Ecology Of Parasites Research Articles

First occurrence of ophiuroid-parasitic genus Ophieulima (Mollusca: Gastropoda: Eulimidae) in the North Pacific Ocean

Abstract A eulimid gastropod of the genus Ophieulima, parasitic on the disc of the ophiactid brittle star Ophiactis dyscrita, was collected from 256–343 m deep off Kanagawa, central Japan. This represents the first record of the genus from Japanese waters and even from the North Pacific Ocean. Here we describe it as Ophieulima yoshiharai n. sp. The generic assignment is justified by its conchological characters including (1) a small, conical shape with convex teleoconch whorls, (2) many fine growth lines and some strong growth pause scars on the teleoconch, (3) a well-developed, twisted columella, and (4) a multispiral, brownish transparent protoconch. Ophieulima yoshiharai n. sp. is distinguishable from the three (two named and one undescribed) extant, as well as two fossil congeners by its slender shell with the length of 2.1 times larger than width, a small aperture and a protoconch of 3.5 whorls. The new species is also characterized by its bathymetric distribution, which is shallower than the extant species of Ophieulima. On the other hand, the hosts of Ophieulima species are so far restricted to ophiuroids of the genus Ophiactis and the three named species have mostly been found attached to the lateral and/or dorsal sides of the host's disc, suggesting their similar parasitic ecology.

Taxonomy, Biodiversity, and Ecology of Parasites of Aquatic Organisms: A Special Issue

Parasitism is ubiquitous and one of the most successful lifestyles on Earth, with more than 200 independent transitions from non-parasitic ancestors considered only in the kingdom Animalia [...]

Breeding ecology of Eastern Crowned Leaf Warbler and brood parasitism by the Oriental Cuckoo

Breeding ecology of Eastern Crowned Leaf Warbler and brood parasitism by the Oriental Cuckoo

Ecology and Diversity of Angiosperm Parasites and Their Host Plants along Elevation Gradient in Al-Baha Region, Saudi Arabia

The ecology and diversity of flowering parasitic plants and their hosts are poorly investigated and usually ignored in Saudi Arabian plant communities. Therefore, this work aimed at assessing the ecology and diversity of parasitic plants and their hosts along an elevation gradient in the Al-Baha region (1300–2400 m.a.s.l.). Different quantitative vegetation parameters were applied to analyze the collected data. Eight parasitic plants from six genera and four families were identified along the gradient, with 67% of them being zoochorously dispersed species. They accounted for approximately 23.5% (8 out of 34) of those found throughout Saudi Arabia. Perennials, stem hemiparasites, and biregional taxa accounted for around 62.5% of the total parasites, whereas indigenous species accounted for 75%. The dominant family of parasitic species was Loranthaceae (50%), and Phragmanthera austroarabica A.G.Mill. & J.A.Nyberg was the most important species (IVI = 107.28). Orobanche cernua Loefl. and Loranthella deflersii (Tiegh.) S.Blanco & C.E.Wetzel were restricted to the dry zone (low elevation) only, while the other parasites were distributed across the surveyed region. Twenty-three host plants were identified throughout the study region. About 83% of them were phanerophytes and bioregional plants, with 91% being perennial species. The prevalent host plant family across all sites was Fabaceae, with Nicotina glauca Graham being the most important host species (IVI = 32.44%). P. austroarabica and Plicosepalus curviflorus Tiegh. preferred Vachellias as host plants, while Vachellia flava (Forssk.) Kyal. & Boatwr. was the heavily infected host by P. austroarabica. P. austroarabica had a broad spectrum of host range (13 host plants), while O. cernua had a very narrow host range (only Rumex nervosus Vahl). Individual parasite and host species were markedly more abundant in the wet zone than in the low-altitude dry zone. Further research is needed to fully understand such distinctive groups of plants and their negative and positive ecological consequences on plant biodiversity and natural ecosystems.

Helminth parasitic ecology in Gymnodactylus geckoides Spix, 1825 (Squamata: Phyllodactylidae) from Caatinga domain, north-eastern Brazil

ABSTRACT Gymnodactylus geckoides is an endemic lizard from the Caatinga domain. However, the relationship of G. geckoides with its parasites remains largely unknown. Therefore, the present study aimed to identify the helminth fauna of G. geckoides in a Caatinga fragment and determine the influence of factors such as host morphology, sex, diet and seasonality on parasite load. The study was conducted at the Conservation Unit (CU) of the Catimbau National Park located in Catimbau, Pernambuco, north-eastern Brazil. In total, 83 individuals were captured, among which 43 (51.8%) were infected by the following helminths: Acanthocephala cystacanths (prevalence, 47%; mean intensity, 2 ± 3.99; mean abundance, 1.61 ± 3.25) and the nematodes Parapharyngodon alvarengai (prevalence, 15.7%; mean intensity, 1 ± 0.74; mean abundance, 0.25 ± 0.66), Physaloptera lutzi (prevalence, 2.4%; mean intensity, 4 ± 1.00; mean abundance, 0.10 ± 0.64) Physaloptera sp. (prevalence, 4.8%; mean intensity, 1 ± 0.00; mean abundance, 0.05 ± 0.24), and Spauligodon oxkutzcabiensis (prevalence, 3.6%; mean intensity, 1 ± 0.94; mean abundance, 0.06 ± 0.36). A significantly positive relationship was found between the intensity of infection by the most prevalent helminth (which belonged to Acanthocephala) and host morphology (snoutvent length) (β ± SE = 6.421 ± 1.555, z = 4.128, p < .001), as well as prey type (β ± SE = 0.256 ± 0.078, z = 3.251, p < .001). Acanthocephala infection had a higher intensity during the rainy season (Analysis of Variance1,81: p < .01) in both female and male hosts (ANOVA1,73: p = 0.21). The present study is the first to identify the ecological patterns of the host–parasite relationships of G. geckoides. The results of this study contribute to the knowledge of the parasitic fauna of lizards in the Neotropical region. http://www.zoobank.org/urn:lsid:zoobank.org:pub:0C037904-257A-40E1-9460-487B9FAFE786

Space-environment relationship in the identification of potential areas of expansion of Trypanosoma cruzi infection in Didelphis aurita in the Atlantic Rainforest.

Ecological Niche Modeling is widely used for animals, but rarely for understanding the parasite ecology. Trypanosoma cruzi is a heterogeneous and widely dispersed multi-host parasite. Didelphis aurita is a generalist species, both in terms of diet and environments. We modeled the D. aurita niche and T. cruzi infection in the Brazilian Atlantic Rainforest, using the models of two common vector species (Triatoma vitticeps and Panstrongylus megistus) as biotic variables, predicting their occurrence. Records of T. cruzi infected and non-infected D. aurita were analyzed through climate and landscape approaches by the Ecoland method. Models for each triatomine species and infected and noninfected D. aurita were produced considering climate and landscape: resolution of ~1km2 selected by Pearson's correlation [-0.7≤α≤0.7]. For modeling, seven algorithms available in ModleR package were used. True Skill Statistic was used to evaluate the models' performance (≥ 0.7). T. vitticeps indicates that there is a spatial dependence with warm areas in the southeastern region while P. megistus presented a distribution with high environmental suitability concentrated in the Southeast. High values of climatic suitability, landscape and potential presence of T. vitticeps and P. megistus were considered necessary, but not sufficient for the presence of D. aurita infected by T. cruzi. Climate models showed an ecological niche with suitability variations homogeneous, and landscape models showed a distribution of habitat conditions along the biome, with a fragmented profile and heterogeneous between locations. Ecoland demonstrated that D. aurita has different degrees of impact on its role in the enzootic cycle in different locations of the Atlantic Rainforest. Associating the models with the Ecoland method allowed the recognition of areas where D. aurita are important T. cruzi reservoirs. Areas of high suitability for the presence of marsupials are a necessary, but not sufficient for D. aurita to act as a reservoir for T. cruzi.

Enigmatic freshwater mussel declines could be explained by the biodiversity‐disease relationship

AbstractThe biodiversity‐disease relationship states that increased species richness leads to lower pathogen pressure (i.e. the dilution effect), an effect that erodes with biodiversity loss. However, whether losses of the dilution effect can trigger extinction cascades remains largely unexplored.To explore this idea, we consider declines in freshwater mussels, on average the most threatened non‐marine group of organisms in the world. We argue that anthropogenically stimulated declines in mussel richness amplify pathogens in remaining species. Pathogen amplification triggers further local losses in both mussel abundance and richness, explaining the observed so‐called “enigmatic” declines in freshwater mussels.Vulnerable communities could become trapped in cycles of pathogen amplification and host decline. We highlight knowledge gaps and provide key steps to assess the likelihood of this occurring; these key steps are applicable to any host group.Policy implications. Our argument constitutes a testable hypothesis that may explain richness or abundance declines in previously intact communities. We provide further impetus for the consideration and preservation of diversity at a local scale and show that effective conservation requires integration of both host and parasite ecology.

Interrelationships and properties of parasite aggregation measures: a user’s guide

Aggregation of macroparasites among hosts is nearly universal among parasite-host associations. Researchers testing hypotheses on origins of parasite aggregation and its importance to parasite and host population ecology have used different measures of aggregation that are not necessarily measuring the same thing, potentially clouding our understanding of underlying epidemiological processes. We highlight these differences in meanings by exploring properties and interrelationships of six common measures of parasite aggregation, and provide a “user’s guide” to inform researchers’ decisions regarding their application. We compared the mathematical expressions of the different measures of aggregation, and ran two series of simulations and analyses. The first simulations tested the effect of random removals of parasites on aggregation levels under different conditions, while the second explored interrelationships between the measures, as well as between other individual parasitological sample measures (i.e. mean abundance, prevalence) and aggregation. Results of simulations and analyses showed that the six measures of aggregation could be separated readily into three groups: the variance-to-mean ratio (VMR) together with mean crowding, patchiness with k of the negative binomial, and Poulin’s D with Hoover’s index. These three pairs of measures showed differing responses to random parasite removals and differing relations with mean abundance and/or prevalence, highlighting that metrics capture different variation in other sample measures and different attributes of aggregation. We used results of our simulations and analyses, and a literature review, to list the properties, advantages, and disadvantages of each aggregation metric. We provide a comprehensive exploration of what is assessed by each metric, as a guide to metric choice. We implore researchers to provide enough information such that aggregation measures from each group are reported or can be readily calculated. Such steps are needed to allow large-scale analyses of variation in degrees of aggregation within and among parasite-host associations, to uncover epidemiological processes shaping parasite distributions.

Deepest digenean parasite: Molecular evidence of infection in a lower abyssal gastropod at 6,200 m

Little is known about the diversity and ecology of digenean parasites in the abyssal ocean (3500–6500 m deep) with previous occurrence records down only to 4877 m. Here, we report a 28S rDNA sequence of the fish digenean genus Lepidapedon (Lepidapedidae), amplified from DNA extract of a velutinid gastropod collected at 6185–6221 m in the Kuril–Kamchatka Trench, Northwest Pacific. This represents the deepest record for the platyhelminth class Digenea and, to our knowledge, for any group of fish parasites. Our finding also verifies for the first time that abyssal lepidapedids exploit benthic snails as intermediate hosts. The present species of Lepidapedon presumably accomplishes its life cycle in the lowermost abyssal zone with macrourid fish as the definitive host.

A Methodology to Produce Specific-Pathogen-Free Penaeid Shrimp for Use in Empirical Investigations of Parasite Ecology

Emerging infectious diseases in marine systems threaten food security and ecosystem function. Experiments to determine drivers of transmission and mortality from emerging pathogens require a reliable supply of disease-free animals. Imperfect detection of subclinical, latent, and early stage infections, however, necessitates effective treatments to remove infection from animals with unknown infection status. In this study, a procedure utilizing elevated temperatures and over-the-counter parasiticides to remove Hyalophysa lynni was developed. The apostome ciliate H. lynni is responsible for shrimp black gill (sBG) disease in commercially important southeastern shrimp fishery species, including Litopenaeus setiferus (white shrimp). Following a series of pilot studies to determine parasiticides combination and dosage, L. setiferus of unknown infection status were exposed to either 20°C or 30°C artificial seawater, and a parasiticide cocktail of metronidazole (3.15 mg L–1) and Cu+2 (0.5 mg L–1) or a medication-free control for 14 days in a fully crossed experimental design. All treatments, except for the 20°C without medications treatment, significantly reduced pathogen prevalence. The 30°C artificial seawater with parasiticide treatment resulted in complete curing of the experimental population, but shrimp mortality in this treatment was high (50%). This high mortality may have contributed to the low parasite prevalence found in this treatment by differentially culling infected individuals. If this is the case, the parasiticides may lower the parasite prevalence both by curing infections and heightening stress and subsequent mortality of diseased individuals. Although this procedure was developed to produce H. lynni-free shrimp to facilitate experimental studies of sBG disease, it is likely that this methodology would effectively produce specific-pathogen-free individuals in other crustacean species.

Tracking life cycles of parasites across a broad taxonomic scale in a marine ecosystem

Parasitic helminths exhibit remarkable diversity in their life cycles, although few parasite species have their whole life cycles resolved. Owing to the fact that parasite life stages within hosts are often not comparable using morphological data, genetic data provides convincing evidence of transmission pathways between intermediate and definitive hosts. We took this approach to an ecosystem level, genetically matching parasite (acanthocephalan, cestode, nematode and trematode) life stages across a broad taxonomic range of intermediate and definitive hosts (invertebrates, seabirds, elasmobranchs and teleost fish) in Otago’s (New Zealand) coastal marine ecosystem. We identified which transmission routes are utilized by the most parasite species and assessed which intermediate hosts are most important in facilitating the transmission of parasites in this ecosystem. Our findings reveal 59 new records of larval parasites infecting their respective intermediate hosts and 289 transmission pathways utilized by 35 helminth species to complete their life cycles. Sprat, triplefin and arrow squid all hosted the highest number of larval parasite species, suggesting they play important roles as intermediate hosts. We then used the new life cycle data to provide a synthetic overview of the life cycles known for various parasite groups in New Zealand. This study highlights how studying parasite life cycles can enhance our understanding of the ecology and evolution of parasites and hosts in natural systems, beyond simply resolving life cycles.

Drought correlates with reduced infection complexity and possibly prevalence in a decades-long study of the lizard malaria parasite Plasmodium mexicanum.

Microparasites often exist as a collection of genetic 'clones' within a single host (termed multi-clonal, or complex, infections). Malaria parasites are no exception, with complex infections playing key roles in parasite ecology. Even so, we know little about what factors govern the distribution and abundance of complex infections in natural settings. Utilizing a natural dataset that spans more than 20 years, we examined the effects of drought conditions on infection complexity and prevalence in the lizard malaria parasite Plasmodium mexicanum and its vertebrate host, the western fence lizard, Sceloporus occidentalis. We analyzed data for 14,011 lizards sampled from ten sites over 34 years with an average infection rate of 16.2%. Infection complexity was assessed for 546 infected lizards sampled during the most recent 20 years. Our data illustrate significant, negative effects of drought-like conditions on infection complexity, with infection complexity expected to increase by a factor of 2.27 from the lowest to highest rainfall years. The relationship between rainfall and parasite prevalence is somewhat more ambiguous; when prevalence is modeled over the full range in years, a 50% increase in prevalence is predicted between the lowest and highest rainfall years, but this trend is not apparent or is reversed when data are analyzed over a shorter timeframe. To our knowledge, this is the first reported evidence for drought affecting the abundance of multi-clonal infections in malaria parasites. It is not yet clear what mechanism might connect drought with infection complexity, but the correlation we observed suggests that additional research on how drought influences parasite features like infection complexity, transmission rates and within-host competition may be worthwhile.

Atypical life cycle does not lead to inbreeding or selfing in parasites despite clonemate accumulation in intermediate hosts.

Many parasites utilize asexual and sexual reproduction and multiple hosts to complete their life cycles. How these taxa avoid inbreeding is an essential question for understanding parasite evolution and ecology. Aquatic trematodes that require multiple host species may benefit from diverse genetic parasite assemblages accumulating within second intermediate hosts prior to sexual reproduction in definitive hosts. However, Cotylurus species are able to utilize the same snail species as first and second intermediate hosts, potentially resulting in the accumulation of genetically identical clones (clonemates) prior to sexual reproduction. In this study, we developed and analysed novel microsatellite loci to determine if clones are accumulating within snail hosts prior to ingestion by bird hosts and the effects this could have on parasite inbreeding. Contrary to previous studies of aquatic trematodes, significantly large numbers of clonemates were present within snails, but full-sibs were not. Genetic structure was present over a relatively small geographical scale despite the use of vagile definitive hosts. Phylogenetic analysis identified the Cotylurus sp. clones as belonging to a single species. Despite the presence of clones within snails, mating between clones/selfing was not common and heterozygosity is maintained within individuals. Potential issues with clones mating may be mitigated by the presence of snails with numerous clones, the consumption of many snails by bird hosts and parasite clone recognition/avoidance. Use of the same host species for multiple life stages may have advantages when parasites are able to avoid inbreeding and the required hosts are common.

How to use natural history collections to resurrect information on historical parasite abundances.

Many of the most contentious questions that concern the ecology of helminths could be resolved with data on helminth abundance over the past few decades or centuries, but unfortunately these data are rare. A new sub-discipline - the historical ecology of parasitism - is resurrecting long-term data on the abundance of parasites, an advancement facilitated by the use of biological natural history collections. Because the world's museums hold billions of suitable specimens collected over more than a century, these potential parasitological datasets are broad in scope and finely resolved in taxonomic, temporal and spatial dimensions. Here, we set out best practices for the extraction of parasitological information from natural history collections, including how to conceive of a project, how to select specimens, how to engage curators and receive permission for proposed projects, standard operating protocols for dissections and how to manage data. Our hope is that other helminthologists will use this paper as a reference to expand their own research programmes along the dimension of time.

Modeling the geographical distributions of Chordodes formosanus and its mantis hosts in Taiwan, with considerations for their niche overlaps.

Species distribution models (SDMs) have conventionally been used for evaluating the distribution of individual species, but they can also be used, through comparing different SDMs, to evaluate the geographic similarity between taxa. In this study, we used a parasite and host system to infer the geographic overlaps between species with tight biological interaction, for example, parasites and their obligate host. Specifically, we used the horsehair worm Chordodes formosanus and its three mantis hosts to study the extent of niche overlap. We retrieved presence points for the host species and the parasite, and then we built SDMs with MaxEnt implemented in ENMeval using selected bioclim variables (based on variance inflation factor values) at 30s scale. The models showed that the hosts and parasite do not occur in the high elevation areas in Taiwan, which is expected based on their biology. Interestingly, the predicted parasite distribution included areas without collection records, implying local extinction or sampling bias. We subsequently evaluated niche overlap between hosts and the parasite according to five similarity indices (Schoener's D, I statistic, relative rank, Pearson correlation coefficient, and the rank correlation coefficient rho). Our models showed a high similarity of SDM predictions between hosts and the parasite. There were differences among metrics for which host shared the highest similarity with the parasite, but the majority of the results indicated that the Japanese boxing mantis had the highest niche similarity with the horsehair worm. The choice of the niche overlap metric to use can uncover information on the parasite's ecology, which can be important for endangered species. SDMs are reliable tools for host and parasite conservation management and could help improve our understanding of parasite biology and ecology.

ICOPA 2022: living with parasites, collaborating globally, and breaking a glass ceiling

ICOPA 2022: living with parasites, collaborating globally, and breaking a glass ceiling

Morphological characterization of fluke eggs in green turtles (Chelonia mydas) found on the coast of Espírito Santo State, Brazil

Although some studies have identified parasites in green turtles (Chelonia mydas), little is known about the morphology of helminth eggs in the feces of these animals. The aim of this study was to morphologically characterize helminth eggs recovered in coproparasitological exams by sedimentation and to analyze their relationship with helminth species recovered during necropsy of juvenile specimens of C. mydas. Four different egg morphotypes were found, identified, and classified as digenetic trematodes of the families Microscaphidiidae, Cladorchiidae, and Spirorchiidae. There was morphological diversity in the size of the eggs measured directly in adult parasites, with sizes ranging from 19.07 to 99.28 μm in length and from 11.35 to 45.66 μm in width. The observation of eggs on coproparasitological exams is important for studying the ecology of sea turtle parasites, since the life cycle of some species is not yet fully understood.

Grand challenges in parasite epidemiology and ecology

Grand challenges in parasite epidemiology and ecology

The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk.

Different hosts in different lakes: prevalence and population genetic structure of plerocercoids of Ligula intestinalis (Cestoda) in Czech water bodies.

Ligula intestinalis (Linnaeus, 1758) is a tapeworm parasite with a worldwide distribution that uses a wide variety of fish species as its second intermediate host. In the present study, we investigated the prevalence and population genetic structure of plerocercoids of L. intestinalis in five common cyprinoid species, roach Rutilus rutilus (Linnaeus), freshwater bream Abramis brama (Linnaeus), white bream Blicca bjoerkna (Linnaeus), bleak Alburnus alburnus (Linnaeus), and rudd Scardinius erythrophthalmus (Linnaeus), collected in six water bodies of the Czech Republic (Milada, Most, Medard, Jordán, Římov and Lipno). Of the six study sites, the highest frequency of parasitism was recorded in Lake Medard (15%). The overall prevalence rate among the species was as follows: roach > rudd ≥ freshwater bream > bleak > white bream. Two mitochondrial genes (cytb and COI) were used to compare the population genetic structure of parasite populations using selected samples from the five fish species. The results of the phylogenetic analysis indicated that all populations of L. intestinalis were placed in Clade A, previously identified as the most common in Europe. At a finer scale, haplotype network and PCoA analyses indicated the possible emergence of host specificity of several mtDNA haplotypes to the freshwater bream. Moreover, pairwise Fixation indices (FST) revealed a significant genetic structure between the parasite population in freshwater bream and other host species. Parasite populations in roach not only showed the highest rate of prevalence but also depicted a maximum number of shared haplotypes with populations from bleak and rudd. Our results suggest that recent ecological differentiation might have influenced tapeworm populations at a fine evolutionary scale. Thus, the differences in prevalence between fish host species in different lakes might be influenced not only by the parasite's ecology, but also by its genetic diversity.