Global analysis of seasonal changes in trematode infection levels reveals weak and variable link to temperature.

Seasonal changes in environmental conditions drive phenology, i.e., the annual timing of biological events ranging from the individual to the ecosystem. Phenological patterns and successional abundance cycles have been particularly well studied in temperate freshwater systems, showing strong and predictable synchrony with seasonal changes. However, seasonal successional changes in the abundance of parasites or their infection levels in aquatic hosts have not yet been shown to follow universal patterns. Here, using a compilation of several hundred estimates of spring-to-summer changes in infection by trematodes in their intermediate and definitive hosts, spanning multiple species and habitats, we test for general patterns of seasonal (temperature) driven changes in infection levels. The data include almost as many decreases in infection levels from spring to summer as there are increases, across different host types. Our results reveal that the magnitude of the spring-to-summer change in temperature had a weak positive effect on the concurrent change in prevalence of infection in first intermediate hosts, but no effect on the change in prevalence or abundance of infection in second intermediate or definitive hosts. This was true across habitat types and host taxa, indicating no universal effect of seasonal temperature increase on trematode infections. This surprising variation across systems suggests a predominance of idiosyncratic and species-specific responses in trematode infection levels, at odds with any clear phenological or successional pattern. We discuss possible reasons for the minimal and variable effect of seasonal temperature regimes, and emphasise the challenges this poses for predicting ecosystem responses to future climate change.

Some like it hotter: trematode transmission under changing temperature conditions.

Climate change-related increases in temperature will influence the interactions between organisms, including the infection dynamics of parasites in ecosystems. The distribution and transmission of parasites are expected to increase with warmer temperature, but to what extent this will affect closely related parasite taxa living in sympatry is currently impossible to predict, due to our extremely limited understanding of the interspecific variation in transmission potential among parasite species in changing ecosystems. Here, we analyse the transmission patterns of four trematode species from the New Zealand mudsnail Potamopyrgus antipodarum with different life cycles and transmission strategies under two temperature scenarios, simulating current and future warmer temperatures. In a comparative experimental study, we investigated the effects of temperature on the productivity, movement and survival of the parasites' transmission stages (cercariae) to quantify the net effect of temperature on their overall transmission potential. Our results show that increases in temperature positively affect cercarial transmission dynamics, yet these impacts varied considerably between the cercariae of different trematode species, depending on their host-searching behaviour. These different species-specific transmission abilities as well as the varying individual patterns of productivity, activity and longevity are likely to have far-reaching implications for disease dynamics in changing ecosystems, since increases in temperature can shift parasite community structure. Due to the parasites' capacity to regulate the functioning of whole ecological communities and their potential impact as disease agents, understanding these species-specific parasite transmission traits remains a fundamental requirement to predict parasite dynamics under changing environmental conditions.

Parasitological research in the molecular age.

New technological methods, such as rapidly developing molecular approaches, often provide new tools for scientific advances. However, these new tools are often not utilized equally across different research areas, possibly leading to disparities in progress between these areas. Here, we use empirical evidence from the scientific literature to test for potential discrepancies in the use of genetic tools to study parasitic vs non-parasitic organisms across three distinguishable molecular periods, the allozyme, nucleotide and genomics periods. Publications on parasites constitute only a fraction (<5%) of the total research output across all molecular periods and are dominated by medically relevant parasites (especially protists), particularly during the early phase of each period. Our analysis suggests an increasing complexity of topics and research questions being addressed with the development of more sophisticated molecular tools, with the research focus between the periods shifting from predominantly species discovery to broader theory-focused questions. We conclude that both new and older molecular methods offer powerful tools for research on parasites, including their diverse roles in ecosystems and their relevance as human pathogens. While older methods, such as barcoding approaches, will continue to feature in the molecular toolbox of parasitologists for years to come, we encourage parasitologists to be more responsive to new approaches that provide the tools to address broader questions.

Non-host organisms impact transmission at two different life stages in a marine parasite.

The potential for local biodiversity to 'dilute' infection risk has been shown to be particularly important in aquatic trematodes, where non-host organisms can feed on free-living infective stages (cercariae) and reduce transmission rates to target hosts. Non-host organisms could also impact transmission during other stages of the trematode life cycle. In Philophthalmus spp., cercariae encyst as metacercariae on external surfaces, where they remain exposed to the adverse effects of non-host organisms. In laboratory experiments, we tested the potential for a range of non-host organisms to (i) prey on cercariae, (ii) induce early (i.e., faster) encystment and (iii) prey on or destroy metacercariae. Our results show that intertidal anemones, and to a lesser extent clams, can consume substantial numbers of cercariae. However, we found no strong evidence that the presence of these predators causes cercariae to encyst faster as a way to escape from predation. We also found that grazing snails can reduce numbers of encysted metacercariae, either by eating or crushing them. Our findings add to the growing evidence that trematode transmission success can be strongly affected by the local diversity of non-host organisms. They also reinforce the notion that parasites are potentially important food items for many organisms, thus playing roles other than consumers in many food webs.

Parasites in space and time: a novel method to assess and illustrate host-searching behaviour of trematode cercariae.

The transmission from one host to another constitutes a challenging obstacle for parasites and is a key determinant of their fitness. Due to their complex life histories involving several different hosts, the free-living dispersal stages (cercariae) of digenean trematodes show a huge diversity in morphology and behaviour. On a finer scale, we still have an extremely limited understanding of the inter- and intraspecific variation in transmission strategies of many trematode species. Here, we present a novel method to study the movement patterns of cercariae of four New Zealand trematode species (Coitocaecum parvum, Maritrema poulini, Apatemon sp. and Aporocotylid sp. I.) via automated video tracking. This approach allows to quantify parameters otherwise not measurable and clearly illustrates the individual strategies of parasites to search for their respective target hosts. Cercariae that seek out an evasive fish target hosts showed higher swimming speeds (acceleration and velocity) and travelled further distances, compared with species searching for high-density crustacean hosts. Automated video tracking provides a powerful tool for such detailed analyses of parasites' host-searching strategies and can enhance our understanding of complex host-parasite interactions, ranging from parasite community structure to the transmission of potential disease agents.

Prior infections or defence priming: what determines the risk of trematode infections in amphipod hosts?

Inducible defences against parasites that are only activated when needed can mitigate the cost of immune or behavioural evasion of parasites. Priming of the immune system and activation of behavioural defences can follow exposure to cues associated with imminent infection risk. In contrast, prior infection can cause immune depression or leave the host with less energy to defend itself against further infections. We investigate the priming of anti-parasite defences and the effect of prior infections in the amphipod Paracalliope fluviatilis, the second intermediate host of the trematode Coitocaecum parvum. During experimental infections, amphipods that had been primed by exposure to chemical cues (from first intermediate snail hosts infected by C. parvum) of infection risk were not better at avoiding further infection than control amphipods. All amphipods showed the same swimming behaviour, whether or not they had been primed by chemical cues from infected snails, or whether or not they were in the presence of live infective stages. In contrast, regardless of whether or not they had been exposed to control water or chemical cues from infected snails, amphipods harbouring prior infections acquired in nature were significantly more likely to acquire new parasites under controlled conditions. These results suggest that the induction of defences via external cues associated with the threat of infection do not play a role in the amphipod's anti-parasite strategy. However, prior infections may pre-dispose a host to acquire further parasites, with consequences for the distribution of parasites among host individuals and the regulation of the host population.

Morphological and molecular data for larval stages of four species of Petasiger Dietz, 1909 (Digenea: Echinostomatidae) with an updated key to the known cercariae from the Palaearctic.

Large-tailed echinostomatid cercariae of the genus Petasiger Dietz, 1909 (Digenea: Echinostomatidae) from the planorbid snails Gyraulus albus (Müller) and Planorbis planorbis (L.) collected in Germany and the Czech Republic and metacercariae from Gasterosteus aculeatus L. (Gasterosteiformes: Gasterosteidae) collected in Canada are characterised morphologically and molecularly. The rediae, cercariae and metacercariae are described in detail and compared with the existing data on the larval stages of Petasiger spp. Comparative molecular analyses using 28S rDNA and nad1 mitochondrial sequences supported the distinct status of four species of Petasiger. Molecular and morphological evidence for their distinction and an updated key to the known large-tailed cercariae of Petasiger from the Palaearctic are provided.

Environmental parasitology: stressor effects on aquatic parasites.

Anthropogenic stressors are causing fundamental changes in aquatic habitats and to the organisms inhabiting these ecosystems. Yet, we are still far from understanding the diverse responses of parasites and their hosts to these environmental stressors and predicting how these stressors will affect host-parasite communities. Here, we provide an overview of the impacts of major stressors affecting aquatic ecosystems in the Anthropocene (habitat alteration, global warming, and pollution) and highlight their consequences for aquatic parasites at multiple levels of organisation, from the individual to the community level. We provide directions and ideas for future research to better understand responses to stressors in aquatic host-parasite systems.

Mussel memory: can bivalves learn to fear parasites?

Fear plays a crucial role in predator-prey interactions and can have cascading impacts on the structure of whole ecosystems. Comparable fear effects have recently been described for hosts and their parasites but our understanding of the underlying mechanisms remains limited by the lack of empirical examples. Here, we experimentally tested if bivalves Mytilus edulis can potentially 'learn to fear' the infective transmission stages (cercariae) of the trematode Himasthla elongata, and if experienced mussels change their parasite-avoidance behaviour accordingly. Our results show that previous experience with parasites, but not established infections, lead to a reduced filtration activity in mussels in the presence of cercariae compared to parasite-naive conspecifics. This reduction in filtration activity resulted in lower infection rates in mussels. Since parasite avoidance comes at the cost of lower feeding rates, mussels likely benefit from the ability to adjust their defence behaviour when infection risks are high. Overall, these dynamic processes of avoidance behaviour can be expected to play a significant role in regulating the bivalves' ecosystem engineering function in coastal habitats.

Bridging the gap: aquatic parasites in the One Health concept.

The One Health framework emphasizes the interconnectedness of humans, animals, and the environment but often remains focused on human health. Here we highlight how the evolutionary and ecological dynamics of aquatic parasites are crucial to our understanding of these connected health aspects, especially in the light of environmental changes.

Rare inventory of trematode diversity in a protected natural reserve.

In the face of ongoing habitat degradation and the biodiversity crisis, natural reserves are important refuges for wildlife. Since most free-living organisms serve as hosts to parasites, the diverse communities in protected areas can be expected to provide suitable habitats for a species-rich parasite fauna. However, to date, assessments of parasite diversity in protected nature reserves are rare. To expand our knowledge of parasite communities in natural habitats, we examined 1994 molluscs belonging to 15 species for trematode infections in a central European natural reserve. The parasitological examination revealed an overall prevalence of 17.3% and a total species richness of 40 trematode species. However, the parasite diversity and prevalence did not differ markedly from trematode communities in non-protected environments, which might be partly explained by a dilution effect caused by a high number of non-host organisms in our study system. The proportion of complex and long life cycles of parasites in the present study is high, indicating complex biotic interactions. We conclude that life cycle complexity, in addition to parasite diversity and trematode species richness, can provide valuable information on ecosystem health and should therefore be considered in future studies.

Temperature-parasite interaction: do trematode infections protect against heat stress?

Blue mussels (Mytilus edulis) are important ecosystem engineers along Atlantic coastlines, where they are regularly subjected to rapid changes in temperature during the transition between tides. Global climate change and more frequent extreme weather events are expected to intensify this thermal stress even further. These increases in temperatures will not only affect intertidal mussels directly but also increase transmission dynamics of their parasites. Together, the effects of rises in temperature and parasitism will likely result in higher pressure on M. edulis and their ability to perform vital ecosystem services. In a set of experiments, we tested the effects of infections with the trematode Himasthla elongata and high temperatures during low tide air-exposure. Overall, we hypothesised that temperature and parasite infection intensity would each have significant negative effects on M. edulis survival, and that both stressors together would have a synergistic detrimental impact. Overall, high temperature levels had a strong negative effect on mussel survival. However, our results revealed a surprisingly more complex picture in infected individuals. While moderate parasite loads and increased temperature showed additive negative effects on mussel survival, high parasite infection intensities appeared to nullify the detrimental effects of temperature stress on mussels. Under climate warming, these benefits of parasites might actually outweigh the costs of infection and prove beneficial. Overall, these results suggest that the interactions between host-parasite systems and their changing environment are much more complex than a simple additive effect of multiple stressors.

Hidden parasite diversity in a European freshwater system.

Parasites comprise a huge part of the biodiversity on earth. However, on a local scale, not much is known about their diversity and community structure. Here, we assess the diversity of larval trematode communities in an interconnected freshwater system of the River Ruhr in Germany and analyse how the parasites are spatially and temporally distributed in the ecosystem. A total of 5347 snail hosts belonging to six species revealed a highly diverse parasite fauna with 36 trematode species. More abundant snail species harboured more species-rich trematode faunas and communities, with the two dominant snail species, Radix auricularia and Gyraulus albus, accounting for almost 90% of the trematode diversity and harbouring spatially and temporally stable parasite communities. The results highlight the important role of stable keystone host populations for trematode transmission, structure and diversity. This local trematode diversity reveals information on definitive host occurrence and trophic interactions within ecosystems.

Cercarial Behavior Determines Risk of Predation.

The potential for local biodiversity to affect transmission success of parasites has been shown to be particularly important in trematodes, where non-host organisms can feed on and 'dilute' free-living infective stages (cercariae). Earlier studies have analyzed the effects of various predators on transmission stages of single trematode species, but not how cercariae of different species react to predation pressure. Here, we tested whether cercariae with different host-searching movement patterns show varying susceptibility to predation by non-host species with different feeding habits. For this study, we performed a set of predation experiments with 6 species of trematode cercariae (Coitocaecum parvum, Maritrema poulini, Apatemon sp., Telogaster opisthorchis, Plagiorchioid sp. I, and Aporocotylid sp. II) that represent 2 groups of host-searching behavior, free-swimming vs. bottom-dwelling, and 2 predators ( Sphaerium sp., Physa acuta) with distinct feeding modes, a filter feeder and a grazer. Our results show that cercarial susceptibility to predation is highly dependent on the interspecific interaction between dispersal behavior of cercariae and feeding behavior of non-host organisms: Filter feeders only diluted free-swimming cercarial stages, not bottom-dwelling ones; grazers on the other hand, had no effect on free-swimming cercariae but reduced bottom-dwelling cercariae in 1 trematode species. Our findings give further support to the hypothesis that the transmission dynamics of trematodes do not simply depend on local biodiversity but rather on the species-specific interactions between parasite transmission stages and free-living organisms in the ecosystem. This has important implications for disease dynamics in ecological communities (e.g., the parasites' infection success), and for ecosystem energetics, as cercariae constitute important food items.

Parasites Lost: Neglecting a Crucial Element in De-Extinction.

Bringing back iconic and beloved extinct species is a hot and intensely debated current topic. Yet, the parasites of de-extinction candidate species have remained largely overlooked in this debate. Here we point out the potentially far-reaching ecological impacts of bringing back extinct species without their parasites.

Parasite responses to pollution: what we know and where we go in 'Environmental Parasitology'.

Environmental parasitology deals with the interactions between parasites and pollutants in the environment. Their sensitivity to pollutants and environmental disturbances makes many parasite taxa useful indicators of environmental health and anthropogenic impact. Over the last 20 years, three main research directions have been shown to be highly promising and relevant, namely parasites as accumulation indicators for selected pollutants, parasites as effect indicators, and the role of parasites interacting with established bioindicators. The current paper focuses on the potential use of parasites as indicators of environmental pollution and the interactions with their hosts. By reviewing some of the most recent findings in the field of environmental parasitology, we summarize the current state of the art and try to identify promising ideas for future research directions. In detail, we address the suitability of parasites as accumulation indicators and their possible application to demonstrate biological availability of pollutants; the role of parasites as pollutant sinks; the interaction between parasites and biomarkers focusing on combined effects of parasitism and pollution on the health of their hosts; and the use of parasites as indicators of contaminants and ecosystem health. Therefore, this review highlights the application of parasites as indicators at different biological scales, from the organismal to the ecosystem.

GM-CSF priming of human monocytes is dependent on ERK1/2 activation.

The ability to augment monocyte functions such as TNF-alpha-producing capacities confers a high immunostimulating potential to GM-CSF. In the present investigation, the mechanism of the GMCSF-mediated enhancement of monocyte cytokine production was analysed with regard to the involvement of intracellular signalling pathways. GM-CSF primes human monocytes dose- and time-dependently for enhanced LPS-stimulated TNF-alpha synthesis. Pre-incubation with 10 ng/ml GM-CSF for 6 h before LPS stimulation (10 ng/ml) caused a 3.4 +/- 1.9-fold increase in TNF-alpha release compared to unprimed controls. This was associated with increased phosphorylation of IkappaBalpha and elevated nuclear levels of the NF-kappaB components p50 and p65 and NF-kappaB binding to DNA. LPS-induced AP-1 binding to DNA was also enhanced in GM-CSF-pre-incubated cells. GMCSF treatment also caused a slight increase in TLR4 expression on monocytes while CD14 expression remained unchanged. GM-CSF-priming was unaffected by inhibitors of p38 MAPK (SB203580) and lipoxygenase (NDGA). In contrast, the broad-spectrum tyrosine kinase inhibitor genistein and the MEK-1 inhibitor (PD98059) abrogated GM-CSF priming of TNF-alpha release and activation of both NF-kappaB and AP-1. It is concluded that a tyrosine kinase of the GM-CSF-triggered ERK1/2 pathway augments the LPS-induced NF-kappaB and AP-1 activation.

The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis.

Digenean trematodes are common and abundant in aquatic habitats and their free-living larvae, the cercariae, have recently been recognized as important components of ecosystems in terms of comprising a significant proportion of biomass and in having a potentially strong influence on food web dynamics. One strategy to enhance their transmission success is to produce high numbers of cercariae which are available during the activity peak of the next host. In laboratory experiments with 13 Lymnaea stagnalis snails infected with Trichobilharzia szidati the average daily emergence rate per snail was determined as 2,621 cercariae, with a maximum of 29,560. During a snail's lifetime this summed up to a mass equivalent of or even exceeding the snail's own body mass. Extrapolated for the eutrophic pond where the snails were collected, annual T. szidati biomass may reach 4.65 tons, a value equivalent to a large Asian elephant. Emission peaks were observed after the onset of illumination, indicating emission synchronizing with the high morning activities of the definitive hosts, ducks. However, high cercarial emission is possible throughout the day under favorable lightning conditions. Therefore, although bird schistosomes, such as T. szidati constitute only a fraction of the diverse trematode communities in the studied aquatic ecosystem, their cercariae can still pose a considerable risk for humans of getting cercarial dermatitis (swimmer's itch) due to the high number of cercariae emitted from infected snails.

Estimating the risk of swimmer's itch in surface waters - A case study from Lake Baldeney, River Ruhr.

Swimmer's itch is a zoonotic disease caused by certain digenean trematodes, in Europe most noticeably by bird schistosomes of the genus Trichobilharzia. These parasites require waterfowl and aquatic snails as final and intermediate hosts, respectively, to complete their life cycle. Swimmer's itch occurs when the free-swimming larvae emitted from snails, the cercariae, accidentally infect humans. Here the parasites cannot complete their life cycle but can cause allergic inflammatory responses of the skin. In the context of the joint BMBF project 'Sichere Ruhr' (Safe Ruhr), which evaluates the Ruhr River as a potential bathing water, the occurrence of the causative agents of swimmer's itch in Lake Baldeney was studied. A total of 1741 snails was examined for the presence of trematode infections, including bird schistosomes. Snails infected with Trichobilharzia spp. were found at three sampling locations but showed low overall prevalences (0.6-3.0%). Based on parasite and host biology, risk factors were evaluated and discussed in the context of the potential use of Lake Baldeney as a bathing water. Although bird schistosomes only constitute a fraction of the trematode diversity occurring in natural snail populations and show low prevalence, they still pose an infection risk due to the high emission rates of cercariae from individual snail hosts. A wide variety of often interacting biotic and abiotic factors, as well as personal behaviour have an effect on the likelihood and severity of a human infection. Based on these risk factors, a number of possible preventive actions aiming at the disruption of the life cycle, or personal protective measures can be suggested. While absolute protection is impossible (unless swimming in natural waters is altogether avoided) some preventive measures can reduce the risk of human infections.