Parasite Biogeography Research Articles

Tapping into natural history collections to assess latitudinal gradients of parasite diversity.

Parasites are key components of the biosphere not only due to their huge diversity, but also because they exert important influences on ecological processes. Nevertheless, we lack an understanding of the biogeographical patterns of parasite diversity. Here, we tap into the potential of biodiversity collections for understanding parasite biogeography. We assess species richness of supracommunities of helminth parasites infecting mammal assemblages in the Nearctic, and describe its relation to latitude, climate, host diversity, and land area. We compiled data from parasitology collections and assessed parasite diversity in Nearctic ecoregions for the entire parasite supracommunity of mammals in each ecoregion, as well as separately from carnivores and rodents to explore the effect of host taxonomic resolution on observed patterns. For carnivores, we found evidence of a negative latitudinal gradient, while parasites of rodents displayed no clear pattern. We found that parasite diversity was positively correlated with mean annual temperature and negatively correlated with seasonal precipitation. Parasite richness shows a diversity peak at intermediate host richness values and in carnivores correlates with temperature and seasonal precipitation. Rodent parasite diversity did not correlate with explored factors. Other researchers are encouraged to use parasitology collections to continue exploring patterns of parasite biogeography and macroecology.

Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite – The Ligula intestinalis species complex

Studies on parasite biogeography and host spectrum provide insights into the processes driving parasite diversification. Global geographical distribution and a multi-host spectrum make the tapeworm Ligula intestinalis a promising model for studying both the vicariant and ecological modes of speciation in parasites. To understand the relative importance of host association and biogeography in the evolutionary history of this tapeworm, we analysed mtDNA and reduced-represented genomic SNP data for a total of 139 specimens collected from 18 fish-host genera across a distribution range representing 21 countries. Our results strongly supported the existence of at least 10 evolutionary lineages and estimated the deepest divergence at approximately 4.99–5.05 Mya, which is much younger than the diversification of the fish host genera and orders. Historical biogeography analyses revealed that the ancestor of the parasite diversified following multiple vicariance events and was widespread throughout the Palearctic, Afrotropical, and Nearctic between the late Miocene and early Pliocene. Cyprinoids were inferred as the ancestral hosts for the parasite. Later, from the late Pliocene to Pleistocene, new lineages emerged following a series of biogeographic dispersal and host-switching events. Although only a few of the current Ligula lineages show narrow host-specificity (to a single host genus), almost no host genera, even those that live in sympatry, overlapped between different Ligula lineages. Our analyses uncovered the impact of historical distribution shifts on host switching and the evolution of host specificity without parallel host-parasite co-speciation. Historical biogeography reconstructions also found that the parasite colonized several areas (Afrotropical and Australasian) much earlier than was suggested by only recent faunistic data.

Vertebrates as uninfected disseminators of helminth eggs and larvae.

The passive dispersal of non-mobile organisms by vertebrates (zoochory) is a common mechanism used to explain their often widespread distribution. Transport occurs either internally via the vertebrate digestive tract (endozoochory), or externally be adhering to skin, feathers or fur (ectozoochory), and its success is due to both physiological and ecological factors associated with the disseminating 'hosting' animal. Helminth eggs and larvae are generally non-mobile stages that are largely dependent on the movement of another animal, typically a host, for geographical dissemination. Studies on the zoochory of helminths by vertebrates are extensive and particularly long-standing, stretching back to the 19th century, although this literature is often overlooked when considering the biogeography of parasites. This review assesses the potential of helminths to be dispersed passively by zoochory examining evidence from both laboratory and field studies. The physiological dynamics of the vertebrate intestines and skin surface as hostile environments, as well as the characteristics of eggs and larvae which may facilitate successful transport are evaluated. The various mechanisms of helminth endo- and ectozoochory are presented and the likelihood of long-distance dispersal determined. It is concluded that zoochory is a potentially important means of disseminating parasites.

Acromyrmex fowleri: a new inquiline social parasite species of leaf-cutting ants from South America, with a discussion of social parasite biogeography in the Neotropical region

Ant inquiline social parasites obligately depend on their hosts for survival and reproduction. Because of their shift from a eusocial to a socially parasitic life history, inquiline social parasites are interesting study systems for exploring the dynamics between conflict and cooperation in eusocial insect colonies. In addition, inquiline social parasites are of interest to evolutionary biology, because some species evolved directly from their hosts via sympatric speciation. With five described species, inquiline social parasites are relatively diverse in the fungus-growing ants. So far, four species have been reported from the leaf-cutting ant genus Acromyrmex and its closely affiliated social parasite genus Pseudoatta. In contrast, only a single parasite species was described from the lower attine genus Mycocepurus. Here, we describe a new species of inquiline social parasite, Acromyrmex fowleri sp. nov., which was discovered 27 years ago in the tropical region of Brazil (State of Bahia), living inside the colonies of its host Acromyrmex rugosus. We also report observations on the behavioral ecology and natural history of A. fowleri and its host. Our study suggests that A. fowleri is an obligate, queen-tolerant, workerless inquiline social parasite of A. rugosus and that A. fowleri represents some but not all morphological and life history characters of the inquiline syndrome, supporting the hypothesis that the complex traits of the inquiline syndrome evolve in a mosaic fashion. Considering that A. fowleri is a new social parasite species from tropical Brazil, we discuss the paradoxical biogeographic distribution of ant social parasites, which we refer to as the “Kutter–Wilson Paradox”, and conclude that the Kutter–Wilson Paradox is a genuine biogeographical pattern, instead of being a mere sampling artifact.

Phylogenetic uniqueness, not latitude, explains the diversity of avian blood parasite communities worldwide

AbstractAimCharacterizing macroecological patterns in biodiversity is key to improve our understanding of community assembly. Global biodiversity for many taxa follows a latitudinal gradient, with increased diversity in tropical latitudes. Less is known about global parasite biodiversity, inhibiting our ability to predict how global change will impact parasitic disease emergence. Using distribution and phylogenetic data for 2,386 avian haemosporidian blood parasites (genera Plasmodium, Haemoproteus and Leucocytozoon), I assessed how contemporary and historical drivers influence the composition of parasite communities worldwide.LocationGlobal.Time periodCurrent.Major taxa studiedHaemosporidian blood parasites.MethodsParasite distribution and cytochrome b sequence data were accessed from an open‐source database. Bayesian phylogenetic tree distributions were constructed for each parasite genus using two substitution models to capture uncertainty. Hierarchical regressions assessed effects of environmental variation, latitude and phylogenetic β‐diversity (βdiv; a proxy for phylogenetic uniqueness) on the diversity and asymmetry of parasite communities around the globe.ResultsI uncovered biodiversity hotspots and identified broad variation in global diversity patterns among parasite genera. Community diversity increased with increasing phylogenetic uniqueness for all three parasite genera; however, these diverse and unique regions did not consistently occur in the tropics. I found no evidence of a latitudinal diversity gradient, and support for a latitudinal gradient in community phylogenetic asymmetry was weak.Main conclusionsGlobal variation in avian haemosporidian phylogenetic diversity does not reflect a latitudinal gradient. Instead, parasite biogeography may reflect fundamental differences in host‐switching tendencies or the timing of avian evolutionary radiations. Examining the interplay between shared evolutionary history and phylogenetic diversity can provide important insights into the drivers of parasite biodiversity at global scales.

Phylogeography and connectivity of molluscan parasites: Perkinsus spp. in Panama and beyond

Panama is a major hub for commercial shipping between two oceans, making it an ideal location to examine parasite biogeography, potential invasions, and the spread of infectious agents. Our goals were to (i) characterise the diversity and genetic connectivity of Perkinsus spp. haplotypes across the Panamanian Isthmus and (ii) combine these data with sequences from around the world to evaluate the current phylogeography and genetic connectivity of these widespread molluscan parasites. We collected 752 bivalves from 12 locations along the coast of Panama including locations around the Bocas del Toro archipelago and the Caribbean and Pacific entrances to the Panama Canal, from December 2012 to February 2013. We used molecular genetic methods to screen for Perkinsus spp. and obtained internal transcribed spacer region (ITS) ribosomal DNA (rDNA) sequences for all positive samples. Our sequence data were used to evaluate regional haplotype diversity and distribution across both coasts of Panama, and were then combined with publicly available sequences to create global haplotype networks. We found 26 ITS haplotypes from four Perkinsus spp. (1–12 haplotypes per species) in Panama. Perkinsus beihaiensis haplotypes had the highest genetic diversity, were the most regionally widespread, and were associated with the greatest number of hosts. On a global scale, network analyses demonstrated that some haplotypes found in Panama were cosmopolitan (Perkinsus chesapeaki, Perkinsus marinus), while others were more geographically restricted (Perkinsus olseni, P. beihaiensis), indicating different levels of genetic connectivity and dispersal. We found some Perkinsus haplotypes were shared across the Isthmus of Panama and several regions around the world, including across ocean basins. We also found that haplotype diversity is currently underestimated and directly related to the number of sequences. Nevertheless, our results demonstrate long-range dispersal and global connectivity for many haplotypes, suggesting that dispersal through shipping probably contributes to these biogeographical patterns.

Hidden in plain sight: Cryptic and endemic malaria parasites in North American white-tailed deer (Odocoileus virginianus).

Malaria parasites of the genus Plasmodium are diverse in mammal hosts, infecting five mammalian orders in the Old World, but were long considered absent from the diverse deer family (Cervidae) and from New World mammals. There was a description of a Plasmodium parasite infecting a single splenectomized white-tailed deer (WTD; Odocoileus virginianus) in 1967 but none have been reported since, which has proven a challenge to our understanding of malaria parasite biogeography. Using both microscopy and polymerase chain reaction, we screened a large sample of native and captive ungulate species from across the United States for malaria parasites. We found a surprisingly high prevalence (up to 25%) and extremely low parasitemia of Plasmodium parasites in WTD throughout the eastern United States. We did not detect infections in the other ungulate species nor in western WTD. We also isolated the parasites from the mosquito Anopheles punctipennis. Morphologically, the parasites resemble the parasite described in 1967, Plasmodium odocoilei. Our analysis of the cytochrome b gene revealed two divergent Plasmodium clades in WTD representative of species that likely diverged 2.3 to 6 million years ago, concurrent with the arrival of the WTD ancestor into North America across Beringia. Multigene phylogenetic analysis placed these clades within the larger malaria parasite clade. We document Plasmodium parasites to be common in WTD, endemic to the New World, and as the only known malaria parasites from deer (Cervidae). These findings reshape our knowledge of the phylogeography of the malaria parasites and suggest that other mammal taxa may harbor infection by endemic and occult malaria parasites.

The impact of host dispersal on parasite biogeography

The impact of host dispersal on parasite biogeography

The impact of host dispersal on parasite biogeography

The impact of host dispersal on parasite biogeography

Biogeography of Parasitic Nematode Communities in the Galápagos Giant Tortoise: Implications for Conservation Management.

The Galápagos giant tortoise is an icon of the unique, endemic biodiversity of Galápagos, but little is known of its parasitic fauna. We assessed the diversity of parasitic nematode communities and their spatial distributions within four wild tortoise populations comprising three species across three Galápagos islands, and consider their implication for Galápagos tortoise conservation programmes. Coprological examinations revealed nematode eggs to be common, with more than 80% of tortoises infected within each wild population. Faecal samples from tortoises within captive breeding centres on Santa Cruz, Isabela and San Cristobal islands also were examined. Five different nematode egg types were identified: oxyuroid, ascarid, trichurid and two types of strongyle. Sequencing of the 18S small-subunit ribosomal RNA gene from adult nematodes passed with faeces identified novel sequences indicative of rhabditid and ascaridid species. In the wild, the composition of nematode communities varied according to tortoise species, which co-varied with island, but nematode diversity and abundance were reduced or altered in captive-reared animals. Evolutionary and ecological factors are likely responsible for the variation in nematode distributions in the wild. This possible species/island-parasite co-evolution has not been considered previously for Galápagos tortoises. We recommend that conservation efforts, such as the current Galápagos tortoise captive breeding/rearing and release programme, be managed with respect to parasite biogeography and host-parasite co-evolutionary processes in addition to the biogeography of the host.

Unforeseen biogeographical patterns in a multiple parasite system in Macaronesia

AbstractAimUnderstanding the reasons why hosts lose, maintain or swap their parasite burden after colonizing new areas has long intrigued island biogeographers. Using molecular markers, we evaluated parasite biogeography of a multiple parasite system of Apicomplexa protozoans (haemosporidian and coccidian parasites) showing different modes of transmission in the spectacled warbler (Sylvia conspicillata), a small passerine with recently founded populations in Macaronesia.LocationTwelve oceanic islands of three Macaronesian archipelagos (Madeira, the Canary Islands and Cape Verde) and two continental areas (the Iberian Peninsula and Morocco).MethodsWe amplified and sequenced fragments of the parasite mitochondrial genome (cytochrome b for haemosporidian and cytochrome c oxidase subunit I for coccidian parasites) to determine the prevalence, richness, diversity and associations between groups of pathogens from the continental sources to the Macaronesian islands. We also built a haplotype network for the coccidian parasites to obtain insights on their evolutionary history.ResultsWe did not find a significant reduction in parasite diversity in the Macaronesian islands compared with the mainland. The prevalence was higher in Macaronesia for both parasite groups than on the mainland, although it was only significant for the haemosporidian parasites. The haplotype network revealed an unexpectedly strong differentiation in the coccidia, with a similar structure to the haplotype topology previously found in the host.Main conclusionsOceanic islands provide model systems for disentangling geographical origins, colonization pathways, and diversification of avian hosts through analysis of parasites. We show that analysis of coccidians, which closely track the evolutionary history of their avian hosts, may illuminate co‐speciation processes in both groups. Our results show that coccidian populations in Macaronesia are highly structured but fail to provide support for the predicted impoverishment of parasite assemblages on islands.

Coevolutionary patterns and diversification of avian malaria parasites in African sunbirds (Family Nectariniidae)

The coevolutionary relationships between avian malaria parasites and their hosts influence the host specificity, geographical distribution and pathogenicity of these parasites. However, to understand fine scale coevolutionary host-parasite relationships, robust and widespread sampling from closely related hosts is needed. We thus sought to explore the coevolutionary history of avian Plasmodium and the widespread African sunbirds, family Nectariniidae. These birds are distributed throughout Africa and occupy a variety of habitats. Considering the role that habitat plays in influencing host-specificity and the role that host-specificity plays in coevolutionary relationships, African sunbirds provide an exceptional model system to study the processes that govern the distribution and diversity of avian malaria. Here we evaluated the coevolutionary histories using a multi-gene phylogeny for Nectariniidae and avian Plasmodium found in Nectariniidae. We then assessed the host-parasite biogeography and the structuring of parasite assemblages. We recovered Plasmodium lineages concurrently in East, West, South and Island regions of Africa. However, several Plasmodium lineages were recovered exclusively within one respective region, despite being found in widely distributed hosts. In addition, we inferred the biogeographic history of these parasites and provide evidence supporting a model of biotic diversification in avian Plasmodium of African sunbirds.

Evolution of parasite island syndromes without long‐term host population isolation: parasite dynamics in Macaronesian blackcaps Sylvia atricapilla

AbstractAimThe study of parasite biogeography on islands is important for our understanding of both the processes involved in the evolution of parasite assemblages worldwide and the ecology and conservation of insular communities. By studying the haemosporidian blood parasites of a bird that has recently colonized a number of oceanic islands, we were able to test hypotheses relating to the processes of parasite colonization and community assembly prior to the permanent isolation of host species on islands.LocationThe Atlantic Ocean archipelagos of Madeira and the Canary Islands.MethodsWe used cytochrome b DNA sequences to determine the prevalence and richness of parasites of the genera Haemoproteus, Plasmodium and Leucocytozoon in blackcaps, Sylvia atricapilla, a widespread passerine that colonized these archipelagos during the Last Glacial Maximum. We compared insular blackcap parasite assemblages with those observed in 37 blackcap populations sampled on mainland Europe.ResultsThe insular parasite assemblage was impoverished, containing c. 10% of the parasites found on the continent. None of the parasites observed on the islands were blackcap specific. Some of the observed parasites appear to have switched from blackcaps to other Macaronesian host species, whereas others were of Afrotropical origin and were acquired after blackcaps colonized the islands. The prevalence of parasites in the island populations of blackcaps was lower than in mainland blackcap populations and parasite richness decreased with increasing island distance to the continent.Main conclusionsMacaronesian blackcaps do not face the strong parasite load encountered by their mainland counterparts despite the fact that blackcap migration from the continent may directly transport mainland blackcap parasites to the islands. This supports the idea that normal mainland host–parasite associations are compromised on islands and that parasite island syndromes (low richness, frequent host‐switching and reduced specialization) evolve even before insular host populations become completely isolated from their mainland counterparts.

The comparative ecology and biogeography of parasites

Comparative ecology uses interspecific relationships among traits, while accounting for the phylogenetic non-independence of species, to uncover general evolutionary processes. Applied to biogeographic questions, it can be a powerful tool to explain the spatial distribution of organisms. Here, we review how comparative methods can elucidate biogeographic patterns and processes, using analyses of distributional data on parasites (fleas and helminths) as case studies. Methods exist to detect phylogenetic signals, i.e. the degree of phylogenetic dependence of a given character, and either to control for these signals in statistical analyses of interspecific data, or to measure their contribution to variance. Parasite-host interactions present a special case, as a given trait may be a parasite trait, a host trait or a property of the coevolved association rather than of one participant only. For some analyses, it is therefore necessary to correct simultaneously for both parasite phylogeny and host phylogeny, or to evaluate which has the greatest influence on trait expression. Using comparative approaches, we show that two fundamental properties of parasites, their niche breadth, i.e. host specificity, and the nature of their life cycle, can explain interspecific and latitudinal variation in the sizes of their geographical ranges, or rates of distance decay in the similarity of parasite communities. These findings illustrate the ways in which phylogenetically based comparative methods can contribute to biogeographic research.

Host-parasite relationships in flatfish (Pleuronectiformes) – the relative importance of host biology, ecology and phylogeny

The extent to which host biology, ecology and phylogeny determine the diversity of macroparasite assemblages has been investigated in recent years in several taxa, including fish. However, consensus has not been reached probably as a result of data being collected from different sources, different temporal scales or host and parasite biogeography and phylogeny having greater influence than expected. The present study evaluates the relative importance of 27 biological, ecological and phylogenetic characteristics of 14 flatfish species on the diversity of their ecto- and endoparasite assemblages, comprising a total of 53 taxa. Redundancy analyses were applied to the mean abundance of each parasite taxa infecting each host and to the richness, taxonomic distinctness and variance in taxonomic distinctness calculated for each assemblage within each host. Only a few host characteristics contributed significantly to the observed patterns: host distribution was more important in determining the type and mean abundance of ectoparasites present in an assemblage, whereas diversity of these assemblages were mainly related to the host's maximum size. Endoparasite mean abundance and diversity were mostly influenced by the number of food items ingested and by the presence of Crustacea and Polychaeta in the diet. However, the sympatric occurrence of related hosts also played an important role in the diversity values found in macroparasite assemblages. Results showed that a host characteristic has different importance according to the host-parasite relationship being examined, suggesting an important role for host-parasite co-evolution on the diversity of extant macroparasite assemblages.

Sturgeons (Chondrostei: Acipenseridae) and their metazoan parasites: patterns and processes in historical biogeography

Abstract Aim The historical biogeography of host‐parasite associations is examined in a geologically old group of fishes, the sturgeons (Osteichthyes: Acipenseridae), and their parasite assemblage. Evidence from phylogenetics and biogeographical studies of several parasite groups is used to formulate and evaluate hypotheses about the coevolutionary history of this host‐parasite association and, ultimately, the origin of sturgeons. Location The geographical areas discussed in this study are the temperate regions of North America and Eurasia, including the North Atlantic, North Pacific, Mediterranean and Ponto‐Caspian basins and their drainages. Methods Relationships of parasites in several clades (Truttaedacnitis, Diclybothriidae, Deropristiidae, Spinitectus and Acrobothriidae) are analysed or re‐analysed using cladistics. These results are combined with hypotheses of relationships of sturgeons and their biogeography. We largely follow an ‘empirical synthetic pattern approach' (Grande & Bemis, 1998) where the search is primarily for broadly congruent patterns, keeping interpretations close to the data and to known or postulated Earth history (palaeogeography). The evidence from the cladistic analyses is first interpreted within the context of vicariance events, but dispersalist scenarios are also discussed where warranted. We also use the concept of Croizat's ‘biogeographical tracks' to characterize broadly congruent distributional patterns. Results Phylogenetic hypotheses and biogeography of parasites indicate three major biogeographical tracks, of which a Holarctic track involving northern and north‐eastern Asian regions and North America is predominant (in Crepidostomum auriculatum, Polypodium hydriforme, Truttaedacnitis, Capillospirura, Diclybothriidae, Amphilina), with evidence for a recurring basal trans‐Pacific track (in Truttaedacnitis, Diclybothriidae). Trans‐Atlantic tracks appear to be either independent of (in Deropristidae) or secondarily derived from (in Bothrimonus and Truttaedacnitis sphaerocephala) a Holarctic track. Evidence from parasites supports the hypothesis of sister relationships between Acipenser medirostris and A. mikadoi, and between A. fulvescens and A. brevirostrum. Main conclusions This host–parasite association was historically structured by colonization and subsequent coevolution. Dispersal and vicariance of acipenserids resulted in small but widespread, highly distinct, monophyletic parasite lineages. Species of such parasite clades remain associated with major and often discrete continental and oceanic formations, and occasionally with related sturgeon species. Biogeographical tracks implicate the Cretaceous and early Tertiary Asian–American peninsula (Beringian region) as a historically important region in the origin and early geodispersion of the parasite fauna. This is consistent with hypotheses of the northern north‐eastern Asian region, or the more inclusive Asian–American peninsula, as a key area in the early diversification of sturgeons and the acquisition of their parasite fauna. The parasite fauna supports the hypothesis of a former continuous distribution of Nearctic and eastern Palaearctic (Siberian) sturgeons that was subsequently fragmented by geological and climatic events, resulting in major displacement of ancestral sturgeon populations in North America. The parasites also reflect a historical connection with marine and brackish water environments that pre‐dates the diversification of sturgeons, indicating that ancestral acipenserids were diadromous.

Questions and Answers on the Web

Shukri Adams (University of Cape Town, South Africa), studying parasite biogeography as a tool for fisheries management, was frustrated: `important publications ... are just not available in this country, and with the terrible Rand–US$ exchange rate and bad postal service, it's very difficult and costly getting publications through interlibrary loans/photocopies.' Why can't people scan papers and e-mail them to those in need? Is it legal to place scans on a website? One reply came: Jerry McLaughlin (University of Indiana, USA) suspected it was not legal, but that classics, where copyright has expired, may provide an exception.

Evaluation of the synlophe of Nematodirus urichi and N. lamae (Trichostrongyloidea) from Mazama americana and camelids (Artiodactyla) in the Neotropics

The synlophes of male and female specimens of Nematodirus urichi and male specimens of Nematodirus lamae are characterized. In the cervical region, at the level of the cervical papillae there were 34 and 42 ridges of variable height in male and female N. urichi, respectively. Ten (male) and 14 (female) ridges extend to the base of the cephalic expansion. In males there are 33 ridges at midbody with the synlophe extending posteriad to within 100 μm of the prebursal papillae. In females there are 38 or 39 ridges at midbody, the synlophe terminating at the level of the vulva. For N. lamae, there were 38–42 ridges in the cervical region; 14 extend to the base of the cephalic expansion. There are 36 ridges at midbody, the synlophe extending posteriad to within 100 μm of the prebursal papillae. An evaluation of parasite morphology and host–parasite biogeography may indicate a close relationship between N. urichi and N. lamae.

Synlophe of Nematodirus odocoilei (Trichostrongyloidea) from deer and caribou in North America with comments on the evolution of Nematodirus spp. among the Cervidae (Artiodactyla)

The synlophe for specimens of Nematodirus odocoilei from deer (Odocoileus hemionus) and woodland caribou (Rangifer tarandus caribou) is characterized. In the cervical region, at the level of the cervical papillae, there are 36–42 and 38–47 ridges of variable height in males and females, respectively. Sixteen ridges extend to the cephalic expansion. In males, 34–40 ridges occur at midbody, and the synlophe extends posteriad to within 50 μm of the prebursal papillae. In females, 36–42 ridges occur at midbody; the maximum number of ridges occurs posterior to the vulva (50) with a decrease again posteriad. The synlophe is continuous and extends to the caudal extremity of females. Based on concepts of parasite–host biogeography, both host switching and coevolution appear as determinants in the relationships of Nematodirus spp. and cervids. An evaluation of parasite morphology and host–parasite biogeography suggests that in the plesiomorphic condition the synlophe is composed of a high number of ridges as exemplified by Nematodirus spp. from cervids and neotropical camelids.

Biogeography of parasites in Australia.

Biogeography of parasites in Australia.