New insights into avian malaria infections in New Zealand seabirds.

The past few years have been marked by a drastic increase in pathogen spillover events. However, the extent and taxonomic range at which these events take place remain as crucial unanswered questions in many host-pathogen systems. Here, we take advantage of opportunistically sampled bird carcasses from the South Island of New Zealand, with the aim of identifying Plasmodium spp. infections in native and endemic New Zealand seabird species. In total, six samples from five bird species were positive for avian malaria, including four of which were successfully sequenced and identified as Plasmodium matutinum LINN1 lineage. These results provide new Plasmodium infection records in seabirds, including the first documented case in Procellariiformes in New Zealand, highlighting the potential disease risk to these species.

Effects of forest loss and fragmentation on bat-ectoparasite interactions.

Human land use causes habitat loss and fragmentation, influencing host-parasite associations through changes in infestation rates, host mortality and possibly local extinction. Bat-ectoparasite interactions are an important host-parasite model possibly affected by such changes, as this system acts as both reservoirs and vectors of several pathogens that can infect different wild and domestic species. This study aimed to assess how the prevalence and abundance of bat ectoparasites respond to forest loss, fragmentation, and edge length. Bats and ectoparasites were sampled at twenty sites, forming a gradient of forest cover, in southwestern Brazil during two wet (2015 and 2016) and two dry (2016 and 2017) seasons. Effects of landscape metrics on host abundance as well as parasite prevalence and abundance were assessed through structural equation models. Nine host-parasite associations provided sufficient data for analyses, including one tick and eight flies on four bat species. Forest cover positively influenced the prevalence or abundance of three fly species, but negatively influenced one fly and the tick species. Prevalence or abundance responded positively to edge length for three fly species, and negatively for the tick. In turn, number of fragments influenced the prevalence or abundance of four fly species, two positively and two negatively. Our results support species-specific responses of ectoparasites to landscape features, and a tendency of host-generalist ticks to benefit from deforestation while most host-specialist flies are disadvantaged. Differences in host traits and abundance, along with parasite life cycles and environmental conditions, are possible explanations to our findings.

Battle of the sexes: analysis of sex bias in host use and reporting practices in parasitological experiments.

Experimental approaches are among the most powerful tools available to biologists, yet in many disciplines their results have been questioned due to an underrepresentation of female animal subjects. In parasitology, experiments are crucial to understand host-parasite interactions, parasite development, host immune responses, as well as the efficacy of different control methods. However, distinguishing between species-wide and sex-specific effects requires the balanced inclusion of both male and female hosts in experiments and the reporting of results for each sex separately. Here, using data from over 3600 parasitological experiments on helminth-mammal interactions published in the past four decades, we investigate patterns of male versus female subject use and result reporting practices in experimental parasitology. We uncover multiple effects of the parasite taxon used, the type of host used (rats and mice for which subject selection is fully under researcher control versus farm animals), the research subject area and the year of publication, on whether host sex is even specified, whether one or both host sexes have been used (and if only one then which one), and whether the results are presented separately for each host sex. We discuss possible reasons for biases and unjustifiable selection of host subjects, and for poor experimental design and reporting of results. Finally, we make some simple recommendations for increased rigour in experimental design and to reset experimental approaches as a cornerstone of parasitological research.

Preliminary Investigation of Schmalhausen's Law in a Directly Transmitted Pathogen Outbreak System.

The past few decades have been marked by drastic modifications to the landscape by anthropogenic processes, leading to increased variability in the environment. For populations that thrive at their distributional boundaries, these changes can affect them drastically, as Schmalhausen's law predicts that their dynamics are more likely to be susceptible to environmental variation. Recently, this evolutionary theory has been put to the test in vector-borne disease emergences systems, and has been demonstrated effective in predicting emergence patterns. However, it has yet to be tested in a directly transmitted pathogen. Here, we provide a preliminary test of Schmalhausen's law using data on Marburg virus outbreaks originating from spillover events. By combining the two important aspects of Schmalhausen's law, namely climatic anomalies and distance to species distributional edges, we show that Marburgvirus outbreaks may support an aspect of this evolutionary theory, with distance to species distributional edge having a weak influence on outbreak size. However, we failed to demonstrate any effect of climatic anomalies on Marburgvirus outbreaks, arguably related to the lack of importance of these variables in directly transmitted pathogen outbreaks. With increasing zoonotic spillover events occurring from wild species, we highlight the importance of considering ecological variability to better predict emergence patterns.

Footprint of war: integrating armed conflicts in disease ecology.

War is an understudied and yet significant contributor to disease outbreaks, necessitating approaches incorporating conflicts into disease studies. We discuss mechanisms by which war affects disease dynamics, and supply an illustrative example. Lastly, we provide relevant data sources and pathways for incorporating metrics of armed conflict into disease ecology.

Metatranscriptomic Comparison of Viromes in Endemic and Introduced Passerines in New Zealand.

New Zealand/Aotearoa has many endemic passerine birds vulnerable to emerging infectious diseases. Yet little is known about viruses in passerines, and in some countries, including New Zealand, the virome of wild passerines has been only scarcely researched. Using metatranscriptomic sequencing we characterised the virome of New Zealand endemic and introduced species of passerine. Accordingly, we identified 34 possible avian viruses from cloacal swabs of 12 endemic and introduced bird species not showing signs of disease. These included a novel siadenovirus, iltovirus, and avastrovirus in the Eurasian blackbird (Turdus merula, an introduced species), song thrush (Turdus philomelos, introduced) and silvereye/tauhou (Zosterops lateralis, introduced), respectively. This is the first time novel viruses from these genera have been identified in New Zealand, likely reflecting prior undersampling. It also represents the first identification of an iltovirus and siadenovirus in blackbirds and thrushes globally. These three viruses were only found in introduced species and may pose a risk to endemic species if they were to jump species boundaries, particularly the iltoviruses and siadenoviruses that have a prior history of disease associations. Further virus study and surveillance are needed in New Zealand avifauna, particularly in Turdus populations and endemic species.

Infection patterns and new definitive host records for New Zealand gordiid hairworms (phylum Nematomorpha).

Some parasites modify the phenotype of their host in order to increase transmission to another host or to an environment suitable for reproduction. This phenomenon, known as host manipulation, is found across many parasite taxa. Freshwater hairworms are known for the behavioural changes they cause in their terrestrial arthropod hosts, increasing their likelihood of entering water to exit the host and reproduce. Understanding how infected arthropods move around in the natural environment could help uncover alterations in spatial distribution or movement induced by hairworms in their terrestrial definitive hosts. Moreover, few hairworm-host records exist for New Zealand, so any additional record could help elucidate their true host specificity. Here, we investigated whether infected terrestrial arthropods were more likely to approach streams in two subalpine communities of invertebrates, using a spatial grid of specialised pitfall traps. Although hairworm infection could not explain the movements of arthropod hosts near streams, we found several new host records for hairworms, including the first records for the recently described Gordionus maori. We also found some new host-parasite associations for mermithid nematodes. These records show that the host specificity of hairworms is quite low, suggesting that their diversity and distribution may be greater than what is currently known for New Zealand.

Anthropogenic landscape alteration promotes higher disease risk in wild New Zealand avian communities.

Anthropogenic changes can have dramatic effects on wild populations. Moreover, by promoting the emergence of vector-borne diseases in many ecosystems, those changes can lead to local extinction of native wildlife. One of those diseases, avian malaria, has been shown to be on the rise in New Zealand, threatening native bird species that are among the most extinction-prone in the world. It is thus of prime importance to better understand the potential cascading effects that anthropogenic modifications have on those fragile species. Here, we aim to test how long-lasting modification to regional environmental filters can subsequently alter local biotic filters, in turn promoting the emergence of avian malaria in New Zealand avian communities. To this end, we used Bayesian structural equation modelling to unravel the drivers of disease emergence within the complex interplay between landscape and local species pools. We show that altered landscape, quantified through a lower enhanced vegetation index, leads to more infections in Turdus spp. and modification in avian community composition, potentially raising the probability of infection for other species in the community. In addition, we show that climatic variables associated with the presence of vectors play a predominant role in shaping the regional pattern of avian malaria occurrence. Our results suggest long-lasting impacts of anthropogenic changes on regional environmental filters and demonstrate that conservation efforts should align toward restoring the landscape to prevent further emergence of infectious diseases in wild ecosystems.

Host specificity and the reproductive strategies of parasites.

Environmental stability can have profound impacts on life history trait evolution in organisms, especially with respect to development and reproduction. In theory, free-living species, when subjected to relatively stable and predictable conditions over many generations, should evolve narrow niche breadths and become more specialized. In parasitic organisms, this level of specialization is reflected by their host specificity. Here, we tested how host specificity impacts the reproductive strategies of parasites, a subject seldomly addressed for this group. Through an extensive review of the literature, we collated a worldwide dataset to predict, through Bayesian multilevel modelling, the effect of host specificity on the reproductive strategies of parasitic copepods of fishes or corals. We found that copepods of fishes with low host specificity (generalists) invest more into reproductive output with larger clutch sizes, whereas generalist copepods of corals invest less into reproductive output with smaller clutch sizes. The differences in host turnover rates through an evolutionary timescale could explain the contrasting strategies across species observed here, which should still favour the odds of parasites encountering and infecting a host. Ultimately, the differences found in this study reflect the unique evolutionary history that parasites share both intrinsically and extrinsically with their hosts.

Building a comprehensive phylogenetic framework in disease ecology.

Disease spillover can have dramatic consequences in multispecies systems, potentially leading to the emergence of zoonoses. To better understand disease emergence patterns, an approach encompassing species relatedness metrics is needed. We show that integrating phylogenetic information in disease ecology is still lagging, and we highlight potential solutions to solve this problem.

The rise of big data in disease ecology.

Big data have become readily available to explore patterns in large-scale disease ecology. However, the rate at which these public databases are exploited remains unknown. We highlight trends in big data usage in disease ecology during the past decade and encourage researchers to integrate big data into their study framework.

The people vs science: can passively crowdsourced internet data shed light on host-parasite interactions?

Every internet search query made out of curiosity by anyone who observed something in nature, as well as every photo uploaded to the internet, constitutes a data point of potential use to scientists. Researchers have now begun to exploit the vast online data accumulated through passive crowdsourcing for studies in ecology and epidemiology. Here, we demonstrate the usefulness of iParasitology, i.e. the use of internet data for tests of parasitological hypotheses, using hairworms (phylum Nematomorpha) as examples. These large worms are easily noticeable by people in general, and thus likely to generate interest on the internet. First, we show that internet search queries (collated with Google Trends) and photos uploaded to the internet (specifically, to the iNaturalist platform) point to parts of North America with many sightings of hairworms by the public, but few to no records in the scientific literature. Second, we demonstrate that internet searches predict seasonal peaks in hairworm abundance that accurately match scientific data. Finally, photos uploaded to the internet by non-scientists can provide reliable data on the host taxa that hairworms most frequently parasitize, and also identify hosts that appear to have been neglected by scientific studies. Our findings suggest that for any parasite group likely to be noticeable by non-scientists, information accumulating through internet search activity, photo uploads, social media or any other format available online, represents a valuable source of data that can complement traditional scientific data sources in parasitology.

iParasitology: Mining the Internet to Test Parasitological Hypotheses.

Digital data (internet queries, page views, social media posts, images) are accumulating online at increasing rates. Tools for compiling these data and extracting their metadata are now readily available. We highlight the possibilities and limitations of internet data to reveal patterns in host-parasite interactions and encourage parasitologists to embrace iParasitology.

Does ecological release from distantly related species affect phenotypic divergence in brook charr?

Ecological opportunity occurs when a resource becomes available through a decrease of interspecific competition and another species colonizes the vacant niche through phenotypic plasticity and intraspecific competition. Brook charr exhibit a resource polymorphism in some Canadian Shield lakes, where a littoral ecotype feeds mainly on zoobenthos and a pelagic ecotype feeds mostly on zooplankton. The objectives of this study were to test that (i) resource polymorphism is common in these brook charr populations, (ii) the presence creek chub and white sucker, two introduced species competing with brook charr for littoral resources, will decrease the phenotypic divergence between the two brook charr ecotypes, and (iii) the ecological release from introduced species will increase population and/or individual niche widths in brook charr. The study was based on 27 lakes and five indicators of resource use (stomach content, liver δ13C, muscle astaxanthin concentration, pyloric caecum length, and gill raker length). Our results indicate that within-lake differences in resource use by both ecotypes are common and stable through time. When facing interspecific competition, both littoral and pelagic brook charr incorporated more pelagic prey into their diet but maintained the amplitude of their differences in resource use, which contradicts our second prediction. Finally, we did not find any significant effect of introduced species on population and individual niche widths of brook charr. We suggest that the difference in feeding mode among distantly related competitors could prevent the complete exclusion of a species from a given niche and explain the lack of response to the ecological release.

Large-scale disease patterns explained by climatic seasonality and host traits.

Understanding factors affecting the distribution of vector-borne diseases in space and across species is of prime importance to conservation ecologists. Identifying the underlying patterns of disease requires a perspective encompassing large spatial scales. However, few studies have investigated disease ecology from a macroecological perspective. Hence, we use a global disease database to uncover worldwide infection patterns using avian malaria (Plasmodium) as a model for vector-borne disease transmission. Using data on 678 bird species from 442 locations, we show that environmental variables likely to synchronize bird and vector abundance are the key factors dictating infection risk for birds. Moreover, direct effects of host traits on exposure risk as well as potential trade-offs in resource allocation were also shown to affect disease susceptibility, with larger bird species being more prone to infection. Our results suggest that considering evolutionary strategies and factors influencing spatial overlap between hosts and vectors is crucial for understanding worldwide patterns of disease transmission success.

Alternative host identity and lake morphometry drive trematode transmission in brook charr.

Both biotic and abiotic factors have been invoked to explain the large variations observed in the prevalence and abundance of parasites in aquatic ecosystems. However, we have only a poor knowledge of the potential interplay among these factors in natural systems. It is, therefore, important to analyze the effects of multiple potential environmental drivers together to get an integrated view of their influence on the prevalence and abundance of parasites. To this end, we selected two genera of digenean trematode parasites that require at least two hosts to complete their life cycle and use two different transmission strategies. Crepidostomum moves through a trophic pathway via consumption of infected prey by the host, while Apophallus infects its hosts via direct penetration of their skin. This study was conducted in 23 Canadian Shield lakes exhibiting orthogonal gradients of biotic (fish species richness and biomass) and abiotic (morphometry, physico-chemical) variables. We quantified prevalence and abundance of these parasites in the skin and intestine of brook charr (Salvelinus fontinalis). Our results show that biotic factors are key drivers of parasite abundance and prevalence, with Apophallus being negatively associated with the fish species richness-biomass gradient, and Crepidostomum responding more to identity of host than to the diversity gradient. Among the abiotic variables, lake area was found to be positively related to both prevalence and abundance in Apophallus. Our results suggest that taking into account the interplay of both biotic and abiotic factors is crucial for understanding patterns of parasite transmission success in boreal lakes.

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.

Behavioural modification of personality traits: testing the effect of a trematode on nymphs of the red damselfly Xanthocnemis zealandica.

Research on animal personality is increasingly demonstrating that individuals in a population are characterised by distinct sets of behavioural traits that show consistency over time and across different situations. Parasites are known to alter the behaviour of their hosts, although their role in shaping host personality remains little studied. Here, we test the effect of trematode infection on two traits of their host's personality, activity and boldness, in nymphs of the red damselfly Xanthocnemis zealandica. Genetic analyses indicate that the undescribed trematode species falls within the superfamily Microphalloidea. Results of laboratory behavioural tests indicate that the two behavioural traits are related to each other: bolder individuals also show higher levels of spontaneous activity than shy ones. However, parasite infection had no effect on either of these behaviours or on their repeatability over three separate testing sessions. Although our findings suggest that this trematode does not influence personality traits of the damselfly host, it remains possible that other standard personality traits not tested here (exploratory tendency, aggressiveness) are affected by infection.