, National Geographic, the Colorado Division of Wildlife, and the David and Lucile Packard Foundation, as well as participating as a co-applicant on numerous other grants. ...Pieter has helped to cultivate a wide appreciation of parasites by his activities to engage the broader public and future generations of researchers.
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Infected hosts are exposed to many environmental stressors that must be taken into account in order to determine the importance of disease, as various combinations can interact in unpredictable ways. ...Here, northern leopard frog (
Rana pipiens
) tadpoles, a species in decline, were exposed to stressors singly or in combination. Stressors included infection by
Echinostoma trivolvis
(a trematode parasite), exposure to predator chemical cues (larval dragonflies), and exposure to varying concentrations of the herbicide atrazine. Parasitism decreased survival only in combination with exposure to 3 μg/L atrazine, with a negative interaction observed for mass as well. Similarly, a negative interaction of parasitism and predation on survival occurred. However, atrazine exposure alone negatively affected the survival, mass, and developmental stage of tadpoles. These results indicate that certain stressor combinations are particularly deleterious for young parasitized tadpoles. Notably, very common low-intensity parasite infection can be particularly harmful in certain situations. Such negative impacts on larval amphibians in certain scenarios may contribute to ongoing amphibian population declines, emphasizing that the combination of environmental stressors must be considered when evaluating the general role of disease in species extinctions.
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Approaches based on organismal DNA found in the environment (eDNA) have become increasingly utilized for ecological studies and biodiversity inventories as an alternative to traditional field survey ...methods. Such DNA-based techniques have largely been used to establish the presence of free-living organisms, but have much potential for detecting and quantifying infectious agents in the environment, which is necessary to evaluate disease risk. We developed an eDNA method to examine the distribution and abundance of the trematode
Ribeiroia ondatrae
, a pathogenic parasite known to cause malformations in North American amphibians. In addition to comparing this eDNA approach to classical host necropsy, we examined the detectability of
R. ondatrae
in water samples subject to different degradation conditions (time and temperature). Our test exhibited high specificity and sensitivity to
R. ondatrae
, capable of detecting as little as 14 fg (femtograms) of this parasite's DNA (1/2500th of a single infectious stage) from field water samples. Compared to our results from amphibian host necropsy, quantitative PCR was ~90% concordant with respect to
R. ondatrae
detection from 15 field sites and was also a significant predictor of host infection abundance. DNA was still detectable in lab samples after 21 days at 25°C, indicating that our method is robust to field conditions. By comparing the advantages and disadvantages of eDNA vs. traditional survey methods for determining pathogen presence and abundance in the field, we found that the lower cost and effort associated with eDNA approaches provide many advantages. The development of alternative tools is critical for disease ecology, as wildlife management and conservation efforts require reliable establishment and monitoring of pathogens.
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Given the threat presented by parasites and pathogens, insects employ various defences to protect themselves against infection, including chemical secretions. The red flour beetle Tribolium castaneum ...releases a secretion containing the benzoquinones methyl-1,4-benzoquinone (MBQ) and ethyl-1,4-benzoquinone (EBQ) into the environment. These compounds have known antimicrobial effects; however, their role in defence against macroparasites is not known. Entomopathogenic nematodes, such as Steinernema carpocapsae, present a serious threat to insects, with successful infection leading to death. Thus, quinone-containing secretions may also aid in host defence. We tested how exposure to the individual components of this quinone secretion, as well as a mix at naturally-occurring proportions, affected the survival and thrashing behaviour of S. carpocapsae, as well as their virulence to a model host (Galleria mellonella). Exposure to high concentrations of MBQ and EBQ, as well as the quinone mix, significantly increased nematode death but did not consistently reduce thrashing, which would otherwise be expected given their toxicity. Rather, quinones may act as a host cue to S. carpocapsae by triggering increased activity. We found that exposure to quinones for 24 or 72 hours did not reduce nematode virulence, and surviving nematodes remained infective after non-lethal exposure. Our results indicate that quinone secretions likely serve as a defence against multiple infection threats by reducing S. carpocapsae survival, but further research is required to contextualize their roles by testing against other nematodes, as well as other helminths using insects as hosts.
The negative effects of abiotic and biotic stressors on animal condition, physiology, behaviour, and fitness have become increasingly recognized, making it critical to understand how these may be ...mitigated, such as through diet. When consumed, dietary antioxidants (secondary metabolites produced by plants) provide protection from oxidative damage that can result from exposure to stressors. We examined the effects of dietary antioxidants (β-carotene and vitamin E) on the ability of Lithobates sylvaticus (wood frog) tadpoles to overcome the detrimental effects imposed by two common environmental stressors – exposure to the herbicide atrazine or infection by a pathogenic helminth parasite (Echinostoma trivolvis). Tadpoles which were fed high concentrations of either vitamin E or β-carotene had a greater immune response compared to those given trace diets of either compound as measured by circulating white blood cells and a phytohemaglutination assay (PHA). Similarly, tadpoles in the herbicide and parasitism treatments that were given trace antioxidant diets had significant weight loss, whereas those consuming high levels of vitamin E or β-carotene did not. Our results suggest that dietary antioxidants, specifically β-carotene and vitamin E, have a positive effect on tadpole immune systems and overall condition that likely allows them to better cope with natural stressors, with potential implications for their foraging behaviour.
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Given their sheer cumulative biomass and ubiquitous presence, parasites are increasingly recognized as essential components of most food webs. Beyond their influence as consumers of host tissue, many ...parasites also have free-living infectious stages that may be ingested by non-host organisms, with implications for energy and nutrient transfer, as well as for pathogen transmission and infectious disease dynamics. This has been particularly well-documented for the cercaria free-living stage of digenean trematode parasites within the Phylum Platyhelminthes. Here, we aim to synthesize the current state of knowledge regarding cercariae consumption by examining: (a) approaches for studying cercariae consumption; (b) the range of consumers and trematode prey documented thus far; (c) factors influencing the likelihood of cercariae consumption; (d) consequences of cercariae consumption for individual predators (e.g. their viability as a food source); and (e) implications of cercariae consumption for entire communities and ecosystems (e.g. transmission, nutrient cycling and influences on other prey). We detected 121 unique consumer-by-cercaria combinations that spanned 60 species of consumer and 35 trematode species. Meaningful reductions in transmission were seen for 31 of 36 combinations that considered this; however, separate studies with the same cercaria and consumer sometimes showed different results. Along with addressing knowledge gaps and suggesting future research directions, we highlight how the conceptual and empirical approaches discussed here for consumption of cercariae are relevant for the infectious stages of other parasites and pathogens, illustrating the use of cercariae as a model system to help advance our knowledge regarding the general importance of parasite consumption.
Many temperate freshwater habitats are at risk for contamination by run-off associated with the application of road de-icing salts. Elevated salinity can have various detrimental effects on ...freshwater organisms, including greater susceptibility to infection by parasites and pathogens. However, to better understand the net effects of road salt exposure on host-parasite dynamics, it is necessary to consider the impacts on free-living parasite infectious stages, such as the motile aquatic cercariae of trematodes. Here, we examined the longevity and activity of cercariae from four different freshwater trematodes (Ribeiroia ondatrae, Echinostoma sp., Cephalogonimus sp. and an unidentified strigeid-type) that were exposed to road salt at five different environmentally relevant concentrations (160, 360, 560, 760 and 960 mg/ml of sodium chloride). Exposure to road salt had minimal detrimental effects, with cercariae activity and survival often greatest at intermediate concentrations. Only the cercariae of Cephalogonimus sp. showed reduced longevity at the highest salt concentration, with those of both R. ondatrae and the unidentified strigeid-type exhibiting diminished activity, indicating interspecific variation in response. Importantly, cercariae seem to be relatively unaffected by salt concentrations known to increase infection susceptibility in some of their hosts. More studies will be needed to examine this potential dichotomy in road salt effects between hosts and trematodes, including influences on parasite infectivity.
Abstract
Anguillid eels were once considered to be the classic example of catadromy. However, alternative life cycles have been reported, including skipping the freshwater phase and habitat shifting ...between fresh, brackish, and saltwater throughout the growth phase. There is a lack of knowledge regarding these alternate life strategies, for example, the proportion of individuals in the population that adopt them compared to classic catadromy. We provide a description of these alternate life cycle strategies in temperate anguillids, their possible drivers, and the methods available to investigate them. These methods (lethal and non-lethal), include otolith microchemistry, fatty acid and stable isotope analyses, parasite identification, blood transcriptomics, and electronic tags. We argue that since the current management framework for the European eel and other temperate eels is based mainly on the freshwater component of the population, it ignores eels growing in saline waters. Many of the factors that are thought to be responsible for the precipitous decline of the eel population are more prevalent in freshwater systems. Therefore, the contribution of saline eels may be more important than currently estimated. The habitat-shifting ability of eels may be all the more crucial for the persistence and recovery of those species that are endangered.
The range of hosts used by a parasite is influenced by macro-evolutionary processes (host switching, host–parasite co-evolution), as well as ‘encounter filters’ and ‘compatibility filters’ at the ...micro-evolutionary level driven by host/parasite ecology and physiology. Host specialization is hypothesized to result in trade-offs with aspects of parasite life history (e.g. reproductive output), but these have not been well studied. We used previously published data to create models examining general relationships among host specificity and important aspects of life history and reproduction for nematodes parasitizing animals. Our results indicate no general trade-off between host specificity and the average pre-patent period (time to first reproduction), female size, egg size, or fecundity of these nematodes. However, female size was positively related to egg size, fecundity, and pre-patent period. Host compatibility may thus not be the primary determinant of specificity in these parasitic nematodes if there are few apparent trade-offs with reproduction, but rather, the encounter opportunities for new host species at the micro-evolutionary level, and other processes at the macro-evolutionary level (i.e. phylogeny). Because host specificity is recognized as a key factor determining the spread of parasitic diseases understanding factors limiting host use are essential to predict future changes in parasite range and occurrence.
Habitat attributes are known to influence infectious diseases such as those caused by parasites, but most studies have only considered single host and (or) parasite taxa, making it difficult to ...assess which features may be of general importance and to predict how alterations could affect disease dynamics. We examined infection with trematode (flatworm) parasites in two commonly co-occurring host taxa (larval amphibians and larval odonates (dragonflies and damselflies)) to investigate links with landscape-level features, including agricultural activity. We also assessed pond community composition with respect to the abundance and richness of aquatic arthropods known to prey upon tadpoles and (or) free-swimming trematode infectious stages. Larval amphibians from agricultural sites were most likely to be parasitized but had lower infection intensities, and infected hosts were positively associated with increasing distance to the nearest forest habitat, but negatively with road distance. The opposite was observed for larval odonate infection status; however, probability and intensity of parasitism in both host taxa was negatively associated with greater predatory arthropod abundance, consistent with the “dilution effect” of biodiversity on infectious diseases. Our approach demonstrates the importance of considering multiple host taxa when studying habitat links to diseases, and future studies incorporating even greater diversity will be needed.
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