Diseases of Iberian ibex (Capra pyrenaica).

Iberian ibex (Capra pyrenaica) is an ecologically and economically relevant medium-sized emblematic mountain ungulate. Diseases participate in the population dynamics of the species as a regulating agent, but can also threaten the conservation and viability of vulnerable population units. Moreover, Iberian ibex can also be a carrier or even a reservoir of pathogens shared with domestic animals and/or humans, being therefore a concern for livestock and public health. The objective of this review is to compile the currently available knowledge on (1) diseases of Iberian ibex, presented according to their relevance on the health and demography of free-ranging populations; (2) diseases subjected to heath surveillance plans; (3) other diseases reported in the species; and (4) diseases with particular relevance in captive Iberian ibex populations. The systematic review of all the information on diseases affecting the species unveils unpublished reports, scientific communications in meetings, and scientific articles, allowing the first comprehensive compilation of Iberian ibex diseases. This review identifies the gaps in knowledge regarding pathogenesis, immune response, diagnostic methods, treatment, and management of diseases in Iberian ibex, providing a base for future research. Moreover, this challenges wildlife and livestock disease and wildlife population managers to assess the priorities and policies currently implemented in Iberian ibex health surveillance and monitoring and disease management.

First record of Pharyngomyia picta (Diptera: Oestridae) parasitizing Cervus elaphus in Sierra Nevada National Park.

The necropsy made to two adult individuals of red deer shot in Sierra Nevada National Park revealed infestation by second- and third-instar larvae of the oestrid Pharyngomyia picta (Meigen 1824). The animals were shot in Dehesa de las Hoyas, about 2000 m above sea level. This is the first record of this parasite in Sierra Nevada National Park. Furthermore, the occurrence of adult P. picta at this altitude could indicate significant changes of the climatic conditions, now matching better the environmental requirements of this bot fly. Its monitoring may, therefore, be of great help for detecting global change signs.

Development and characterization of 15 novel polymorphic microsatellite loci for two important bot flies (Diptera, Oestridae) by next-generation sequencing.

Cephenemyia stimulator and Oestrus ovis are two important parasitic bot flies (Oestridae) species causing myiasis, with a potential negative impact on the welfare of the host. Using next-generation sequencing approach and bioinformatics tools, a large panel of possible microsatellites loci was obtained in both species. Primer pairs were designed for 15 selected microsatellite loci in C. stimulator and other 15 loci in O. ovis for PCR amplification. Loci amplification and analysis were performed in four populations of each species. The results demonstrated that all selected loci were polymorphic, with the number of alleles ranging from 2 to 6 per locus in C. stimulator and 3 to 13 per locus in O. ovis. This is the first time to describe these microsatellite loci for C. stimulator and O. ovis. These two sets of microsatellite markers could be further used for biogeographic and population genetics studies.

Individual stress responses to Sarcoptes scabiei infestation in Iberian ibex, Capra pyrenaica.

In this study we have monitored the stress of Iberian ibex at individual level within the course of an experimental infection with Sarcoptes scabiei mites. For this purpose we have measured faecal 11-ketoetiocholanolone (11-k) using high-performance liquid chromatography coupled with tandem mass spectrometry (HPLC-MS/MS). We used linear mixed models to explore the effects of host sex and age, clinic (mange status) and time (number of days post-infection) on the concentration of faecal 11-k. The most parsimonious model included clinic, time and host age, which explained 76.6% of the variance of the response variable. Moreover, the concentration of faecal 11-k varied greatly between individuals. Our results evidence the stressor nature of the disease and highlight the negative effects on hosts due to cortisol release and activity.

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).

Characterizing the growth of Sarcoptes scabiei infrapopulations.

During the course of parasitic disease infestations, parasite population sizes change at both individual host (infrapopulation) and host population (metapopulation) levels. However, most studies only report epidemiological values for specific locations and times. In this study we analysed the dynamics of several Sarcoptes scabiei infrapopulations from experimentally infested Iberian ibex, Capra pyrenaica. We obtained mite counts by digesting small skin biopsies, which we compared with indices obtained from histopathological analyses performed on adjacent skin biopsies. We obtained the finite growth rate and the daily growth rate for the mite infrapopulations: mean ± SE = 11.53 ± 10.17 and 0.10 ± 0.08 mites/day, respectively. Mite counts derived from skin sample digestion did not correlate with the histological mite indices obtained from adjacent skin biopsies. At a metapopulational level, both indices of mite abundance were modelled using GLMMs and the factors influencing their variation are analysed and discussed. Our results suggest that mites are not distributed uniformly over the whole area of the skin lesion. Therefore, direct diagnoses of mange and mite counts could be inaccurate if only small skin samples are used.

First report of oestrosis in aoudad from southeastern Spain.

In spring 2016, we analyzed the skull of 44 aoudads (Ammotragus lervia) from Sierra Espuña Regional Park (SE Spain) for the presence of oestrid larvae. Oestrus ovis larvae were found in 27.3% of sampled hosts, with a mean intensity of 1.5 ± 6.1 larvae/per parasitized host (range 1-21). To our knowledge, this is the first report of oestrosis affecting this host species.

Toxic and Essential Element Concentrations in Iberian Ibex (Capra pyrenaica) from the Sierra Nevada Natural Park (Spain): Reference Intervals in Whole Blood.

Iberian ibex (Capra pyrenaica) blood samples from the Sierra Nevada Natural Park (Spain) were analyzed to establish concentrations of toxic and essential elements. Samples (whole blood from 32 males and 34 females) were taken from wild animals and the concentrations of inorganic elements considered as (1) non-essential and toxic (Pb, Cd and As), (2) essential but potentially toxic (Cu, Zn and Mn) and (3) occasionally beneficial (B, Cr, Al and Ni), as well as (4) essential minerals (Ca, Na, K, P, Mg, S, Co and Fe), were analyzed. The low concentration of Pb and Cd indicated that there is no heavy metal contamination in this geographical area for these elements. The concentration of elements in this ibex population was defined for different genders and ages. Significant differences between genders were only found for Mg and Cu, while significant differences in concentrations of Ca, Cr, Fe, Mn, P, S and Zn were found between ages.

Postural laterality in Iberian ibex Capra pyrenaica: effects of age, sex and nursing suggest stress and social information.

Most studies of lateralized behaviour have to date focused on active behaviour such as sensorial perception and locomotion and little is known about lateralized postures, such as lying, that can potentially magnify the effectiveness of lateralized perception and reaction. Moreover, the relative importance of factors such as sex, age and the stress associated with social status in laterality is now a subject of increasing interest. In this study, we assess the importance of sex, age and reproductive investment in females in lying laterality in the Iberian ibex (Capra pyrenaica). Using generalized additive models under an information-theoretic approach based on the Akaike information criterion, we analyzed lying laterality of 78 individually marked ibexes. Sex, age and nursing appeared as key factors associated, in interaction and non-linearly, with lying laterality. Beyond the benefits of studying laterality with non-linear models, our results highlight the fact that a combination of static factors such as sex, and dynamic factors such as age and stress associated with parental care, are associated with postural laterality.

How many threatened lice are there? An approximation to the red list of the Spanish Phthiraptera.

Although the idea of conserving parasites as part of biodiversity is not new, these in general and lice in particular, are not included in the threatened list of invertebrate fauna. Assuming that the conservation status of a lice species is similar to that of its host, the number of threatened lice within the Spanish entomofauna was estimated based on the known host-lice assemblages. The lice parasitizing many of the Spanish birds and mammals are unknown. Overall, I found 6 extinct (EX) species; 4 critically endangered (CR); 15 endangered (EN), 7 vulnerable (VU) and 1 species near threatened (NT), at regional level. Since the status of hosts varies through time and space, it, (together with those of their lice, must be periodically updated. In addition to a number of reasons that justify the conservation of parasites, lice deserve being conserved, particularly, because of their scientific value.

In vitro acaricidal activity of several natural products against ibex-derived Sarcoptes scabiei.

In this study we analysed the effect of the temperature, diverse strains of Bacillus thuringiensis, Lysinibacillus sphaericus and nanoformulations with essential plant oils (EONP) on the survival of Sarcoptes scabiei mites derived from naturally-infested Iberian ibex (Capra pyrenaica). In general, mites maintained at 12ºC survived more than those maintained at 35ºC (40.7 hr and 31.2 hr, respectively). Mites with no treatment survived 27.6 h on average. Mites treated with B. thuringiensis serovar. konkukian and geranium EONP showed significant reduction in their survival. Despite the fact that these agents seem to be promising candidates for controlling sarcoptic mange in the field, further research is still needed to get stable, efficient and eco-friendly acaricides.

Home range in genus Capra: from polygons to Brownian bridges of scabietic and healthy Iberian ibexes (Capra pyrenaica).

Home range and home range overlap can be used to describe use of space and movement of wildlife. During the last years, advancements in technology have greatly improved our understanding of animal movement, especially among large herbivores. Wild ungulate abundance and distribution have increased in temperate areas. Moreover, their diseases-including sarcoptic mange in the Iberian Ibex (Capra pyrenaica)-have become a cause of concern for livestock, public health, and wildlife conservation. In this study, we first reviewed existing literature on the home range of species in the genus Capra. We then analyzed data from 52 GPS-GSM-collared Iberian ibexes, of which 33 were healthy and 19 were affected by sarcoptic mange from 3 different populations in the southeastern Iberian Peninsula to analyze: (1) differences in size and characteristics of home ranges obtained by the 3 most commonly used methodologies-minimum convex polygon, kernel density estimation, and Brownian bridges movement models (BBMMs); and (2) the impact of endemic sarcoptic mange on Iberian Ibex home range. The literature review revealed that available information on spatial behavior of Capra spp. was based only on 3 species, including the Iberian Ibex, estimated through a diversity of methods which made it difficult to compare results. We found positive correlations among the different home range estimation methods in the Iberian Ibex, with BBMMs proving to be the most accurate. This study is the first to use BBMMs for estimating home range in this species, and it revealed a marked seasonal behavior in spatial use, although sarcoptic mange smoothed such seasonal pattern. The seasonal overlaps obtained suggest that core areas of the Iberian Ibex change within wider home range areas, which are ecological parameters relevant to identifying key areas for species management and conservation.

Detailed morphological structure and phylogenetic relationships of Degeeriella punctifer (Phthiraptera: Philopteridae), a parasite of the bearded vulture Gypaetus barbatus (Accipitriformes: Accipitridae).

Habitat loss is one of the main threats to species survival and, in the case of parasites, it is their hosts that provide their habitat. Therefore, extinction even at local scale of host taxa also implies the extinction of their parasites in a process known as co-extinction. This is the case of the bearded vulture (Gypaetus barbatus), which almost became extinct at the beginning of the twentieth century. After several attempts, this species was successfully reintroduced into the Alps at the end of the twentieth century. We collected 25 lice specimens from an electrocuted bearded vulture from Susa (Italian Alps) that were morphologically identified as Degeeriella punctifer. Six individuals were studied by scanning electron microscopy, with particular emphasis on their cephalic sensorial structures, while four further specimens were characterized at molecular level by amplifying partial regions of the 12SrRNA, COX1 and elongation factor 1 alpha (EF-1) genes. From a morphological perspective, the number, type and arrangement of the sensillae on the two distal antennal segments is quite similar to that of other species of the family Philopteridae (Phthiraptera: Ischnocera). The mandibles and tarsal claws allow lice to cling firmly to their host's feathers. Phylogenetic analyses help unravel the paraphyletic nature of the genus Degeeriella and demonstrate the clear differentiation between lice parasitizing Accipitriformes and Falconiformes, as well as the close relationship between D. punctifer, D. fulva, D. nisus and Capraiella sp. that, along with other genera, parasitize rollers (Aves: Coraciiformes).

Co-infection patterns in the ectoparasitic community affecting the Iberian ibex Capra pyrenaica.

BACKGROUND: Sarcoptic mange is one of the main parasitic diseases affecting the Iberian ibex Capra pyrenaica. Scabietic animals suffer a decline in body condition and reproductive fitness and in severe cases may die. Although several previous studies of the pathology of this disease and the physiological changes it produces in ibex have been carried out in recent years, our knowledge of the relationship between Sarcoptes scabiei and other ectoparasites of this host is still limited. METHODS: We analysed 430 Iberian ibex skin samples. Ectoparasites were removed, counted and identified. Mite (S. scabiei) numbers were obtained after digesting the skin samples in a 5% KOH solution. We modelled mite numbers in terms of host sex and age, site, year, season and the presence of other ectoparasites such as ticks and lice using generalized linear mixed models (GLMMs) and ectoparasite co-occurrence patterns using two different models: the probabilistic model species co-occurrence and the generalized linear latent variable model (GLLVM). RESULTS: The ectoparasite community was mainly composed of S. scabiei, six ticks (Haemaphysalis sulcata, Haemaphysalis punctata, Rhipicephalus bursa, Rhipicephalus turanicus, Dermacentor marginatus and Ixodes ricinus) and two lice (Bovicola crassipes and Linognathus stenopsis). Adult male ibex harboured more mites than females. Mite numbers varied greatly spatially and seasonally and increased with the presence of other parasites. Some positive co-occurrence relationships between pairs of different ectoparasites were observed, particularly between ticks. The presence of S. scabiei negatively affected lice and H. sulcata numbers. CONCLUSIONS: Sarcoptic mange has spread above all in ibex populations in and around the Mediterranean Basin, where it is now found in almost a third of its host's range. Mite numbers varied seasonally and spatially and were higher in male hosts. The presence of S. scabiei had a negative effect on lice numbers but favoured the presence of ticks.

The local skin cellular immune response determines the clinical outcome of sarcoptic mange in Iberian ibex (Capra pyrenaica).

Introduction: Sarcoptic mange, caused by Sarcoptes scabiei, is a disease with implications for wildlife conservation and management. Its severity depends on the host's local skin immune response, which is largely unknown in Iberian ibex (Capra pyrenaica), a mountain ungulate dramatically affected by mange. In this species, the clinical outcome of sarcoptic mange varies among individuals, and the local immune response could be key to controlling the infestation. This study aims to characterize the local cellular immune response and its relationship with the clinical outcome. Methods: Fourteen Iberian ibexes were experimentally infested with S. scabiei and six more served as controls. Clinical signs were monitored, and skin biopsies were collected from the withers at 26, 46, and 103 days post-infection (dpi). The presence and distribution of macrophages (including M1 and M2 phenotypes), T lymphocytes, B lymphocytes, plasma cells, and interleukine 10 were quantitatively evaluated using immunohistochemical techniques. Results: An inflammatory infiltrate that decreased significantly from 26 to 103 dpi was observed in all the infested ibexes. The predominant inflammatory cell population in the skin of the mangy ibexes was formed by macrophages (mainly the M2 phenotype) followed by T lymphocytes, with lower numbers of B lymphocytes and plasma cells. Three clinical courses were identified: total recovery, partial recovery, and terminal stage. The inflammatory infiltrates were less pronounced in the fully recovered ibexes than in those that progressed to the terminal stage throughout the study. Discussion: The results suggest an exacerbated but effective Th1-type cellular immune response controlling mange in Iberian ibex. Furthermore, the local immune response appears to determine the variability of the clinical responses to S. scabiei infestation in this species. This first report on the progression of local skin immune cells is relevant not only for individuals but also for population management and conservation.

Monitoring bluetongue virus vectors in Andalusia (SW Europe): Culicoides species composition and factors affecting capture rates of the biting midge Culicoides imicola.

In this work, we summarize the results of captures of Culicoides species in Andalusia (S Spain) during 2007-2008. Four out of the 15 midge species-Culicoides imicola, Culicoides obsoletus complex, Culicoides pulicaris complex, and Culicoides nubeculosus-accounted for 80.7 % of captures (n = 68,190). Captures were seasonal and mostly occurred in May-November. The overall number of Culicoides specimens captured and the mean number of caught per trap were higher in 2007. We used an information-theoretic approach to analyze whether environmental factors (e.g., weather, altitude above the sea level, distance of the trap from the ground, distance to animals, and land use) affected C. imicola capture probability and success. Mean temperature and rainfall (both integrated into the Gaussen index), distance of traps to host animals, and trap height above the ground were the main factors explaining variance in capture rates in the Bluetongue Entomologic Surveillance Andalusian Program (BESAP). However, all of these patterns strongly varied among traps. As previously remarked by other authors, standardized capture methods and protocols for trap use are needed to ensure that results obtained in different geographical areas and/or periods are comparable.

First Study of Pharingomyia picta and Cephanemyia auribarbis in Wild Populations of Red Deer (Cervus elaphus) in Portugal.

Nasopharyngeal myiasis in red deer has never been studied in Portugal. For this reason, from December 2015 to February 2016 a study was derived on hunted red deer in Idanha-a-Nova county to evaluate the Diptera larvae presence. During the initial examination on the spot, the larvae was analysed at the nasopharynx. When present, larvae were collected for further species identification. The infestation prevalence was 50.6 ± 7.61% (CI 95%), and the mean parasitism intensity was 11.38 larvae per affected host. Two larvae species were found, Pharyngomyia picta and Cephenemyia auribarbis, both on single or concomitant infection, with the first species having a higher prevalence and mean infestation intensity than the second. The larvae's prevalence was significantly higher (X2 = 4.35; p = 0.0370) in males (62.16 ± 11.05%) than in females (41.30 ± 10.06%). Within age groups, younger animals showed a higher prevalence. This study shows the presence of P. picta and C. auribarbis larvae in the wild red deer population in Portugal for the first time. The high parasitic prevalence and mean intensity highlight the importance of this parasitosis in this wild species. For this reason, more scientific research is required to accurately assess its prevalence in other geographic areas, and evaluate the risk factors as well effects of this parasitosis on the deer population.

Epidemiology of Trichinella infection in wild boar from Spain and its impact on human health during the period 2006-2019.

Trichinellosis is a notifiable zoonotic disease caused by parasitic nematode larvae belonging to the genus Trichinella. Domestic pig and wild boar are important hosts within the natural cycle of T. spiralis, the last one being an animal whose populations have experienced an important growth. Therefore, this paper studies the prevalence of Trichinella infection in wild boar in Spain, as well as its relation with hunting and its impact on public health during the period 2006-2019. For this purpose, different sources of information were consulted and analyzed depending on the autonomous communities of Spain and years. During the fourteen years of study, the number of wild boars hunted and the number of cases of Trichinella infection in them increased (from 172 cases in 2006 to 421 in 2019), although prevalence values remained low as the number of animals analyzed also increased. On the other hand, trichinellosis in humans tended to decrease (from a peak of 107 cases in 2007 to 11 cases in 2019). Nevertheless, the numbers of both wild boars and humans infected with Trichinella in Spain are among the highest in Europe, and this emphasizes the importance of food safety, sanitary controls of game meat and citizen awareness campaigns, which prevent the spread of Trichinella through the human population.

Drivers of the Ectoparasite Community and Co-Infection Patterns in Rural and Urban Burrowing Owls.

Urbanization creates new ecological conditions that can affect biodiversity at all levels, including the diversity and prevalence of parasites of species that may occupy these environments. However, few studies have compared bird-ectoparasite interactions between urban and rural individuals. Here, we analyze the ectoparasite community and co-infection patterns of urban and rural burrowing owls, Athene cunicularia, to assess the influence of host traits (i.e., sex, age, and weight), and environmental factors (i.e., number of conspecifics per nest, habitat type and aridity) on its composition. Ectoparasites of burrowing owls included two lice, one flea, and one mite. The overall prevalence for mites, lice and fleas was 1.75%, 8.76% and 3.50%, respectively. A clear pattern of co-infection was detected between mites and fleas and, to less extent, between mites and lice. Adult owls harbored fewer ectoparasites than nestlings, and adult females harbored more lice than males. Our results also show that mite and flea numbers were higher when more conspecifics cohabited the same burrow, while lice showed the opposite pattern. Rural individuals showed higher flea parasitism and lower mite parasitism than urban birds. Moreover, mite numbers were negatively correlated with aridity and host weight. Although the ectoparasitic load of burrowing owls appears to be influenced by individual age, sex, number of conspecifics per nest, and habitat characteristics, the pattern of co-infection found among ectoparasites could also be mediated by unexplored factors such as host immune response, which deserves further research.