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

Abstract 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.

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Sarcoptes scabiei: Specific immune response to sarcoptic mange in the Iberian ibex Capra pyrenaica depends on previous exposure and sex

Experimental Parasitology ◽

10.1016/j.exppara.2009.10.008 ◽

2010 ◽

Vol 124 (3) ◽

pp. 265-271 ◽

Cited By ~ 38

Author(s):

Mathieu Sarasa ◽

Luisa Rambozzi ◽

Luca Rossi ◽

Pier G. Meneguz ◽

Emmanuel Serrano ◽

...

Keyword(s):

Immune Response ◽

Sarcoptes Scabiei ◽

Sarcoptic Mange ◽

Specific Immune Response ◽

Previous Exposure ◽

Capra Pyrenaica ◽

Iberian Ibex

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

Parasites & Vectors ◽

10.1186/s13071-021-04979-w ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Marta Valldeperes ◽

Barbara Moroni ◽

Luca Rossi ◽

Jorge Ramón López-Olvera ◽

Roser Velarde ◽

...

Keyword(s):

Wild Boar ◽

Inflammatory Infiltrate ◽

Skin Lesions ◽

Sarcoptes Scabiei ◽

Sarcoptic Mange ◽

Blue Staining ◽

Histopathological Analysis ◽

Capra Pyrenaica ◽

Wild Boars ◽

Chain Reactions

Abstract 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. Graphical abstract

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Multivariate Abundance Analysis of Multi-Host/Multi-Parasite Lungworms in a Sympatric Wild Ruminant Population

Diversity ◽

10.3390/d13060227 ◽

2021 ◽

Vol 13 (6) ◽

pp. 227

Author(s):

Tessa Carrau ◽

Carlos Martínez-Carrasco ◽

María Magdalena Garijo ◽

Francisco Alonso ◽

Rocío Ruiz de Ybáñez ◽

...

Keyword(s):

Population Level ◽

Parasite Load ◽

Fallow Deer ◽

Host Population ◽

Marginal Effect ◽

Wild Ruminant ◽

Additional Species ◽

Parasite Abundance ◽

Associated Risk Factors ◽

Natural Dynamics

In the analysis of a multi-host/multi-parasite system and its associated risk factors, it is particularly interesting to understand the natural dynamics among pathogens, their hosts, and the environment in wildlife populations. This analysis is particularly feasible in a scenario where multiple overlapping host populations are present in high densities, along with a complex community of parasites. We aimed to describe and analyze the naturally occurring lungworm polyparasitism in a wild ruminant community in Southeast Spain. The respiratory tracts of 250 specimens belonging to four different species (red deer, mouflon, Iberian ibex, and fallow deer) were studied. Almost half (48.0%) of the animals were infected with bronchopulmonary nematodes. Seven different nematodes were identified of which two genera (Protostrongylus spp. and Dictyocaulus spp.) and three additional species (Cystocaulus ocreatus, Muellerius capillaris, and Neostrongylus linearis) were recorded in at least two ruminants, with the mouflon as the commonest host. Our study shows a significant effect of host species and sampling area, plus a marginal effect of age, on parasite multivariate abundance at the host population level. Mouflon and adults of all hosts appear to carry the highest parasite load on average. From a spatial perspective, the highest parasite abundance was detected at the central part of the park.

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Non-Invasive Molecular Survey of Sarcoptic Mange in Wildlife: Diagnostic Performance in Wolf Faecal Samples Evaluated by Multi-Event Capture–Recapture Models

Pathogens ◽

10.3390/pathogens10020243 ◽

2021 ◽

Vol 10 (2) ◽

pp. 243

Author(s):

Julieta Rousseau ◽

Mónia Nakamura ◽

Helena Rio-Maior ◽

Francisco Álvares ◽

Rémi Choquet ◽

...

Keyword(s):

Molecular Detection ◽

High Specificity ◽

Sarcoptes Scabiei ◽

Sarcoptic Mange ◽

Diagnostic Specificity ◽

Non Invasive ◽

Faecal Samples ◽

Capture Recapture ◽

The Mean ◽

Event Capture

Sarcoptic mange is globally enzootic, and non-invasive methods with high diagnostic specificity for its surveillance in wildlife are lacking. We describe the molecular detection of Sarcoptes scabiei in non-invasively collected faecal samples, targeting the 16S rDNA gene. We applied this method to 843 Iberian wolf Canis lupus signatus faecal samples collected in north-western Portugal (2006–2018). We further integrated this with serological data (61 samples from wolf and 20 from red fox Vulpes vulpes, 1997–2019) in multi-event capture–recapture models. The mean predicted prevalence by the molecular analysis of wolf faecal samples from 2006–2018 was 7.2% (CI95 5.0–9.4%; range: 2.6–11.7%), highest in 2009. The mean predicted seroprevalence in wolves was 24.5% (CI95 18.5–30.6%; range: 13.0–55.0%), peaking in 2006–2009. Multi-event capture–recapture models estimated 100% diagnostic specificity and moderate diagnostic sensitivity (30.0%, CI95 14.0–53.0%) for the molecular method. Mange-infected individually identified wolves showed a tendency for higher mortality versus uninfected wolves (ΔMortality 0.150, CI95 −0.165–0.458). Long-term serology data highlights the endemicity of sarcoptic mange in wild canids but uncovers multi-year epidemics. This study developed and evaluated a novel method for surveying sarcoptic mange in wildlife populations by the molecular detection of S. scabiei in faecal samples, which stands out for its high specificity and non-invasive character.

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ATTEMPTED EXPERIMENTAL TRANSFER OF SARCOPTIC MANGE (Sarcoptes scabiei, ACARINA: SARCOPTIDAE) AMONG RED FOX, COYOTE, WOLF AND DOG

Journal of Wildlife Diseases ◽

10.7589/0090-3558-17.3.343 ◽

1981 ◽

Vol 17 (3) ◽

pp. 343-347 ◽

Cited By ~ 16

Author(s):

W.M. SAMUEL

Keyword(s):

Red Fox ◽

Sarcoptes Scabiei ◽

Sarcoptic Mange

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Evaluation of three enzyme-linked immunosorbent assays for sarcoptic mange diagnosis and assessment in the Iberian ibex, Capra pyrenaica

Parasites & Vectors ◽

10.1186/s13071-016-1843-4 ◽

2016 ◽

Vol 9 (1) ◽

Cited By ~ 12

Author(s):

Arián Ráez-Bravo ◽

José Enrique Granados ◽

Emmanuel Serrano ◽

Debora Dellamaria ◽

Rosa Casais ◽

...

Keyword(s):

Sarcoptic Mange ◽

Capra Pyrenaica ◽

Iberian Ibex ◽

Immunosorbent Assays

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Usefulness of estimated surface area of damaged skin as a proxy of mite load in the monitoring of sarcoptic mange in free-ranging populations of Iberian wild goat, Capra pyrenaica

Veterinary Parasitology ◽

10.1016/j.vetpar.2010.11.002 ◽

2011 ◽

Vol 176 (2-3) ◽

pp. 258-264 ◽

Cited By ~ 27

Author(s):

Jesús M. Pérez ◽

José E. Granados ◽

Mathieu Sarasa ◽

Emmanuel Serrano

Keyword(s):

Surface Area ◽

Sarcoptic Mange ◽

Capra Pyrenaica ◽

Free Ranging

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Of microbes and mange: consistent changes in the skin microbiome of three canid species infected with Sarcoptes scabiei mites

Parasites & Vectors ◽

10.1186/s13071-019-3724-0 ◽

2019 ◽

Vol 12 (1) ◽

Cited By ~ 4

Author(s):

Alexandra L. DeCandia ◽

Kennedy N. Leverett ◽

Bridgett M. vonHoldt

Keyword(s):

North American ◽

Treatment Strategies ◽

Skin Barrier ◽

Sarcoptes Scabiei ◽

Sarcoptic Mange ◽

Interspecies Transmission ◽

Skin Microbiome ◽

Red Foxes ◽

Mammal Species ◽

Alpha And Beta Diversity

Abstract Background Sarcoptic mange is a highly contagious skin disease caused by the ectoparasitic mite Sarcoptes scabiei. Although it afflicts over 100 mammal species worldwide, sarcoptic mange remains a disease obscured by variability at the individual, population and species levels. Amid this variability, it is critical to identify consistent drivers of morbidity, particularly at the skin barrier. Methods Using culture-independent next generation sequencing, we characterized the skin microbiome of three species of North American canids: coyotes (Canis latrans), red foxes (Vulpes vulpes) and gray foxes (Urocyon cinereoargenteus). We compared alpha and beta diversity between mange-infected and uninfected canids using the Kruskal–Wallis test and multivariate analysis of variance with permutation. We used analysis of composition of microbes and gneiss balances to perform differential abundance testing between infection groups. Results We found remarkably consistent signatures of microbial dysbiosis associated with mange infection. Across genera, mange-infected canids exhibited reduced microbial diversity, altered community composition and increased abundance of opportunistic pathogens. The primary bacteria comprising secondary infections were Staphylococcus pseudintermedius, previously associated with canid ear and skin infections, and Corynebacterium spp., previously found among the gut flora of S. scabiei mites and hematophagous arthropods. Conclusions This evidence suggests that sarcoptic mange infection consistently alters the canid skin microbiome and facilitates secondary bacterial infection, as seen in humans and other mammals infected with S. scabiei mites. These results provide valuable insights into the pathogenesis of mange at the skin barrier of North American canids and can inspire novel treatment strategies. By adopting a “One Health” framework that considers mites, microbes and the potential for interspecies transmission, we can better elucidate the patterns and processes underlying this ubiquitous and enigmatic disease.

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Dynamics of host populations affected by the emerging fungal pathogen Batrachochytrium salamandrivorans

Royal Society Open Science ◽

10.1098/rsos.160801 ◽

2017 ◽

Vol 4 (3) ◽

pp. 160801 ◽

Cited By ~ 16

Author(s):

Benedikt R. Schmidt ◽

Claudio Bozzuto ◽

Stefan Lötters ◽

Sebastian Steinfartz

Keyword(s):

Emerging Infectious Diseases ◽

Disease Outbreaks ◽

Host Population ◽

Mitigation Measures ◽

Disease Emergence ◽

Batrachochytrium Salamandrivorans ◽

In The Wild ◽

Successful Control ◽

Using Data ◽

Local Extirpation

Emerging infectious diseases cause extirpation of wildlife populations. We use an epidemiological model to explore the effects of a recently emerged disease caused by the salamander-killing chytrid fungus Batrachochytrium salamandrivorans ( Bsal ) on host populations, and to evaluate which mitigation measures are most likely to succeed. As individuals do not recover from Bsal , we used a model with the states susceptible, latent and infectious, and parametrized the model using data on host and pathogen taken from the literature and expert opinion. The model suggested that disease outbreaks can occur at very low host densities (one female per hectare). This density is far lower than host densities in the wild. Therefore, all naturally occurring populations are at risk. Bsal can lead to the local extirpation of the host population within a few months. Disease outbreaks are likely to fade out quickly. A spatial variant of the model showed that the pathogen could potentially spread rapidly. As disease mitigation during outbreaks is unlikely to be successful, control efforts should focus on preventing disease emergence and transmission between populations. Thus, this emerging wildlife disease is best controlled through prevention rather than subsequent actions.

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