Valldeperes et al. Parasites Vectors (2019) 12:405 https://doi.org/10.1186/s13071-019-3665-7 Parasites & Vectors SHORT REPORT Open Access How sensitive and specific is the visual diagnosis of sarcoptic mange in free‑ranging Iberian ibexes? Marta Valldeperes1 , José Enrique Granados2, Jesús María Pérez3 , Inmaculada Castro3, Arián Ráez‑Bravo1, Paulino Fandos4, Jorge Ramón López‑Olvera1, Emmanuel Serrano1,5* and Gregorio Mentaberre1,6 Abstract Background: Sarcoptic mange is a broadly distributed parasitic disease caused by Sarcoptes scabiei that affects wild mammals from all over the world, including the Iberian ibex (Capra pyrenaica). Selective culling of the scabietic individuals is the main management measure for disease control in Iberian ibex populations. Although visual identifi‑ cation of mange-compatible lesions is the reference method to decide the target individual, both false negative and positive cases are common in the wild. The aim of this work is to determine the sensitivity (SE), and the specificity (SP) of selective culling after evaluating 403 ibexes hunted in the Sierra Nevada Nature Space for sarcoptic mange control between 2002 and 2015. Methods: A combination of skin scrapings and potassium hidroxide (KOH) skin digestion was used for sarcoptic mange diagnosis. Generalized linear models (GLM) were used to assess the effects of sex, age (juveniles and adults) and period of the year (wet and dry periods) on the SE and SP of the visual diagnosis method. Results: The SE obtained for the visual determination of scabietic ibexes was 87.14%, whereas the SP was 60.71%. According to our model selection, SE of the visual diagnosis was explained by the additive effects of age and the period of the year. In fact, SE was lower in juveniles (64.76%) than in adults (94.26%) and during the dry period (73.44%) as compared to the wet period (92.09%). On the other hand, SP was best explained by the GLM including the additive effects of sex and the period of the year. The visual diagnosis of sarcoptic mange resulted less specific in females (22.73%) than in males (74.19%) and during the wet (55.22%) than in the dry period (82.35%). Conclusions: Maximizing SE and SP is essential to achieving a high rate of removal of affected individuals from the environment without eliminating potentially resistant individuals. Selective culling must be conservative during the wet period and with females due to the lower SP. Conversely, visual diagnosis of scabietic juveniles and during the dry period has to be improved, due to the lower SE. Keywords: Capra pyrenaica, Sarcoptes scabiei, Selective culling, Visual diagnostic, Wildlife disease management *Correspondence: emmanuel.serrano@uab.cat 1 Wildlife Ecology & Health group (WE&H) and Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona (UAB), 08190 Bellaterra, Barcelona, Spain Full list of author information is available at the end of the article © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat​iveco​mmons​.org/ publi​cdoma​in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Valldeperes et al. Parasites Vectors (2019) 12:405 Page 2 of 7 Background generally based on the selective culling of individuals Sarcoptic mange is a parasitic disease caused by Sar- with sarcoptic mange compatible lesions and pruritus, coptes scabiei reported in at least 104 mammal species as the main clinical sign [3, 12, 17, 23, 24], as well as the from 27 families and 10 orders, responsible for wild- administration of antiparasitic drugs such as ivermec- life population collapses all over the world [1–3]. These tin or amitraz [5, 6, 10, 12]. The characteristic lesions of include: carnivores, e.g. coyote (Canis latrans) [4], chee- sarcoptic mange include erythematous eruptions, pap- tah (Acinonyx jubatus) [5], Eurasian lynx (Lynx lynx) [3, ules, seborrhoea, severe alopecia, crusts, hyperkerato- 6], red fox (Vulpes vulpes) [6, 7] and pine marten (Martes sis and skin lichenification, dermal fissures, eyelid and martes) [6]; marsupials, e.g. wombat (Vombatus ursinus) lip inflammation and, finally, systemic signs as dehydra- [8, 9], koala (Phascolarctos cinereus) [10]; and ungulates, tion and emaciation [1, 2, 12, 13, 15]. e.g. chamois (Rupicapra pyrenaica) [11] and Iberian ibex It is presumed that individuals showing a high pro- (Capra pyrenaica) [12, 13], among others. Despite the portion of damaged skin commonly carry higher mite fact that it has led some populations almost to extinction burden than their less affected counterparts. However, [7, 8, 12, 13], survival of scabietic animals is not rare [14, the individual hypersensitivity response to a given par- 15] (Fig. 1). Once a population is affected by sarcoptic asite burden is in great measure what determines the mange, it remains endemic re-emerging cyclically with outcome of sarcoptic mange infestation [2]. On the lower virulence [3, 12, 16]. other hand, mite burden for a given skin surface can Sarcoptic mange pathology depends on the host and vary seasonally [25]. the environmental conditions. It is typically seasonal [17], Nevertheless, other skin disorders also result in alo- peaking in late winter and spring, when low temperatures pecia, crusts and scales, making it difficult to confirm and high humidity favour the survival and reproduction the visual diagnosis of sarcoptic mange in severely of adult mites [18, 19]. Sexual differences in the preva- affected individuals [26] (Fig. 2). These alterations may lence of sarcoptic mange [17, 20] could be explained by include pemphigus complex, dermatophytosis and der- gender differences in the immune response against the matophilosis, other fungal and bacterial dermatitis, mite [21, 22]. In addition, prevalence differences amongst nutritional imbalances, chorioptic mange, louse, flea age classes have also been reported in mammals, includ- and tick infestations [27, 28], and photo-sensitization, ing wild ungulates, with adults often being more suscep- among others [29]. Furthermore, in early summer tible [11, 12, 16]. As a result, sarcoptic mange outbreaks ibexes molt fur to get the summer coat, presenting an commonly happen in early spring, mostly affecting adult unhealthy appearance in the eyes of an unexperienced males [17, 20]. observer. This emphasizes the need to confirm the vis- Measures for sarcoptic mange control are often ual diagnosis with additional tests, such as potassium implemented to mitigate the impact of the disease on hydroxide (KOH) digestion of the skin with observation wildlife populations, as well as for social and politi- of the mites, ova or faecal pellets under microscopic cal concerns. In field conditions, these measures are scrutiny [30, 31]. Fig. 1 Iberian ibex recovering from sarcoptic mange experimental infestation in SNNS showing healing lesions. New hair is growing Fig. 2 Iberian ibex showing severe alopecia; however, skin scrapings within the old lesions and skin digestions were negative for S. scabiei detection Valldeperes et al. Parasites Vectors (2019) 12:405 Page 3 of 7 Visual diagnosis of sarcoptic mange is the reference > 75%) and then culled as part of previously mentioned field method used not only in wildlife disease research population management programme in the SNNS. In [32] but also in actions for disease control in free ranging addition, sex, age (kid, 0 years; yearling, 1 to 2 years; populations confirmed outbreaks [33]. Few efforts, how- juveniles, 2 to 4 years; and adults, > 4 years), season ever, have been made to determine sensitivity (SE) and and localization were recorded for every ibex. Finally, specificity (SP) of this “visual test and slaughter” method. the diagnosis of sarcoptic mange was confirmed by skin Although there is a need to assess the accuracy of this scrapings and/or KOH digestion (when negative scrap- procedure [25, 31], the effects of age, sex and season on ing was obtained). The combination of these two meth- the SE and SP of visual diagnosis of sarcoptic mange on ods was considered as the gold standard in this study. the field remain untested. Detailed information about the diagnostic procedures The Iberian ibex is a medium-sized mountain ungulate can be found in Pérez et al. [25]. Fifty-six ibexes show- and an excellent model to evaluate the SP and SE of field ing 1–25% of affectation (category 1) were excluded visual diagnosis of sarcoptic mange due to: (i) high sexual from the study because of the potential bias during dimorphism; (ii) easy determination of age; and (iii) exist- the visual diagnosis, as they are the hardest to classify ence of different stages of mange infestation in wild pop- and could thus lead to a higher error in field conditions ulations. Since the first detection of sarcoptic mange in [13]. Thus, only 347 Iberian ibexes were finally included 1992 [17, 27] in the Iberian ibex population of the Sierra in the study (3 kid females and 5 kid males, 13 yearling Nevada Natural Space (Including both the National and females and 19 yearling males, 22 juvenile females and Natural Park, SNNS hereafter), selective culling of indi- 116 juvenile males, 78 adult females and 70 adult males, viduals showing sarcoptic mange compatible lesions has 29 with unrecorded sex and/or age). been applied, together with the habitual hunting plan for population management purposes. On the other hand, individuals in this population have a strong seasonal pat- Statistical procedures tern of body reserves [34] that is partly driven by mange To assess the sex, age and period of the year effects on the infestation [20], particularly during winter [35]. SE and SP of our visual diagnosis method for detecting The aim of this study is to determine the SE and SP of scabietic ibexes we used specific generalized linear mod- the visual diagnosis of sarcoptic mange in Iberian ibex els (GLM) with a binomial error distribution and “logit” spotted during field prospections in the SNNS, and to link function. The GLM for SE used a binomial vari- explore the individual (age and sex) and environmen- able as a response variable: 1 for false positive individual tal (period of the year) effects on the SE and SP of this and 0 otherwise; whereas the GLM for SP used: 1 for method. The information obtained should be useful to false negative individual and 0 otherwise. A false positive improve strategies oriented to improve sarcoptic mange (FP) was considered the case where an Iberian ibex was management and control strategies in wild ungulate visually diagnosed as scabietic, but then was both nega- populations. tive to skin scrapings and skin digestions. A false negative (FN) was considered the case where a visually-diagnosed Methods healthy ibex was subsequently found to have S. scabiei This work was performed with data obtained for the mites either in the skin scrapings or the skin digestions. study of Pérez et al. [25] and with data collected from the True positives (TP) or true negatives (TN) were animals management programme of the Iberian ibex in SNNS. properly diagnosed as infected or uninfected individuals. The explanatory variables where the same in both cases: Animals and sampling sex (males, n = 210; females, n = 116), age class (kids, n Four hundred and three Iberian ibexes culled between = 8; yearlings, n = 32; juveniles, n = 132; adults, n = 148) 2002 and 2015 in the SNNS, southern Spain (36°00′– and the period of the year [dry (summer and autumn), n 37°10′N, 2°34′–3°40′W), were included in this work. = 99; wet (winter and spring), n = 246]. Model selection These were ibexes presenting sarcoptic mange compat- was based on the lowest Akaike information criterion ible lesions, but also apparently healthy ones that were (AIC) [36]. killed either as part of the usual population management Finally, SP and SE estimations were based on Altman programme or through game hunting (females, kids, & Bland [37]: juveniles and trophy-hunted males). Sensitivity = TP / TP + FN The ibexes were first visually classified in five catego- Specificity = TN / TN + FP ries of sarcoptic mange affectation (0, no skin lesions; Statistical procedures were performed using the R 1, 1–25% of the skin affected; 2, 25–50%; 3, 50–75%; 4, software 3.2.2 version. Valldeperes et al. Parasites Vectors (2019) 12:405 Page 4 of 7 Results Table 2 Model selection for exploring the best generalized SE and SP of the visual determination of mangy ani- linear model (GLM) explaining specificity variance of the visual mals were 87.14 and 60.71%, respectively. The model detection of mange in 347 Iberian ibexes. In bold, the model selection indicated age class and period of the year as with substantial support for being the best model the main factors explaining SE (Table 1), while sex and GLM K AIC ΔAIC Wi period of the year were main factors for SP (Table 2). Sex + Period 3 209.91 0.00 0.42 The best model for SE included the additive effects Sex × Period 4 211.24 1.37 0.21 of age class and period of the year, explaining 13.84% Period 2 211.57 1.63 0.19 of the observed variance (Table 1). In particular, juve- Sex 2 213.33 3.39 0.08 niles were more prone to be false negative than adults AgeClass + Period 5 214.27 4.45 0.04 (βjuveniles = 1.4603 ± 0.4716, Z = 3.096, P = 0.00196) and Sex × Period + AgeClass 7 215.11 5.43 0.03 ibexes were more likely to be detected as false negatives AgeClass × Period 8 217.21 7.60 < 0.01 during the dry period than the wet period (βwet period = Sex + AgeClass 5 217.57 7.75 < 0.01 − 1.6736 ± 0.4104, Z = − 4.078, P = 4.55e−05). Spe- Sex × AgeClass + Period 9 218.76 8.89 < 0.01 cifically, juveniles [odds ratio (OR) = ­e1.46 = 4.30] were AgeClass 4 218.76 8.89 < 0.01 4.30 times more likely to be false negative than adults, Sex × AgeClass 8 222.61 13.00 < 0.01 and in the dry period (OR = 1/0.19 = 5.26) the prob- ability of false negative diagnosis was 5.26 higher than GLM: Generalized linear model; K: degrees of freedom, estimated parameters in the model; AIC: Akaike’s information criterion; ΔAIC: difference of AIC with in the wet period (OR = ­e−1.67 = 0.19). Hence, SE was respect to the best model; Wi: Akaike’s weight significantly higher in the wet period than in the dry one (92.01 vs 73.44%, P < 0.001) and for adults as com- pared to juveniles (94.26 vs 64.76%, P < 0.01) (Table 3). Table 3 Sensitivity and specificity of the visual diagnosis of No significant differences in SE were observed for kids sarcoptic mange in 347 Iberian ibexes (kid, yearling, juvenile and yearlings. and adult) culled in Sierra Nevada Natural Space during the wet The best model for SP included the additive effects of (winter and spring) and the dry periods (summer and autumn) sex and period of the year, explaining 4.39% of the vari- of the year. P-values were obtained from the generalized linear models (GLMs) proposed to explain the sensitivity and specificity, ance (Table 2). Specifically, females were more often which included the variables age, sex and period of the year detected as false positives than males (βmale =-0.6896 ± 0.3727, Z = -1.850, P = 0.0643) and in the wet period Parameters involved in the GLMs P-value individuals were more likely detected as false positives Sensitivity (%) Dry period (73.44) Wet period (92.09) < 0.0001 than in the dry period (βwet period =1.2503 ± 0.6218, Z = Juveniles (64.76) Adults (94.26) 0.00196 2.011, P = 0.0443). Specificity (%) Wet period (55.22) Dry period (82.35) 0.0443 Females (22.73) Males (74.19) 0.0643 Table 1 Model selection for exploring the best generalized linear model (GLM) explaining sensitivity variance of the visual Females (OR = 1/0.50 = 2) are two times more prob- detection of mange in 347 Iberian ibexes. In bold, the model able to be found as a false positive than males (OR = with substantial support for being the best model ­e−0.69= 0.50) and ibexes spotted in the wet period are 3.49 GLM K AIC ΔAIC Wi times more likely to be diagnosed as false positive than in AgeClass + Period 5 182.25 0.00 0.58 the dry period (OR = ­e1.25 = 3.49). Thus, visual diagnosis Sex × Period + AgeClass 7 183.86 1.75 0.24 SP was significantly higher for males than females (74.19 Sex × AgeClass + Period 9 184.99 3.05 0.13 vs 22.73%, P < 0.1) and in the dry period compared to the AgeClass × Period 8 187.91 5.88 0.03 wet period (82.35 vs 55.22%, P < 0.05; Table 3). Sex + Period 3 190.51 8.17 < 0.01 Sex × Period 4 190.62 8.33 < 0.01 Discussion Period 2 194.44 12.07 < 0.01 Visual diagnosis of sarcoptic mange aimed at managing AgeClass 4 196.95 14.65 < 0.01 the disease through selective culling is more sensitive Sex + AgeClass 5 198.65 16.40 < 0.01 than specific, resulting in a neglected bias seeking for Sex × AgeClass 8 200.71 18.68 < 0.01 sick ibexes in field conditions. These results contrast with Sex 2 203.46 21.09 < 0.01 previous studies reporting a SE of 60% and a SP of 100% for visual diagnosis of sarcoptic mange in the same host GLM: Generalized linear model; K: degrees of freedom, estimated parameters in the model; AIC: Akaike’s information criterion; ΔAIC: difference of AIC with species [31]. However, the fact that no skin digestions in respect to the best model; Wi: Akaike’s weight healthy individuals were performed by Arenas et al. [31] Valldeperes et al. Parasites Vectors (2019) 12:405 Page 5 of 7 hampers any comparison with our results. Moreover, in intensity [31, 47–50] and mortality [49], and females diagnosis based on clinical signs and lesions, SE depends are normally the immunological stronger gender [21]. on the threshold established to consider a positive diag- Although some species, such as wolves or chamois, do nosis and SP has been observed to be low in human sca- not show sex-bias for the presence of mange-compati- bies studies. Generally, even by adding skin scrapings to ble lesions [11, 24, 43], in other species such as the red visual diagnosis, SE below 50% is common in the scien- deer or aoudad (Ammotragus lervia) sarcoptic mange tific literature [38, 39]. is more prevalent in males than in females [16, 40]. High relative humidity and low temperatures favour S. Similarly, sex is a determining factor for the immune scabiei survival [17, 40], especially when they are off the response to sarcoptic mange in Iberian ibexes. Females host, directly affecting the viability of the mite [18, 41]. In have higher specific acquired response to infestation experimental infestations, lesions were more pronounced and re-infestation than males [22]. In addition, female in moistened areas of skin, increasing the weakness of the Iberian ibexes show lower mange prevalence, better stratum corneum, facilitating mite burrowing [42]. Thus, body condition when infested and are less prone to in a wet and colder environment more severe lesions can develop severe stages of mange than males [20]. The be seen than in dry conditions with the same number lower prevalence and milder lesions of females may of mites [25], and mites commonly increase in number explain the lower SP of visual diagnosis of sarcopic as they are favoured by the weather. Conversely, sum- mange, increasing the difficulty to identify them as mer is the most unfavourable season for S. scabiei [17], scabietic. Conversely, more prevalent and more often as high temperatures and low humidity may cause their severely affected males are more likely to be correctly early death [18]. Accordingly, sarcoptic mange usually classified as affected by sarcoptic mange, showing a reaches its highest prevalence in winter and spring (the better SP. wet period) [17], not only in the Iberian ibex but also in Lower prevalence of mange-compatible lesions in other species, such as the red deer (Cervus elaphus) and juveniles as compared to adults has been repeatedly Iberian wolf (Canis lupus signatus) [40, 43]. These envi- reported in several species, including Iberian wolves ronmental effects on mites are normally reflected in the [38] and aoudad [16]. Juvenile Iberian ibexes also clinical status of mange about 2–3 months afterwards appear to show lower morbidity [12] and progression to [17]. The higher SE and lower SP during the wet period, chronic stages of infection [13], although no differences when mites are more active and lesions are typically more in immune response to sarcoptic mange have been evident, suggest that such wide lesions might be more observed for this age class [22]. In mortality-based easily detected, but also that other skin disorders can studies, the lower proportion of scabietic juveniles has be more easily mistaken as sarcoptic mange at that time been explained by the lower detectability of the smaller of the year. In fact, in late spring, as observed in other juvenile carcasses and the action of scavengers [11, 40]. mountain ungulates [44], Iberian ibexes are molting and The higher proportion of severe mangy adults, how- can show an scabietic aspect increasing the likelihood of ever, could be explained by the behaviour of the adults being wrongly culled for that condition. Along the same during the rutting season, which increases the contact lines, skin disturbances due to other ectoparasite infesta- among them favouring mange transmission. Since the tions can also alter the skin appearance at that time [45, results of the present study show that the sensitivity 46], increasing the probability of misclassification. There- of visual diagnosis of sarcoptic mange in juveniles is fore, during the wet period attention should be paid to lower than in adults, the lower prevalence consistently distinguish mangy ibexes from those suffering from other observed in juveniles could be also related, at least par- skin disorders. Conversely, during the dry period the tially, to the higher rate of false negatives in this age efforts should focus on identifying smaller lesions in oth- group. erwise apparently healthy ibexes. Culling animals affected by sarcoptic mange in order In sexually dimorphic species, males are more sus- to decrease transmission and control the disease is a ceptible to most parasite infestations [47, 48]. Moreo- management measure that must be applied carefully ver, sex-biased parasitism by arthropods rises with and responsibly in order to achieve the objective. Oth- the increase of sexual dimorphism in body mass [48]. erwise, selective culling might be disadvantageous and Although high testosterone and high investment in even counter-productive due to the removal of poten- secondary sexual characters increase mating success, tial resilient animals from the environment [7], dis- they also impair the functioning of the immune sys- rupting the transmission of the genetic resistance to tem [21], specifically under environmental stress [49]. the offspring and increasing sarcoptic mange cases by Thus, males often show higher prevalence, parasite enhancing animal dispersion [7, 22]. Valldeperes et al. Parasites Vectors (2019) 12:405 Page 6 of 7 Conclusions Fellowship (2018FI_B_00978, co-financed by Agència de Gestió dʼAjuts Universitaris i de Recerca and European Social Fund) and ES by the Spanish The SE and SP for the visual determination of mangy Ministerio de Ciencia Innovación y Universidades (MICINN) through a Ramon y Iberian ibexes were found to be influenced by physi- Cajal agreement (RYC-2016-21120). ological (sex and age) and environmental conditions in Availability of data and materials SNNS. If the selective culling of mangy individuals is to The datasets used and/or analysed during the present study are available be an effective and efficient management measure, it is upon request. essential to maximize the SE and SP in order to achieve Ethics approval and consent to participate a high rate of removal of affected individuals from the The ibexes were harvested within the regular Iberian Ibex Management Plan environment without eliminating potentially resistant in the Sierra Nevada Natural Space. Therefore, there was no need for specific individuals. To improve the SE and SP, adaptive criteria ethic approval for this study. must be established and modified according to the period Consent for publication of the year (wet or dry), the sex and the age of the tar- Not applicable. get ibex. Culling should be more conservative during Competing interests the wet period and with females, when visual diagnosis The authors declare that they have no competing interests. SP is low. Females seem to be more able to control sar- coptic mange, maintaining lower mite burdens and being Author details 1 Wildlife Ecology & Health group (WE&H) and Servei d’Ecopatologia de Fauna more sedentary, therefore downplaying their role in the Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat transmission. On the other hand, juveniles are frequently Autònoma de Barcelona (UAB), 08190 Bellaterra, Barcelona, Spain. 2 Espacio asymptomatic carriers and thus the decision of keeping Natural Sierra Nevada, Carretera Antigua de Sierra Nevada, Km 7, Pinos Genil, 18071 Granada, Spain. 3 Departamento de Biología Animal, Biología Vegetal y alive young ibexes showing sarcoptic mange compat- Ecología, Universidad de Jaén, Campus Las Lagunillas, s.n, 23071 Jaén, Spain. ible lesions but potentially resistant to the disease need 4 Agencia de Medio Ambiente y Agua de Andalucía, 41092, Isla de la Car‑ to be discussed. Research to unveil the reason for the tuja, Sevilla, Spain. 5 Dipartimento di Scienze Veterinarie, Universitá di Torino, Grugliasco, Torino, Italy. 6 Departament de Ciència Animal, Escola Tècnica lower lesions presence in juveniles and to define new Superior d’Enginyeria Agraria (ETSEA), Universitat de Lleida (UdL), 25098 Lleida, field methods with higher SE for juveniles should be car- Spain. ried out. Similarly, new methods should be validated to Received: 16 May 2019 Accepted: 9 August 2019 unmask the false negatives during the dry period, before the rutting season when sarcoptic mange spreads due to the increase in contact rate among individuals. References 1. Bornstein S, Mörner T, Samuel WM. Sarcoptes scabiei and sarcoptic mange. Abbreviations In: Samuel WM, Pybus MJ, Kocan AA, editors. Parasitic diseases of wild KOH: potassium hydroxide; SP: specificity; SE: sensitivity; SNNS: Sierra Nevada mammals. 2nd ed. Ames: Iowa Sate University Press; 2001. p. 107–19. Natural Space; GLM: generalized linear model; K: estimated parameters in the 2. Pence DB, Ueckermann E. Sarcoptic mange in wildlife. Rev Sci Tech. model, degrees of freedom; AIC: Akaike’s information criterion; ΔAIC: differ‑ 2002;21:385–98. ence of AIC with respect to the best model; Wi: Akaike’s weight; AICc: Akaike’s 3. Ryser-Degiorgis MP, Ryser A, Bacciarini LN, Angst C, Gottstein B, Janovsky information criterion corrected; OR: odds ratio; TP: true positives; FN: false M, et al. Notoedric and sarcoptic mange in free-ranging lynx from Swit‑ negatives; TN: true negatives; FP: false positives. zerland. J Wildl Dis. 2002;38:228–32. 4. Pence DB, Windberg LA. Impact of a sarcoptic mange epizootic on a Acknowledgements coyote population. J Wildl Manage. 1994;58:624–33. We would like to thank the Consejería de Medio Ambiente de la Junta de 5. Gakuya F, Ombui J, Maingi N, Muchemi G, Ogara W, Soriguer RC, et al. Andalucía and in particular the staff of Sierra Nevada Natural Space (SNNS) Sarcoptic mange and cheetah conservation in Masai Mara (Kenya): for their logistical support. Special thanks are also due to the park wardens epidemiological study in a wildlife/livestock system. Parasitology. and fieldworkers in the SNNS and, in particular, to Apolo Sánchez, José López, 2012;139:1587–95. Isidro Puga, Elías Martínez, Francisco Felipe and Antonio Rodríguez for their 6. Mörner T. Sarcoptic mange in Swedish wildlife. Rev Sci Tech. professional and personal involvement in the study. 1992;11:1115–21. 7. Lindstrom E, Mörner T. The spreading of sarcoptic mange among Swed‑ Authors’ contributions ish red foxes (Vulpes vulpes L) in relation to fox population dynamics. MV and ES designed the work, analysed and interpreted the data, and drafted Ecology. 1985;40:211–6. the work. GM, JEG and ES substantially contributed to the conception of 8. Gray DF. Sarcoptic mange affecting wild fauna in New South Wales. Aust the project. JEG and PF acquired the animal samples and participated in Vet J. 1937;13:154–5. interpreting the data. JMP and IC performed the laboratory analysis. ARB and 9. Martin RW, Handasyde KA, Skerratt LF. Current distribution of sarcoptic GM substantively revised the manuscript. JRLO participated in interpreting the mange in wombats. Aust Vet J. 1998;76:411–4. data. All authors read and approved the final manuscript. 10. Brown AS, Seawwright AA, Wilkinson GT. The use of amitraz in the control of an outbreak of sarcoptic mange in a colony of koalas. Aust Vet J. Funding 1982;58:8–10. This project was funded by the Consejería de Medio Ambiente de la Junta 11. Fernández-Morán J, Gómez S, Ballesteros F, Quirós P, Benito JL, Feliu C, de Andalucía (project 173/2009/M/00; 03/15/M/00; 861_11_M_00 and et al. Epizootiology of sarcoptic mange in a population of cantabrian 2016/00014/M), and by the Spanish Ministerio de Economía y Competitividad chamois (Rupicapra pyrenaica parva) in northwestern Spain. Vet Parasitol. (projects CGL2012-40043-C02-01, CGL2012-40043-C02-02 and CGL2016- 1997;73:163–71. 80543-P). The authors’ research activities are partially supported by the Plan Andaluz de Investigación (RNM-118 group). MV is supported by a FI-GENCAT Valldeperes et al. Parasites Vectors (2019) 12:405 Page 7 of 7 12. Fandos P. La cabra montés (Capra pyrenaica) en el Parque Natural de las 32. Carvalho J, Granados JE, López-Olvera JR, Cano-Manuel FJ, Pérez JM, Sierras de Cazorla, Segura y las Villas. Madrid: Colección Técnica, ICONA; Fandos P, et al. Sarcoptic mange breaks up bottom-up regulation of body 1991. condition in a large herbivore population. Parasit Vectors. 2015;8:572. 13. León-Vizcaíno L, Ruíz de Ybáñez MR, Cubero MJ, Ortíz JM, Espinosa J, 33. Pérez JM. Distribución, genética y estatus sanitario de las poblaciones Pérez L, et al. Sarcoptic mange in Spanish ibex from Spain. J Wildl Dis. andaluzas de cabra montés. Jaén: Universidad de Jaén, Consejería de 1999;35:647–59. Medio Ambiente; 2001. 14. Alasaad S, Granados JE, Fandos P, Cano-Manuel FJ, Soriguer RC, Pérez JM. 34. Serrano E, Granados JE, Sarasa M, González FJ, Fandos P, Soriguer RC, et al. The use of radio-collars for monitoring wildlife diseases: a case study from The effects of winter severity and population density on body stores in Iberian ibex affected by Sarcoptes scabiei in Sierra Nevada, Spain. Parasit the Iberian wild goat (Capra pyrenaica) in a highly seasonal mountain Vectors. 2013;6:242. environment. Eur J Wildl Res. 2011;57:45–55. 15. Espinosa J, Ráez-Bravo A, López-Olvera JR, Pérez JM, Lavín S, Tvarijo‑ 35. Ráez-Bravo A, Granados JE, Cerón JJ, Cano-Manuel FJ, Fandos P, Pérez naviciute A, et al. Histopathology, microbiology and the inflammatory JM, et al. Acute phase proteins increase with sarcoptic mange status process associated with Sarcoptes scabiei infection in the Iberian ibex, and severity in Iberian ibex (Capra pyrenaica Schinz, 1838). Parasitol Res. Capra pyrenaica. Parasit Vectors. 2017;10:596. 2015;114:4005–10. 16. González-Candela M, Léon-Vizcaíno L, Cubero-Pablo MJ. Population 36. Burnham KP, Anderson DR. Model selection and multimodel inference. A effects of sarcoptic mange in Barbary sheep (Ammotragus Lervia) from practical information-theoretic approach. 2nd ed. New York: Springer- Sierra Espuña Regional Park. Spain. J Wildl Dis. 2004;40:456–65. Verlag; 2002. 17. Pérez JM, Ruiz-Martínez I, Granados JE, Soriguer RC, Fandos P. The dynam‑ 37. Altman DG, Bland JM. Diagnostic tests 1: sensitivity and specificity. Br ics of sarcoptic mange in the ibex population of Sierra Nevada in Spain Med J. 1994;308:1552–3. - Influence of climatic factors. J Wildl Res. 1997;2:86–9. 38. Walter B, Heukelbach J, Fengler G, Worth C, Hengge U, Feldmeier H. 18. Arlian LG, Runyan RA, Achar S, Estes SA. Survival and infestivity of Comparison of dermoscopy, skin scraping, and the adhesive tape test Sarcoptes scabiei var. canis and var. hominis. J Am Acad Dermatol. for the diagnosis of scabies in a resource-poor setting. Arch Dermatol. 1984;11:210–5. 2011;147:468–73. 19. Arlian LG, Runyan RA, Vyszenski-Moher DL. Water balance and nutrient 39. Walton SF, Currie BJ. Problems in diagnosing scabies, a global disease in procurement of Sarcoptes scabiei var. canis (Acari: Sarcoptidae). J Med human and animal populations. Clin Microbiol Rev. 2007;20:268–79. Entomol. 1988;25:64–8. 40. Oleaga Á, Casais R, González-Quirós P, Prieto M, Gortázar C. Sarcoptic 20. López-Olvera JR, Serrano E, Armenteros A, Pérez JM, Fandos P, Carvalho J, mange in red deer from Spain: improved surveillance or disease emer‑ et al. Sex-biased severity of sarcoptic mange at the same biological cost gence? Vet Parasitol. 2008;154:103–13. in a sexually dimorphic ungulate. Parasit Vectors. 2015;8:583. 41. Arlian LG, Pole MJ, Vyszensky-Moher DL. Survival of adults and develop‑ 21. Folstad I, Karter AJ. Parasites, bright males, and the immunocompetence mental stages of Sarcoptes scabiei var. canis when off the host. Exp Appl handicap. Am Nat. 1992;139:603–22. Acarol. 1989;6:181–7. 22. Sarasa M, Rambozzi L, Rossi L, Meneguz PG, Serrano E, Granados JE, et al. 42. Ibrahim KEE, Abu-Samra MT. Experimental transmission of a goat strain of Sarcoptes scabiei: specific immune response to sarcoptic mange in the Sarcoptes scabiei to desert sheep and its treatment with ivermectin. Vet Iberian ibex Capra pyrenaica depends on previous exposure and sex. Exp Parasitol. 1987;26:157–64. Parasitol. 2010;124:265–71. 43. Oleaga Á, Casais R, Balseiro A, Espí A, Llaneza L, Hartasánchez A, et al. New 23. Granados JE, Montes J, Pérez JM, Serrano E, Fandos P, Soriguer RC. Plan techniques for an old disease: sarcoptic mange in the Iberian wolf. Vet de gestión de la cabra montés (Capra pyrenaica) en el Espacio Natural Parasitol. 2011;181:255–66. Protegido de Sierra Nevada. 2001. 44. Déry F, Hamle S, Côté S. Gretting ready for the winter: timing and deter‑ 24. Rossi L, Fraquelli C, Vesco U, Permunian R, Sommavilla GM, Carmignola G, minants of molt in alpine ungulate. Ecol Evol. 2019;9:2920–32. et al. Descriptive epidemiology of a scabies epidemic in chamois in the 45. Varela-Castro L, Zuddas C, Ortega N, Serrano E, Salinas J, Castellà J, et al. Dolomite Alps, Italy. Eur J Wildl Res. 2007;53:131–41. On the possible role of ticks in the eco-epidemiology of Coxiella burnetii 25. Pérez JM, Granados JE, Sarasa M, Serrano E. Usefulness of estimated in a Mediterranean ecosystem. Tick Tick Borne Dis. 2018;9:687–94. surface area of damaged skin as a proxy of mite load in the monitoring of 46. Carvalho J, Serrano E, Pettorelli N, Granados JE, Habela MA, Olmeda S, sarcoptic mange in free-ranging populations of Iberian wild goat, Capra et al. Sarcoptes scabiei infestation does not alter the stability of ectopara‑ pyrenaica. Vet Parasitol. 2011;176:258–64. site communities. Parasit Vectors. 2016;9:379. 26. Pérez JM, Castro I, Granados JE, Cano-Manuel FJ, Fandos P, Espinosa J, 47. Klein SL. Hormonal and immunological mechanisms mediating sex differ‑ et al. Does Sarcoptes scabiei synchronize its breeding cycle with that of ences in parasite infection. Parasite Immunol. 2004;26:247–64. the Iberian Ibex, Capra pyrenaica? Int J Acarol. 2016;43:199–203. 48. Moore SL, Wilson K. Parasites as a viability cost of sexual selection in 27. Pérez JM, Granados J, Gomez F, Pérez C, Ruiz-Martínez I. Las parasitosis natural populations of mammal. Science. 2002;297:2015–8. de la cabra montes de Sierra Nevada (Granada). Conf Int Sierra Nevada 49. Toïgo C, Gaillard JM. Causes of sex biased adult survival in ungulates: Conserv y Desarro Sosten. 1996;53:1689–99. sexual size dimorphism, mating tactic or environment harshness? Oikos. 28. Pérez JM, Meneguz PG, Dematteis A, Rossi L, Serrano E. Parasites 2003;101:376–684. and conservation biology: The “ibex-ecosystem”. Biodivers Conserv. 50. Decristophoris PMA, Von Hardenberg A, McElligott AG. Testosterone is 2006;15:2033–47. positively related to the output of nematode eggs in male Alpine ibex 29. Smith MC, Sherman DM. Goat medicine. 2nd ed. Ames: Wiley Blackwell; (Capra ibex) faeces. Evol Ecol Res. 2007;9:1277–92. 2009. 30. Heukelbach J, Feldmeier H. Scabies. Lancet. 2006;367:1767–74. 31. Arenas AJ, Gómez F, Salas R, Carrasco P, Borge C, Maldonado A, et al. An Publisher’s Note evaluation of the application of infrared thermal imaging to the tele- Springer Nature remains neutral with regard to jurisdictional claims in pub‑ diagnosis of sarcoptic mange in the Spanish ibex (Capra pyrenaica). Vet lished maps and institutional affiliations. Parasitol. 2002;109:111–7.