Development of resistance to sarcoptic mange in ibex

Sarcoptic mange affects mammal host species worldwide and, particularly, wild Caprinae throughout much of Eurasia. In the Iberian Peninsula, several outbreaks of sarcoptic mange in Iberian ibex (Capra pyrenaica) have been reported since the 1980s. Using data from a period of long-term monitoring and a seasonal autoregressive integrated moving average (SARIMA)-generalized autoregressive conditional heteroscedasticity (GARCH) model approach, we performed a time-series analysis of the monthly prevalence of sarcoptic mange in the Iberian ibex population in Sierra Nevada Natural Space in southern Spain. In January 2003–March 2021, we documented a significant negative trend in sarcoptic mange prevalence, albeit with some interannual peaks. These findings can only be explained if a certain level of resistance to sarcoptic mange exists in hosts that, along with other factors, could provoke this reduced prevalence. Prevalence values varied seasonally, with maximum values in spring and minimum values at the end of summer, which may be due to factors linked to climate, host behavior, and endocrine activity. Our model predicts that the prevalence of sarcoptic mange in the Iberian ibex will continue to decrease over the next 2 years. Despite the inherent challenges involved, diagnosing and monitoring of wildlife diseases are integral to obtaining reliable epidemiological data and designing appropriate management strategies.     

First description of sarcoptic mange in wild European rabbit (Oryctolagus cuniculus)

The European wild rabbit (Oryctolagus cuniculus) is a keystone species in the Iberian Mediterranean ecosystems being the staple prey of protected and endangered predators. Wild rabbits were once widespread, but the introduction of two viral diseases, myxomatosis in the 1950s and the rabbit hemorrhagic disease in 1989, resulted into a dramatic decline of its populations. Sarcoptic mange is a highly contagious parasitic infection caused by Sarcoptes scabiei. The first cases of sarcoptic mange in a wild rabbit population are recorded from a hunting area in Majorca (Balearic Islands, Spain). Five of 32 inspected rabbits (14.7%) were affected, with similar prevalences in summer and autumn. Sarcoptes scabiei were obtained from the edge of the lesions of two of the rabbits. The most frequently observed lesions were small areas of alopecia and crusts in the limbs. Affected limbs presented also a marked hypertrichosis and an apparent abnormal growth of the nails. One rabbit also presented lesions around mouth and nostrils. Parasitized rabbits were in significant lower body condition than healthy ones. According to previous reports of mange epizooties in other naïve wild species that caused marked short-term effects in their populations, this disease may pose a risk for the conservation of wild rabbit and their predators. Whether mange is endemic in rabbits from Majorca or it has been introduced is unknown. Game managers are encouraged to be aware of introducing sarcoptic mange during rabbit translocations.

     

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

Host acquired immunity is a critical factor that conditions the survival of parasites. Nevertheless, there is a shortage of data concerning inter-individual immunological inequalities in wild mammals. Sarcoptic mange is a widespread parasitosis that severely affects mammals such as the Iberian ibex (Capra pyrenaica). Despite some work on the subject, the immune response to sarcoptic mange infestation is still a complex and poorly understood phenomenon. To improve knowledge of the host-Sarcoptes immunological interaction, 18 Iberian ibexes were experimentally infested. IgG levels were assessed using ELISA to test for potential factors determining the specific immune response to infestation. Previous exposure and sex appeared to affect the IgG response to infestation and our results suggest a sex-biased immunomodulation. We discuss the immunological pattern of host-Sarcoptes interactions and also suggest further lines of work that may improve the understanding of immunological interactions of host-Sarcoptes systems.     

Sarcoptic mange vulnerability in carnivores of the Białowieża Primeval Forest,Poland: underlying determinant factors

Sarcoptic mange caused by Sarcoptes scabiei, is a highly contagious worldwide mite infection responsible for epizootic skin disease in populations of wild and domestic mammals. It causes skin disorders that may lead to severe generalized skin disease (mange). We investigated the spread and dynamics of sarcoptic mange in one of the best preserved carnivore communities in the Bia?owie?a Primeval Forest over the last 20 years. Sarcoptic mange was found in 6 of 10 investigated species. The highest percentage of infected individuals was recorded in red foxes (19 %), European badgers (9 %), grey wolves (7 %), raccoon dogs (6 %), and stone martens (5 %). Other species were not infected (least weasel, American mink, European polecat, pine marten) or infected sporadically (Eurasian lynx––1 case). Rate of infection was correlated with the sum of ecological and behavioral features, which may increase the spread of infection. Outbreaks of sarcoptic mange occurred simultaneously in several species of carnivores, which indicates the occurrence of between species transmission. We found that the source of investigated individuals (trapped, culled and found dead) may influence the results of the analysis. Our study shows that in carnivore communities such as in Bia?owie?a Forest, numerous species may serve as a reservoir of the pathogen and favor its persistence in the environment. This study indicates that sociality and use of den sites are important factors affecting sarcoptic mange spread and prevalence in wild populations of carnivores.     

Management of a caseous lymphadenitis outbreak in a new Iberian ibex (<Emphasis Type="Italic">Capra pyrenaica</Emphasis>) stock reservoir

Background

In 2010, an Iberian ibex (Capra pyrenaica hispanica) stock reservoir was established for conservation purposes in north-eastern Spain. Eighteen ibexes were captured in the wild and housed in a 17 hectare enclosure. Once in captivity, a caseous lymphadenitis (CLA) outbreak occurred and ibex handlings were carried out at six-month intervals between 2010 and 2013 to perform health examinations and sampling. Treatment with a bacterin-based autovaccine and penicillin G benzatine was added during the third and subsequent handlings, when infection by Corynebacterium pseudotuberculosis was confirmed. Changes in lesion score, serum anti-C. pseudotuberculosis antibodies and haematological parameters were analyzed to assess captivity effects, disease emergence and treatment efficacy. Serum acute phase proteins (APP) Haptoglobin (Hp), Amyloid A (SAA) and Acid Soluble Glycoprotein (ASG) concentrations were also determined to evaluate their usefulness as indicators of clinical status.Once in captivity, 12 out of 14 ibexes (85.7%) seroconverted, preceding the emergence of clinical signs; moreover, TP, WBC, eosinophil and platelet cell counts increased while monocyte and basophil cell counts decreased. After treatment, casualties and fistulas disappeared and both packed cell volume (PCV) and haemoglobin concentration significantly increased. Hp, SAA and ASG values were under the limit of detection or showed no significant differences.

Conclusions

A role for captivity in contagion rate is suggested by the increase in antibody levels against C. pseudotuberculosis and the emergence of clinical signs. Although boosted by captivity, this is the first report of an outbreak of caseous lymphadenitis displaying high morbidity and mortality in wild ungulates. Treatment consisting of both vaccination and antibiotic therapy seemed to prevent mortality and alleviate disease severity, but was not reflected in the humoural response. Haematology and APP were not useful indicators in our study, perhaps due to the sampling frequency. Presumably endemic and irrelevant in the wild, this common disease of domestic small ruminants is complicating conservation efforts for the Iberian ibex in north-eastern Spain.

     

Microsatellite-based genotyping of MHC class II DRB1 gene in Iberian and Alpine ibex

In an analysis of a microsatellite locus (OLADRB1) linked to the MHC DRB1 gene of Iberian and Alpine ibex (Capra pyrenaica and Carpa ibex), we detected strong linkage disequilibrium between both loci. The allele length polymorphism at OLADRB1 was unambiguously linked to a particular DRB1 allele. This allowed us to develop a DRB-STR matching method for both ibex species. Validation of the DRB-STR matching method was performed in 160 Iberian ibex from Spain and 98 Alpine ibex from Switzerland and Italy. This simple and relatively inexpensive protocol may find wide applications in a variety of research areas (e.g., mate choice, pathogen-driven selection) and in the biological conservation and management of the Western European ibex populations.     

Conservation Genetics of Threatened Hippocampus guttulatus in Vulnerable Habitats in NW Spain: Temporal and Spatial Stability of Wild Populations with Flexible Polygamous Mating System in Captivity

This study was focused on conservation genetics of threatened Hippocampus guttulatus on the Atlantic coast of NW Iberian Peninsula. Information about spatial structure and temporal stability of wild populations was obtained based on microsatellite markers, and used for monitoring a captive breeding program firstly initiated in this zone at the facilities of the Institute of Marine Research (Vigo, Spain). No significant major genetic structure was observed regarding the biogeographical barrier of Cape Finisterre. However, two management units under continuous gene flow are proposed based on the allelic differentiation between South-Atlantic and Cantabrian subpopulations, with small to moderate contemporary effective size based on single-sample methods. Temporal stability was observed in South-Atlantic population samples of H. guttulatus for the six-year period studied, suggesting large enough effective population size to buffer the effects of genetic drift within the time frame of three generations. Genetic analysis of wild breeders and offspring in captivity since 2009 allowed us to monitor the breeding program founded in 2006 in NW Spain for this species. Similar genetic diversity in the renewed and founder broodstock, regarding the wild population of origin, supports suitable renewal and rearing processes to maintain genetic variation in captivity. Genetic parentage proved single-brood monogamy in the wild and in captivity, but flexible short- and long-term mating system under captive conditions, from strict monogamy to polygamy within and/or among breeding seasons. Family analysis showed high reproductive success in captivity under genetic management assisted by molecular relatedness estimates to avoid inbreeding. This study provides genetic information about H. guttulatus in the wild and captivity within an uncovered geographical range for this data deficient species, to be taken into account for management and conservation purposes.     

Invading parasites cause a structural shift in red fox dynamics

The influence of parasites on host life histories and populations is pronounced. Among several diseases affecting animal populations throughout the world, sarcoptic mange has influenced many carnivore populations dramatically and during the latest epizootic in Fennoscandia reduced the abundance of red fox by over 70%. While the numerical responses of red fox populations, their prey and their competitors as well as clinical implications are well known, knowledge of how sarcoptic mange affects the structure of the dynamics of red fox populations is lacking. Integrating ecological theory and statistical modelling, we analysed the long-term dynamics (1955-1996) of 14 Danish red fox populations. As suggested by the model, invading sarcoptic mange significantly affected direct and delayed density dependence in red fox dynamics and concomitant shifts in fluctuation patterns were observed. Our statistical analyses also revealed that the spatial progressive spread of mange mites was mirrored in the autocovariate structures of red fox populations progressively exposed to sarcoptic mange.     

Distribution,status and conservation problems of the Spanish Ibex,Capra pyrenaica (Mammalia: Artiodactyla)†

In this paper, the distribution and status of the Spanish Ibex, Capra pyrenaica (Mammalia: Artiodactyla), are revised. The whole Iberian population numbers nearly 50 000, distributed in more than 50 nuclei, and has generally increased during the last decades. Nevertheless, within this wider context, different conditions apply to different populations, including recent extinction (the Pyrenean population), recovery from recent severe epizooty of sarcoptic mange (e.g. the Sierras de Cazorla and Segura y Las Villas range population) and populations at high densities (e.g. Gredos mountain range and Sierra de Grazalema Natural Park, among others). The main factors affecting the conservation of this species are also reported and discussed. On the basis of current information we propose the status of ‘vulnerable’ for the Spanish Ibex.     

Comparative pathological and immunohistochemical features of sarcoptic mange in five sympatric wildlife species in Northern Spain

This study collects pathological information concerning sarcoptic mange in sympatric red deer, roe deer, chamois, wolf and red fox from Northern Spain, and discusses reported variations in the response from the different species against Sarcoptes scabiei. Wolf is the only studied species which shows prevalence of the hypersensitivity (alopecic) response to the detriment of the hyperkeratotic form, usually observed in ungulates and fox. The present work shows the use of immunohistochemistry as a valuable tool for the study and diagnosis of sarcoptic mange in those species whose immune response or stage of infestation limits the number of detectable mites, not an unusual difficulty faced when working with sarcoptic mange in wildlife species.     

An Invasive Vector of Zoonotic Disease Sustained by Anthropogenic Resources: The Raccoon Dog in Northern Europe

The raccoon dog (Nyctereutes procyonoides) is an introduced species in Europe with a continually expanding range. Since the species is capable of affecting local ecosystems and is a vector for a number of severe zoonotic diseases, it is important to understand its food habits. Raccoon dog diet was studied in Estonia by examining the contents of 223 stomach samples collected during the coldest period of the year, August to March, in 2010–2012. The most frequently consumed food categories were anthropogenic plants (e.g. cereals, fruits; FO = 56.1%) and carrion (e.g. carcasses of artiodactyls and carnivores; FO = 48.4%). Carrion was also the only food category that was consumed significantly more frequently by raccoon dogs exhibiting symptoms of sarcoptic mange than by uninfected animals. Small mammals, which represent intermediate hosts for the zoonotic tapeworm Echinococcus multilocularis, were more commonly recorded in samples also containing anthropogenic plants than expected by chance. Comparison of raccoon dog and red fox (Vulpes vulpes) diet in Estonia revealed higher overlap than found elsewhere in Europe, with ‘carrion’ and ‘anthropogenic plants’ making up the bulk of both species’ diet; however, raccoon dogs were more omnivorous than red foxes. Our results suggest that while the use of most food categories reflects the phenology of natural food sources, ‘anthropogenic plants’ and ‘carrion’ provide an essential resource for raccoon dogs during the coldest period of the year, with the latter resource especially important for individuals infected with sarcoptic mange. Since both of these food categories and small mammals are often found at supplementary feeding sites for wild boar (Sus scrofa), this game management practice may facilitate high densities of mesocarnivores and promote the spread of some severe zoonotic diseases, including alveolar echinococcosis, trichinellosis, rabies and sarcoptic mange.     

Use of microsatellite data and pedigree information in the genetic management of two long-term salmon conservation programs

In this paper, we describe the utility of microsatellite data and genetic pedigree information to guide the genetic management of two long-term conservation programs for endangered populations of salmon: Snake River Sockeye Salmon, Oncorhynchus nerka, and inner Bay of Fundy Atlantic Salmon, Salmo salar. Both programs are captive broodstock (live gene banking) programs for endangered populations of salmon. In order for these programs to be successful for recovery efforts, genetic change, including accumulation of inbreeding, loss of genetic variation, and adaptation to captivity, must be minimized. We provide an overview of each program, describe broodstock selection and pairing for spawning, and discuss how pedigree data are being used to evaluate different management practices. While there are inherent species and programmatic differences, both of these programs use widely accepted genetic conservation strategies (minimize mean kinship, reduce variance in family size, minimize inbreeding in the next generation, maintain large census and effective population size) to potentially mitigate some unintended side-effects associated with the rearing of small populations in captivity. These case studies highlight the benefits and practical limitations of applying these strategies in the genetic management of salmon, and may be used to inform other conservation programs.     

Sarcoptic mange in raccoons in Michigan

Sarcoptic mange is a cause of pruritic skin disease in domestic dogs and a wide range of wildlife species. We describe sarcoptic mange in free-ranging raccoons (Procyon lotor). Three adult raccoons from upper Wayne County, Michigan (USA), were captured, killed, and submitted for diagnostic evaluation. The animals were intensely pruritic, and two had advanced alopecic and crusting lesions over their dorsum and hind limbs. Skin scrapings and skin biopsies revealed crusting and hyperkeratotic dermatitis with high numbers of Sarcoptes scabiei adults, larvae, nymphs, and eggs. These raccoons were not otherwise debilitated, with minimal internal parasites, good body condition, and no evidence of infectious bacterial or viral diseases. Because sarcoptic mange is highly contagious and affects many species, including humans, transiently, it is important that wildlife biologists and rehabilitators include sarcoptic mange in their differential list for raccoons exhibiting pruritus and alopecia.     

Invasive exotic aoudad (Ammotragus lervia) as a major threat to native Iberian ibex (Capra pyrenaica): a habitat suitability model approach

The introduction of alien species to new environments is one of the main threats to the conservation of biodiversity. One particularly problematic example is that of wild ungulates which are increasingly being established in regions outside their natural distribution range due to human hunting interests. Unfortunately, we know little of the effects these large herbivores may have on the host ecosystems. This study deals with a first comparative analysis of the habitat requirements of two ungulate species that may be facing competition for resources in the south of Europe: the native Iberian ibex (Capra pyrenaica) and the exotic aoudad (Ammotragus lervia). The aoudad is a North African caprid introduced in 1970 as a game species in south‐eastern Spain. It has adapted well, and populations have been freely expanding since then. Ecological Niche Factor Analysis is used to describe the realized niche of both species where their distribution ranges merge. Both species occupy marginal areas of rugged terrain in the region. Marginality is higher for the Iberian ibex, which also presents a higher tolerance of secondary environmental gradients than the aoudad. Highly suitable areas for each species are secondarily suitable for the other. Reclassified and cross‐tabulated habitat suitability maps showing the areas of potential spatial coexistence and differences in ecological traits between both species are provided. The results obtained do not allow inferring resource competition between these species. However, current aoudad expansion could result in it invading the favoured habitats of the ibex. Inadequate hunting policy and monitoring, and increasing climatic resemblance of the study region to the native aoudad areas, due to a strong desertification process, are facilitating a high rate of expansion. We strongly recommend to eradicate or, at least, monitor these exotic populations, and promote active conservation practices, if one wants to preserve the unique natural resources present in this European region.     

Parasites and Conservation Biology: The ‘Ibex-Ecosystem’

Parasites, as organisms with a particular way of life, form an important part of biodiversity, not only regarding the number of known species, but also because of their relevant role within ecological processes. These two facts should justify conservation of parasites, at least within natural and protected areas. Little is known about such complex communities of parasites but they are often considered as pests, even out of the fields of public (human) health and animal production, that is, just in the natural environment or under natural conditions. It is increasingly assumed that wildlife diseases, including those produced by parasites, are one of the main bases for managing animal populations. Parasitic diseases may also be managed and, at this point, we can find multiple technical problems which, in certain occasions, lead into philosophical questions or true dilemmas. These considerations are illustrated by revising parasites of the Spanish ibex (Capra pyrenaica), an Iberian mountain ungulate the parasitofauna of which is relatively well known. As a big game species, its trophies become more and more appreciated. Therefore, human dimensions involved in management of its populations are considerably increased. Finally, reasons and opportunities for managing parasitic diseases affecting ibex are revised and discussed, under a global goal or perspective of conserving parasites within natural areas, particularly those that are protected.     

The efficiency of close inbreeding to reduce genetic adaptation to captivity

Although ex situ conservation is indispensable for thousands of species, captive breeding is associated with negative genetic changes: loss of genetic variance and genetic adaptation to captivity that is deleterious in the wild. We used quantitative genetic individual-based simulations to model the effect of genetic management on the evolution of a quantitative trait and the associated fitness of wild-born individuals that are brought to captivity. We also examined the feasibility of the breeding strategies under a scenario of a large number of loci subject to deleterious mutations. We compared two breeding strategies: repeated half-sib mating and a method of minimizing mean coancestry (referred to as gc/mc). Our major finding was that half-sib mating is more effective in reducing genetic adaptation to captivity than the gc/mc method. Moreover, half-sib mating retains larger allelic and adaptive genetic variance. Relative to initial standing variation, the additive variance of the quantitative trait increased under half-sib mating during the sojourn in captivity. Although fragmentation into smaller populations improves the efficiency of the gc/mc method, half-sib mating still performs better in the scenarios tested. Half-sib mating shows two caveats that could mitigate its beneficial effects: low heterozygosity and high risk of extinction when populations are of low fecundity and size and one of the following conditions are met: (i) the strength of selection in captivity is comparable with that in the wild, (ii) deleterious mutations are numerous and only slightly deleterious. Experimental validation of half-sib mating is therefore needed for the advancement of captive breeding programs.     

Carriage of Staphylococcus aureus by Free-Living Wild Animals in Spain

The presence of methicillin-susceptible Staphylococcus aureus (MSSA) was analyzed in different free-living wild animals to assess the genetic diversity and predominant genotypes on each animal species. Samples were taken from the skin and/or nares, and isolates were characterized by spa typing, multilocus sequence typing (MLST) and antimicrobial susceptibility testing. The proportion of MSSA carriers were 5.00, 22.93, 19.78, and 17.67% in Eurasian griffon vulture, Iberian ibex, red deer, and wild boar, respectively (P = 0.057). A higher proportion of isolates (P = 0.000) were recovered from nasal samples (78.51%) than skin samples (21.49%), but the 9.26% of red deer and 18.25% of wild boar would have been undetected if only nasal samples had been tested. Sixty-three different spa types were identified, including 25 new spa types. The most common were t528 (43.59%) in Iberian ibex, t548 and t11212 (15.79% and 14.04%) in red deer, and t3750 (36.11%) in wild boar. By MLST, 27 STs were detected, of which 12 had not been described previously. The most frequent were ST581 for Iberian ibex (48.72%), ST425 for red deer (29.82%), and ST2328 for wild boar (42.36%). Isolates from Eurasian griffon vulture belong to ST133. Host specificity has been observed for the most frequent spa types and STs (P = 0.000). The highest resistance percentage was found against benzylpenicillin (average, 22.2%), although most of the S. aureus isolates were susceptible to all antimicrobial tested. Basically, MSSA isolates were different from those MRSA isolates previously detected in the same animal species.     

Experimental ivermectin treatment of sarcoptic mange and establishment of a mange-free population of Spanish ibex.

Ivermectin was used to treat sarcoptic mange in Spanish ibex (Capra pyrenaica hispanica). Its therapeutic effectiveness was analyzed when it was administered through subcutaneous injection, to sick animals in the consolidation stage of mange (third phase) and, with double injections to chronically affected animals (fourth phase) at a dosage of 0.2 or 0.4 mg/kg body weight (bw). Three wk after treatment, the animals in the third phase of mange treated with a high dose (0.4 mg/kg bw) of ivermectin were completely cured. The same result was achieved after 4 wk of treatment in those animals in phase 3 of mange when 0.2 mg/kg body weight was used. Double injection with ivermectin, even at high doses, did not guarantee the complete cure of all cases of sarcoptic mange in the chronic stage (phase 4); only three of six animals were free of Sarcoptes scabiei. The second experiment consisted on the application of a sanitation program in order to obtain a population of Spanish ibex free from S. scabiei, starting with free-ranging animals, some of them healthy and others sick. After capture the animals were classified as chronically ill, in which case they were excluded from the program, mite carriers and healthy specimens. All the animals were treated first topically with foxim (500 mg/l) and subcutaneously with ivermectin (0.4 mg/kg bw). The infected animals were housed in the treatment pen, and received two doses of ivermectin (0.2 mg/kg bw) at an interval of 15 days, then spent 15 days in the quarantine pen, where they received a further dose before they were included in the pool of healthy animals, and immediately were placed in the quarantine phase. The sanitation we implemented was fully effective in curing the affliction of Spanish ibex affected by S. scabiei.