Unintentional Recovery of Parasitic Diversity Following Restoration of Red Deer (Cervus elaphus) in North-Western Italy.

Red deer (Cervus elaphus) populations in north-western Italy have been remodeled in recent decades. Multiple translocations and the spontaneous migration from Switzerland and France resulted in the successful redistribution of the red deer after human-driven extirpation during the 18th century. The scarcely diverse parasitic community harbored by these cervids has been enriched with two species-specific taxa, Onchocerca jakutensis and Phayigomyia picta, suggesting that the recovery of parasitic biodiversity could be included amongst future conservation goals of this intensively managed game. Nodular onchocercosis was reported in three red deer populations since 2011, while nasal bots were reported since 2018. Hypoderma spp. larvae were identified for the first time in 1989, then a second record was made in 2014 in the province of Biella, where a yearling male in poor condition infested with Hypoderma diana was observed. In the perspective that the restoration of species-specific parasite communities of native mammals in Europe is increasingly perceived as a conservation target, with similar dignity as the conservation of their hosts, baseline data presented in this communication may give new insights for future parasite conservation efforts.

Sarcoptic mange: An emerging panzootic in wildlife.

Sarcoptic mange, a skin infestation caused by the mite Sarcoptes scabiei, is an emerging disease for some species of wildlife, potentially jeopardizing their welfare and conservation. Sarcoptes scabiei has a near-global distribution facilitated by its forms of transmission and use of a large diversity of host species (many of those with broad geographic distribution). In this review, we synthesize the current knowledge concerning the geographic and host taxonomic distribution of mange in wildlife, the epidemiological connections between species, and the potential threat of sarcoptic mange for wildlife conservation. Recent sarcoptic mange outbreaks in wildlife appear to demonstrate ongoing geographic spread, increase in the number of hosts and increased virulence. Sarcoptic mange has been reported in at least 12 orders, 39 families and 148 species of domestic and wild mammals, making it one of the most generalist ectoparasites of mammals. Taxonomically, the orders with most species found infested so far include Perissodactyla (67% species from the entire order), Artiodactyla (47%), and Diprotodontia (67% from this order). This suggests that new species from these mammal orders are likely to suffer cross-species transmission and be reported positive to sarcoptic mange as surveillance improves. We propose a new agenda for the study of sarcoptic mange in wildlife, including the study of the global phylogeography of S. scabiei, linkages between ecological host traits and sarcoptic mange susceptibility, immunology of individuals and species, development of control strategies in wildlife outbreaks and the effects of global environmental change in the sarcoptic mange system. The ongoing transmission globally and sustained spread among areas and wildlife species make sarcoptic mange an emerging panzootic in wildlife. A better understanding of sarcoptic mange could illuminate the aspects of ecological and evolutionary drivers in cross-species transmission for many emerging diseases.

First report of interspecific transmission of sarcoptic mange from Iberian ibex to wild boar.

BACKGROUND: Sarcoptic mange is a globally distributed parasitic disease caused by the burrowing mite Sarcoptes scabiei. This mite has a certain degree of host specificity, although interspecific transmission can occur among phylogenetically related species or through prey-predator mediated exposure. In 2018, a wild boar (Sus scrofa) with lesions compatible with sarcoptic mange was hunted in Ports de Tortosa i Beseit Natural Park (PTB, north-eastern Spain), where an active epizootic outbreak of sarcoptic mange is affecting Iberian ibexes (Capra pyrenaica) since 2014. METHODS: A complete necropsy, skin scrapings and skin digestions with hydroxide potassium were performed to confirm the diagnosis. Routine histopathological analysis, toluidine blue staining and immunohistochemistry were used to characterize the lesions and the inflammatory infiltrate. Finally, 10 specific S. scabiei microsatellites were molecularly genotyped through polymerase chain reactions in mites obtained from the affected wild boar. For phylogenetic comparison, mites obtained from sympatric Iberian ibexes and allopatric wild boars and Iberian ibexes from southern Spain were analysed. RESULTS: Sarcoptes scabiei was visually and molecularly identified in the infested wild boar from PTB, causing skin lesions with dermal inflammatory infiltrate rich in T and B cells, which indicate an adaptive immune response. Three S. scabiei genetic clusters were identified: one included mites from southern Iberian ibexes, another included mites from southern wild boars, and a third one distinctively grouped the wild boar from PTB with the sympatric ibexes. CONCLUSIONS: To the authors' knowledge, this is the first reported case of sarcoptic mange in wild boar in Spain and the first documented case of S. scabiei cross-transmission from a wild ruminant host to a wild boar. The wild boar presented an ordinary scabies type reaction, which is typical of the self-limiting infestations reported in other cases of interspecific transmission.

Sarcoptic mange in wild ruminants in Spain: solving the epidemiological enigma using microsatellite markers.

BACKGROUND: In Spain, sarcoptic mange was first described in native wildlife in 1987 in Cazorla Natural Park, causing the death of nearly 95% of the local native population of Iberian ibex (Capra pyrenaica). Since then, additional outbreaks have been identified in several populations of ibex and other wild ungulate species throughout the country. Although the first epizootic outbreak in wildlife was attributed to the introduction of an infected herd of domestic goats, the origin and the cause of its persistence remain unclear. The main aims of this study are to understand (i) the number of Sarcoptes scabiei "strains" circulating in wild ruminant populations in Spain, and (ii) the molecular epidemiological relationships between S. scabiei and its hosts. METHODS: Ten Sarcoptes microsatellite markers were used to characterize the genetic structure of 266 mites obtained from skin scrapings of 121 mangy wild ruminants between 2011 and 2019 from 11 areas in Spain. RESULTS: Seventy-three different alleles and 37 private alleles were detected. The results of this study show the existence of three genetic strains of S. scabiei in the wild ruminant populations investigated. While two genetic clusters of S. scabiei were host- and geography-related, one cluster included multi-host mites deriving from geographically distant populations. CONCLUSIONS: The molecular epidemiological study of S. scabiei in wild ruminants in Spain indicates that the spreading and persistence of the parasite may be conditioned by host species community composition and the permissiveness of each host population/community to the circulation of individual "strains," among other factors. Wildlife-livestock interactions and the role of human-driven introduction or trade of wild and domestic animals should be better investigated to prevent further spread of sarcoptic mange in as yet unaffected natural areas of the Iberian Peninsula.

Patterns of helminth infection in Kenyan elephant populations.

BACKGROUND: The dynamics of helminth infection in African elephant populations are poorly known. We examined the effects of age, sex, social structure and the normalized difference vegetation index (NDVI) as primary drivers of infection patterns within and between elephant populations. METHODS: Coprological methods were used to identify helminths and determine infection patterns in distinct elephant populations in Maasai Mara National Reserve, Tsavo East National Park, Amboseli National Park and Laikipia-Samburu Ecosystem. Gaussian finite mixture cluster analyses of egg dimensions were used to classify helminth eggs according to genera. Generalized linear models (GLM) and Chi-square analyses were used to test for variation in helminth infection patterns and to identify drivers in elephant populations. RESULTS: Helminth prevalence varied significantly between the studied populations. Nematode prevalence (96.3%) was over twice as high as that of trematodes (39.1%) in elephants. Trematode prevalence but not nematode prevalence varied between populations. Although we found no associations between helminth infection and elephant social groups (male vs family groups), the median helminth egg output (eggs per gram, epg) did vary between social groups: family groups had significantly higher median epg than solitary males or males in bachelor groups. Young males in mixed sex family groups had lower epg than females when controlling for population and age; these differences, however, were not statistically significant. The average NDVI over a three-month period varied between study locations. Cluster analyses based on egg measurements revealed the presence of Protofasciola sp., Brumptia sp., Murshidia sp., Quilonia sp. and Mammomonogamus sp. GLM analyses showed that the mean epg was positively influenced by a three-month cumulative mean NDVI and by social group; female social groups had higher epg than male groups. GLM analyses also revealed that epg varied between elephant populations: Samburu-Laikipia elephants had a higher and Tsavo elephants a lower epg than Amboseli elephants. CONCLUSIONS: Elephants had infection patterns characterized by within- and between-population variation in prevalence and worm burden. Sociality and NDVI were the major drivers of epg but not of helminth prevalence. Gastrointestinal parasites can have a negative impact on the health of wild elephants, especially during resource scarcity. Thus, our results will be important when deciding intervention strategies.

Molecular identification of Ehrlichia, Anaplasma, Babesia and Theileria in African elephants and their ticks.

Although historical records indicate the presence of Ehrlichia and Babesia in African elephants, not much is known about their prevalence and diversity in elephants and their ticks, Amblyomma thollonii and Rhipicephalus humeralis. We amplified and sequenced the hypervariable V4 region of the 18S rRNA gene of Babesia and Theileria and the heat shock protein gene (groEL) of Ehrlichia/Anaplasma in DNA extracted from elephant blood (n = 104) and from elephant ticks (n = 52). Our results showed that the African elephants were infected with a novel Babesia spp. while A. thollonii was infected with Theileria bicornis and Theileria cf. velifera. This is the first record of T. bicornis; a protozoan that is linked to fatal infection in rhinoceros in a tick. Elephants and their ticks were all infected with a species of Ehrlichia like that identified in Japanese deer. The prevalence of Babesia spp., Theileria spp. and Ehrlichia spp. in ticks was higher than that of their elephant hosts. About 13.5% of elephants were positive for Theileria or Babesia while 51% of A. thollonii ticks and 27% of R. humeralis ticks were positive for Theileria or Babesia. Moreover, 5.8% of elephants were positive for Ehrlichia or Anaplasma compared to 19.5% in A. thollonii and 18% in R. humeralis. There was no association between the positive result in ticks and that of their elephant hosts for either Babesia spp., Theileria spp. or Ehrlichia spp. Our study reveals that the African elephants are naturally infected with Babesia spp and Ehrlichia spp and opens up an opportunity for further studies to determine the role of elephant as reservoirs of tick-borne pathogens, and to investigate their potential in spreading these pathogens as they range extensively. The presence of T. bicornis in A. thollonii also suggests a need for experiments to confirm its vector competence.

Infection dynamics of gastrointestinal helminths in sympatric non-human primates, livestock and wild ruminants in Kenya.

BACKGROUND: Gastrointestinal parasites are neglected infections, yet they cause significant burden to animal and human health globally. To date, most studies of gastrointestinal parasites focus on host-parasite systems that involve either a single parasite or a host species. However, when hosts share habitat and resources, they may also cross-transmit generalist gastrointestinal parasites. Here we explore multi-host-parasite interactions in a single ecosystem to understand the infection patterns, especially those linked to livestock-wildlife interfaces and zoonotic risk. METHODS: We used both coprological methods (flotation and sedimentation; N = 1,138 fecal samples) and molecular identification techniques (rDNA and mtDNA; N = 18 larvae) to identify gastrointestinal parasites in nine sympatric host species (cattle, sheep, goats, wildebeest, Grant's gazelles, Thomson's gazelles, impala, vervet monkeys and baboons) in the Amboseli ecosystem, Kenya. RESULTS: We found that the host community harbored a diverse community of gastrointestinal helminths, including 22 species and/or morphotypes that were heterogeneously distributed across the hosts. Six zoonotic gastrointestinal helminths were identified: Trichuris spp., Trichostrongylus colubriformis, Enterobius spp. Oesophagostomum bifurcum, Strongyloides stercoralis and Strongyloides fuelleborni. The dominant parasite was Trichuris spp, whose ova occurred in two morphological types. Baboons were co-infected with Strongyloides fuelleborni and S. stercoralis. CONCLUSIONS: We found that the interface zone shared by wild ungulates, livestock and non-human primates is rich in diversity of gastrointestinal helminths, of which some are extensively shared across the host species. Closely related host species were most likely to be infected by the same parasite species. Several parasites showed genetic sub-structuring according to either geography or host species. Of significance and contrary to expectation, we found that livestock had a higher parasite richness than wild bovids, which is a health risk for both conservation and livestock production. The zoonotic parasites are of public health risk, especially to pastoralist communities living in areas contiguous to wildlife areas. These results expand information on the epidemiology of these parasites and highlights potential zoonotic risk in East African savanna habitats.

Biogeography of Korea's top predator, the yellow-throated Marten: evolutionary history and population dynamics.

BACKGROUND: Peninsulas often harvest high genetic diversity through repeated southward migrations of species during glacial maxima. Studies addressing within-species evolutionary responses to climate fluctuations in northeast Asia are limited compared to other regions of the world, and more so in the Korean Peninsula. In this study, we conducted the first population-level study of the yellow-throated marten, Martes flavigula, from the Korean Peninsula, Russian, Taiwanese and Chinese localities in a biogeographic framework using mitochondrial (cyt-b, nd2, cr) and nuclear gene sequencing (ghr). RESULTS: Bayesian analyses revealed a rather young population, with a split from the most recent common ancestor at around 125 kya. Martes flavigula likely colonized the Korean Peninsula from Mainland China through the Yellow Sea twice, ca. 60 kya and 20 kya. Korean martens diversified during the Late Pleistocene with at least two dispersal events out of Korea, towards the southwest to Taiwan (ca. 80 kya) and towards the North into Russia and eastern China; most likely after the Last Glacial Maxima (ca. 20 kya). We argue that the lack of population structure and mixed populations is possibly a consequence of the high dispersal capability of the species. The Bayesian skyline plot revealed a population decline within the last 5000 years, suggesting potential negative biotic and anthropogenic effects in the area. We find that local populations are not genetically differentiated, therefore no perceptible population structure within Korea was found. CONCLUSIONS: The topography and geography of the Korean Peninsula has played a pivotal role in its colonization. Connections between the Korean Peninsula and the Mainland through sea-level drops of the Yellow Sea at times of glacial maxima and the high dispersal capability of M. flavigula adds to the lack of geographical structure in this species and the paraphyly of Korean lineages.

International meeting on sarcoptic mange in wildlife, June 2018, Blacksburg, Virginia, USA.

Sarcoptic mange is a globally distributed disease caused by the burrowing mite Sarcoptes scabiei, which also causes scabies in humans. A wide and increasing number of wild mammal species are reported to be susceptible to mange; however, the impacts of the disease in wildlife populations, mechanisms involved in its eco-epidemiological dynamics, and risks to public and ecosystem health are still unclear. Major gaps exist concerning S. scabiei host specificity and the mechanisms involved in the different presentations of the disease, which change between individuals and species. Immunological responses to the mite may have a relevant role explaining these different susceptibilities, as these affect the clinical signs, and consequently, the severity of the disease. Recently, some studies have suggested sarcoptic mange as an emerging threat for wildlife, based on several outbreaks with increased severity, geographical expansions, and novel wild hosts affected. Disease ecology experts convened for the "International Meeting on Sarcoptic Mange in Wildlife" on 4-5 June 2018, hosted by the Department of Fish and Wildlife Conservation at Virginia Tech in Blacksburg, Virginia, USA. The meeting had a structure of (i) pre-workshop review; (ii) presentation and discussions; and (iii) identification of priority research questions to understand sarcoptic mange in wildlife. The workgroup concluded that research priorities should be on determining the variation in modes of transmission for S. scabiei in wildlife, factors associated with the variation of disease severity among species, and long-terms effects of the mange in wildlife populations. In this note we summarize the main discussions and research gaps identified by the experts.

Hidden MHC genetic diversity in the Iberian ibex (Capra pyrenaica).

BACKGROUND: Defining hidden genetic diversity within species is of great significance when attempting to maintain the evolutionary potential of natural populations and conduct appropriate management. Our hypothesis is that isolated (and eventually small) wild animal populations hide unexpected genetic diversity due to their maintenance of ancient polymorphisms or introgressions. RESULTS: We tested this hypothesis using the Iberian ibex (Capra pyrenaica) as an example. Previous studies based on large sample sizes taken from its principal populations have revealed that the Iberian ibex has a remarkably small MHC DRB1 diversity (only six remnant alleles) as a result of recent population bottlenecks and a marked demographic decline that has led to the extinction of two recognized subspecies. Extending on the geographic range to include non-studied isolated Iberian ibex populations, we sequenced a new MHC DRB1 in what seemed three small isolated populations in Southern Spain (n = 132). The findings indicate a higher genetic diversity than previously reported in this important gene. The newly discovered allele, MHC DRB1*7, is identical to one reported in the domestic goat C. aegagrus hircus. Whether or not this is the result of ancient polymorphisms maintained by balancing selection or, alternatively, introgressions from domestic goats through hybridization needs to be clarified in future studies. However, hybridization between Iberian ibex and domestic goats has been reported in Spain and the fact that the newly discovered allele is only present in one of the small isolated populations and not in the others suggests introgression. The new discovered allele is not expected to increase fitness in C. pyrenaica since it generates the same protein as the existing MHC DRB1*6. Analysis of a microsatellite locus (OLADRB1) near the new MHC DRB1*7 gene reveals a linkage disequilibrium between these two loci. The allele OLADRB1, 187 bp in length, was unambiguously linked to the MHC DRB1*7 allele. This enabled us to perform a DRB-STR matching method for the recently discovered MHC allele. CONCLUSIONS: This finding is critical for the conservation of the Iberian ibex since it directly affects the identification of the units of this species that should be managed and conserved separately (Evolutionarily Significant Units).