Human-mediated global environmental change and movement of pathogens and domestic hosts have driven the emergence of disease in wildlife across the globe (Daszak et al., 2000; Tompkins et al., 2015). Evidence supporting that emerging diseases can lead to population declines and extinctions of wild species, and to subsequent changes at the community and ecosystem levels has accumulated in the last decades (Harvell et al., 2019; O’Hanlon et al., 2018; Schultz et al., 2016). Indeed, emerging disease events have become a concern for the conservation of marine and terrestrial biodiversity globally (Daszak et al., 2000; Harvell et al., 2019, 1999; O’Hanlon et al., 2018; Schultz et al., 2016; Tompkins et al., 2015).

Although disease emergence in wild species of South America is underrepresented in the scientific literature (Tompkins et al., 2015), this continent is not exempt from the global trend. For example, a cetacean morbillivirus has recently been associated with mass mortality in Guiana dolphins (Sotalia guianensis) in Brazil (Groch et al., 2018) and Corynebacterium pseudotuberculosis is currently affecting the endangered huemul deer (Hippocamelus bisulcus) in Chile (Morales et al., 2017).

Further, the globally emerging sarcoptic mange (Astorga et al., 2018), caused by the burrowing mite Sarcoptes scabiei, has been anecdotally reported in wild mammals of Chile (Alvarado et al., 2004; Verdugo et al., 2016), including within protected areas (PAs; Cunazza and Diaz, 2014; López Jiménez, 2018). Worryingly, this skin disease can have catastrophic effects on wild populations as seen in other places around the world (Martin et al., 2017). It is therefore of concern that Chilean stakeholders increasingly perceive alopecic native mammals, a classic presentation of S. scabiei infestation, as more common and more broadly spread across the country. However, with no formal national system in place to monitor wildlife health in Chile and no centralized repository of information on disease, tracking sarcoptic mange (or other diseases) over relevant temporal and spatial scales becomes a very difficult task. Moreover, efforts to generate such data country-wide have not been made. These deficiencies and patchy data inherently limit the capability to confirm perceptions and effectively inform policy. If sarcoptic mange is a growing problem in Chile, then public and private action to prevent biodiversity impacts is warranted.

Here, we aimed to describe the trend of sarcoptic mange in Chilean wildlife over a 15-year period (2004–2018) within PAs as well as the location of cases in non-protected landscapes at the country level in recent times (2012–2019). To fulfill these objectives, we relied on abnormal hair loss (herein “abnormal alopecia”), the highly visible main characteristic of sarcoptic mange (Bornstein et al., 2001; Niedringhaus et al., 2019; Pence and Ueckermann, 2002), to establish a definition of a suspect case. With this case definition, we tracked potentially S. scabiei infested mammals over time in PAs of Chile. In addition, we combined multiple independent sources of information to also identify abnormally alopecic wild mammals outside PAs and summarize their locations in this country. Finally, we assessed the validity of abnormal alopecia to track sarcoptic mange cases by testing individuals with this condition admitted to rehabilitation centers. We discuss the implications of our findings for mammal conservation and the need for a National Wildlife Health Surveillance Program in Chile.

Procedures involving human participants were limited to anonymous surveys conducted in accordance with the ethical standards of the University of California, Davis, Institutional Review Board (Protocol # 1320102-1).

Herein we collated data from several sources to describe, to the extent that current information allows, the presence of abnormally alopecic wild mammals in Chilean PAs over a 15-year period (2004–2018) and to summarize the location of affected animals beyond PAs. We observed a potential increment in the number of PAs in Chile in which wild mammals with abnormal alopecia have been sighted during the study period and a broad presence of cases across most of the Chilean territory in recent times. Data also support an increasing number of species observed with abnormal alopecia and a potential increment of cases within specific taxa. This suggested trend follows the current global emergence of sarcoptic mange in wildlife (Astorga et al., 2018; Niedringhaus et al., 2019).

Lycalopex foxes were the group most commonly reported with abnormal alopecia and were present across all data sources and time periods. The information from the Chilean National Park Service (CONAF) park rangers suggests that the geographical distribution of PAs presenting abnormally alopecic foxes has expanded over time. Between 2008–2018, these animals were observed in PAs located beyond Chile's Central Zone where they were thought to be restricted (Cunazza and Diaz, 2014). Moreover, the incorporation of other sources of information, including citizen reports, allowed us to compile dozens of abnormally alopecic mammal reports from many parts of the country. Further, we confirmed S. scabiei in alopecic L. culpaeus from Central Chile, consistent with previous reports in L. griseus from the southern part of the country and in other non-Chilean Lycalopex species (Deem et al., 2002; Verdugo et al., 2016). Through microscopic and molecular confirmatory testing, we showed that abnormal alopecia can be a good indicator of sarcoptic mange in L. culpaeus, similar to previous findings in red fox (Vulpes vulpes) with “mange-like lesions” (Nimmervoll et al., 2013) and that this disease is common in abnormally alopecic Lycalopex individuals.

South American camelids were the second most common group reported with abnormal alopecia. S. scabiei-infested South American camelids have been previously reported in PAs of the North and North-Central Zones (Bonacic et al., 2014; López Jiménez, 2018) in agreement with our survey results. Park ranger reports support that abnormally alopecic vicuna and guanaco were found in a larger number of PAs and in a larger number of individuals during 2014–2018 compared to 2004–2008. However, whether this reflects an increasing trend is unclear. According to two published reports older than 2004 (and, therefore, not included in the internet data subset), sarcoptic mange in guanacos has been observed in the North-Central Zone since 2002 (Zárate and Valencia, 2010) and before 2004 in the Austral Zone (Alvarado et al., 2004). Of note, pre-2004 sarcoptic mange reports in the Austral Zone refer to cases in central and southern Tierra del Fuego Island (Alvarado et al., 2004). No PA was established in central Tierra del Fuego until 2013; therefore, earlier South American camelid cases in the Austral Zone may have been under-reported in earlier years. For comparison, a distribution of South American camelid cases including all data sources and published pre-2004 data is shown in S8. Nevertheless, park ranger data presented here suggest a potential southward spread of abnormally alopecic South American camelids in the North Zone and sarcoptic mange in this taxon has been increasingly described in recent times in Peru, Bolivia, and Argentina (Castillo, 2018).

We also found cases affecting other species, such as a Galictus cuja diagnosed as a sarcoptic mange case through mite identification in a wildlife rehabilitation center. To our knowledge this is the first report of a lesser grison infested with S. scabiei, although sarcoptic mange has been previously reported in other mustelids (Mörner, 1992; Phillips et al., 1987).

Our results tend to support that abnormally alopecic wild mammals are observed more frequently, that these cases belong to a larger number of species over time, and that S. scabiei is a parsimonious explanation for several of the cases observed. Although the search for alopecic mammals through different detection methods, such as questionnaires, carcass collection, and camera traps have been useful to study sarcoptic mange in wildlife (Carricondo-Sanchez et al., 2017; Chen et al., 2012; Pisano et al., 2019; Soulsbury et al., 2007) these data sources are not without limitations. In our case, it is possible that self-selection bias occurred in the rangers that responded to the survey and that those rangers in PAs with alopecic mammals were more likely to participate. Nevertheless, if this were true, the proportion of affected PAs would be biased upwards, but the suggested temporal and spatial trends would remain. We also relied on historical records to avoid recall bias of abnormally alopecic mammal sightings by park rangers; however, the “surveillance” efforts and storage of this information could be better now than 20 years ago. We were informed by CONAF that differences in surveillance efforts and data recording were highly unlikely for the last two 5-year periods (2009–2013 and 2014–2018) when a potential increment in positive PAs was observed.

We advertised the web-platform to report alopecic wild mammals by several means and its value is justified in the recovery of alopecic cases that would otherwise not have been recorded. However, reporting may have been constrained by the visibility of alopecic animals or the degree of public awareness. This first experience suggests that web-based citizen reporting seems to be more useful for wild species present in easily accessed human-modified landscapes such as Lycalopex foxes versus South American camelids (or other taxa). This could explain the reports mostly belonging to the former group but none of the latter.

Further, we assessed the ability of abnormal alopecia to establish a suspect sarcoptic mange case by testing abnormally alopecic wild mammals for S. scabiei. We only had access to abnormally alopecic foxes, specifically, L. culpaeus that were admitted to wildlife rehabilitation centers; therefore, we could only assess the validity of this clinical sign to track sarcoptic mange in this species. This is relevant because the use of alopecia as a proxy to define a sarcoptic mange case in wildlife can be misleading (Valldeperes et al., 2019). We did not test free-ranging abnormal alopecic individuals of this species either. It is possible that S. scabiei-infested foxes are more likely to be captured and admitted into rehabilitation centers compared to other conditions leading to abnormal alopecia. If so, then our results may not apply to the general “abnormally alopecic fox” population. Nonetheless, although the number of foxes used to assess the validity of alopecia is not large, our results clearly show the need for a high “true prevalence” of S. scabiei to detect 9 out of 9 foxes infested. Park rangers (the only source of cases in our data for South American camelids) are most likely capable of distinguishing normal molting from abnormal alopecia. The external appearance of confirmed South American camelid sarcoptic mange cases from a recent outbreak in Argentina matches the observations reported by CONAF, providing more support for S. scabiei infestation in these animals (S5; Ferreyra et al., 2020).

Finally, we cannot claim that all abnormally alopecic mammals were infested with S. scabiei. Indeed, the reported huemul in the Austral Zone is probably an individual affected by C. pseudotuberculosis (Morales et al., 2017).

The data limitations mentioned above result from the fact that Chile, as is the case in all South American nations, does not have a National Wildlife Health Surveillance Program (Pinto et al., 2008). The lack of such a program hinders the collection of representative data on disease and etiologies in native mammal populations; our understanding of the epidemic or endemic nature of diseases, seasonal trends, and eventual populations impacts; and, most importantly, the response and management of health-related and potentially conservation-threatening issues. These threats include pathogens that have recently been detected in Chilean wildlife involving endemic endangered species. For example, caseous lymphadenopathy, echinococcosis, and a parapoxvirus-associated foot disease in the endangered huemul deer (Hernández et al., 2019; Morales et al., 2017; Vila et al., 2019); and Chytridiomycosis in the endangered Darwin's frogs (Rhinoderma spp.; Soto-Azat et al., 2013). Moreover, several other pathogens have been sporadically detected in Chilean wildlife within PAs (Cunazza and Diaz, 2014; López Jiménez, 2018) whose status, trend, and relevance remain unknown.

Considering that several reports we collated correspond to confirmed and probable sarcoptic mange, its etiology, the mite S. scabiei, is a multi-host pathogen (Bornstein et al., 2001; Pence and Ueckermann, 2002), whose transmission may behave in a frequency-dependent manner (Devenish-Nelson et al., 2014), and infested hosts present a long infectious period. These traits have been associated with easier disease spread and disease-mediated extinction (Cross et al., 2005; De Castro and Bolker, 2005). Indeed, this mite is continuously reported in new species (Gonzalez-Astudillo et al., 2018), it can devastate populations of wild species (Martin et al., 2017) and it is currently considered a global emerging threat for wildlife conservation (Astorga et al., 2018). Further, S. scabiei may interact with other conservation threats or it could generate fragmented populations susceptible to stochastic events.

Lycalopex is a Neotropic endemic genus that belongs to a taxonomic family with worldwide records of S. scabiei-driven extirpations or near extirpations of common and endangered species (Henriksen et al., 1993; León-Vizcaíno et al., 1999; Lindström, 1991; Pence and Ueckermann, 2002; Soulsbury et al., 2007; Uraguchi et al., 2014). In Chile, L. culpaeus and L. griseus fulfill the description of the first group, while the endemic and endangered Darwin's fox (Lycalopex fulvipes) and the endemic and vulnerable Fuegian culpeo (L. c. lycoides), certainly belong to the second category (Ministerio del Medio Ambiente, 2011; Silva-Rodríguez et al., 2016). These two endangered foxes would be highly at risk from any lethal disease outbreak. Of concern, mite-associated morbidity (Otodectes cynotis) has recently been reported in these two fox species (Briceño et al., 2020).

In the case of South American camelids, sarcoptic mange is considered a main threat for this group in Chile (Bonacic et al., 2014; Vargas et al., 2016; Zárate and Valencia, 2010). Moreover, an ongoing sarcoptic mange outbreak has nearly caused the local extinction of vicuna and guanaco in San Guillermo National Park in Argentina (Ferreyra et al., 2020), revealing the potential consequences of S. scabiei in these species. In addition to this infectious threat, the guanaco could become extinct in three of the five countries where it is currently present, projections for the conservation of South American camelids in the Chilean North Central Zone are not optimistic, and Chilean coastal populations have rapidly declined (Bonacic et al., 2014; González and Acebes, 2016; Vargas et al., 2016; Zárate and Valencia, 2010).

Despite being previously recognized in Chile and representing a potential threat for Chilean wildlife, data on S. scabiei in Lycalopex sp. and South American camelids are remarkably precarious and this is the first attempt to describe the status of this disease nationwide. Our findings, the potential consequences of this disease, and the absence of robust S. scabiei data further reinforce the need for a National Wildlife Health Surveillance Program.

Furthermore, it is anticipated that disease emergence will occur more often in wild species globally as a result of the human-mediated movement of pathogens, parasites, and domestic hosts, and concurrent changes in the environment including habitat destruction and the climate emergency (Daszak et al., 2000). These drivers are occurring in Chile. For example, 30% of native temperate forest was lost during the last three decades (Zamorano-Elgueta et al., 2015) and 69% of mammals were already threatened by habitat destruction in Central Chile twenty years ago (Simonetti, 1999). Consequently, new disease events in Chilean native species should be expected in the upcoming years.

Based on our previous arguments we encourage the urgent convening of an intersectoral working group of private stakeholders, academia, and public agencies with the goal of establishing a National Wildlife Health Surveillance Program in Chile. Existing uncertainties with respect to sarcoptic mange levels and trends and the potential threat posed by this disease justify its prompt launch and provides an opportunity for capacity-building and troubleshooting during start-up. Such a program should fulfill the attributes, purposes, and roles recently proposed by experts (Stephen et al., 2018) and should engage domestic animal and human health sectors as well as conservation and biodiversity constituents through a One Health approach. Government-led wildlife health programs have had remarkable positive influences on the conservation of species as well as on public health (Brand, 2013; Kuiken et al., 2005; Reif, 2011). Although there is an incipient valuable pilot effort lead by the Chilean National Park Service to monitor diseases, it only covers some PAs and several components need to be expanded or substantially improved to generate a functional country-level Wildlife Health Program (Aizman et al., 2016; Cunazza et al., 2015).

Nations failing to properly prepare to confront pathogen threats in wildlife may expect to experience catastrophic outcomes for conservation as described worldwide (De Castro and Bolker, 2005). Moreover, governments should strive toward fulfilling their responsibilities to meet societal needs and obligations in their role as keepers of a public good.

Abnormally alopecic wild mammals seem to have become more common in Chile and observed in an increasing area of the country over a 15-year period, between 2004–2018. Sarcoptic mange is a likely cause for this disease at least in the genus most commonly reported with alopecia, Lycalopex, and in South American camelids. Based on these findings and the catastrophic consequences that sarcoptic mange has had worldwide, we encourage the establishment of a National Wildlife Health Surveillance Program in Chile. Such a program is also justified by the recent detection of pathogens causing morbidity and mortality in native species, including the iconic Huemul deer, classified as endangered in the IUCN's Red List.

The authors declare no conflict of interest.