Fatal Sarcoptes scabiei and Demodex sp. co-infestation in wolves (Canis lupus) at the Białowieża National Park, Poland – is it a consequence of climate change?

The grey wolf (Canis lupus) is the largest carnivorous mammal of the canid family, the range of which is concentrated in the northern hemisphere, and the favoured habitats of which are the forests, plains, wetlands and mountains of North America and Eurasia. At the beginning of the last century, this species was common in Poland. In 1927, its high abundance caused it to be declared a game animal, which started the process of its culling, culminating in a resolution of the Presidium of the Government of 29 January 1955 “on the extermination of wolves”. These measures resulted in the wolf's numbers falling to below 60 individuals in 1972 (52). In 1998, the wolf was placed on the list of most-protected species, taking into account their role as predators in maintaining the ecological balance. Currently, the wolf population in Poland is estimated at 2–2.5 thousand individuals (15), although the Polish Hunting Association (PZŁ) suggests that this number is a gross underestimation. Nevertheless, the Polish wolf population is among the largest in Europe (19). Three genetic lines of the species are observed in the country: the Central European Lowland, Baltic and Carpathian populations (30). Wolves are present all over the country; however, the distribution is patchy and its density varies significantly between the largest forest complexes. In addition, wolves have been increasingly observed migrating to new areas and forming new packs (64). The highest density, one of over nine wolves per 100 km², was noted in the Bieszczady mountains, while the lowest was in Żywiec and the Silesian Beskids and was approximately one individual per 100 km². The density of the wolf population in the studied area of the Białowieża Forest (BF) fluctuates around three wolves per 100 km², and the population comprises at least four main packs (70). Since anthropopressure and poaching of wolves on the Polish side of the BF is not as frequent as on the Belarusian side (34), the wolves’ habitat there had not been disturbed as heavily as habitats had in other areas of Poland until the recent migration crisis on the Belarusian border because of the Russian invasion of Ukraine. Despite the high protection of the species in the country, the situation of the wolf is complicated for several reasons. While it may not threaten the conservation of the species, poaching or illegal shooting remains a problem. The increasing number of wolves and the human pressure on the environment force them to migrate, leading to increasingly frequent traffic accidents (63). Post-mortem examinations of wolf carcasses reveal lesions indicative of multiple injuries: not only the fatal ones, but others associated with hunting large animals, i.e. red deer (Cervus elaphus), which is the main species wolf packs prey in Poland (36), or European bison (Bison bonasus) which are occasional wolf prey in the BF (35). The epidemiological risks for wolf health and conservation in Poland have not yet been investigated. So far, studies on wolves have focused on the characterisation of their endoparasites, and have not explored the perspective that the wolf is a species with its conservation endangered by these parasites, but rather have regarded the wolf as a potential reservoir (5, 12, 13, 69) or indicatory species (39) with a role in the transmission of pathogens threatening humans or other carnivores, including domestic dogs (28, 62).

The current lifestyle of wolves is the result of adaptation, resilience and innate behaviour in an almost completely urbanised environment. This increasing interpenetration of the synanthropic and sylvatic environments raises the potential for pathogen transmission, many of which are zoonotic. An additional driver for the emergence of diseases that threaten protected species in particular is climate change, which may directly affect the ecology of microorganisms, their vectors such as arthropods and their reservoirs such as rodents and bats (16). An indirect effect of climate change is heat stress in animals, which affects their immune and endocrine functions, reproduction and metabolism and increases their susceptibility to infection/invasion by pathogens which are often opportunistic. Furthermore, climate change may reduce access to food and water, force migration and increase local animal density, and therefore increase interspecies and intraspecies encounters. Sudden climate events are particularly dangerous and do not allow for the adaptation which takes place when the changes gradually progress (3). Sarcoptic mange is considered a neglected disease, whereas Demodex is a frequent skin commensal; however, their re-emergence as pathogens may be a consequence of the recent changes in the ecosystem. The outcomes of skin parasite infestations may serve as an indicator of the health of the environment and inform the investigations of adherents to the common concept of One Health. The European wildlife species for which scabies is most frequently fatal are usually smaller predators like red foxes (Vulpes vulpes), raccoon dogs (Nyctereutes procyonoides) and badgers (Meles meles). In contrast, grey wolves which have scabies usually display alopecic, pruritic skin lesions with crusting which are limited to some areas on the head, hind limbs, flanks and tail and are rarely fatal.

This is the first clinical description of Sarcoptes mange in wolves in Poland and the first identification of Demodex mites in the species. Climate conditions, the geopolitical situation and wolf population dynamics are considered as possible factors associated with the progression of these infestations, which are usually nonfatal in wolves, and are discussed at the microscale of the last remaining primeval forest in Europe.

Scabies is considered a neglected tropical disease, and its re-emergence in animals and humans is becoming a challenge in many parts of the world. The exacerbation of parasite invasions can be seen as a symptom of environmental changes that affect general health and susceptibility to endemic and conditionally pathogenic commensals. For example, an association between human scabies caused by Sarcoptes scabiei varietas hominis and cases of COVID-19 was recently observed in developing countries (22). Initially, the treatment with ivermectin of SARS-CoV-2 infections led to a decline in mange cases; however, the prolonged albeit unintentional effect of this antiparasitic therapy may have been the emergence of drug resistance in mites, thus increasing the number of difficult-to-treat skin infestations in humans (27). It has also been observed that the recent increase in cases of mange in humans in Europe is connected to geopolitical changes including massive intercontinental movements and migration (20, 42). However, the zoonotic potential of the Sarcoptes mites hosted by animals is low, as it is associated only with occasional cases of pseudoscabies. Most of cases of human scabies transmitted from animals (mostly dogs) were transient and self-limiting, as the parasite has less ability to reproduce and persist in human skin (47). Scabies as a reverse zoonosis (zooanthroponosis) was suspected based on historical data; however, transmission from human to animal was never demonstrated (2, 6).

Scabies and demodicosis are caused by parasitic mites classified as the Acari subclass within the Arthropoda phylum and Arachnida class. They belong to two distinct orders. Mites of the Demodex genus represent the Demodicidae family and Trombidiformes order, and include host species–specific parasites, putatively specific to their individual hosts. These mites are genetically highly diverse. Cross-infections are rare; therefore, animal demodicosis does not pose a risk to humans (17, 21, 60). Scabies mites, in contrast, belong to one main species –Sarcoptes scabiei – in the Sarcoptes genus, Sarcoptidae family and Sarcoptiformes order, and have many host-specific variants. In numerous animal species within the Canidae family, S. scabiei varietas canis is most commonly found. Genetic studies of scabies isolated from various host species (including humans) have confirmed only minor variations in the genome (8, 46); therefore, epidemiological investigations based on phylogenetic relationship rarely allow the determination of the direction of transmission (6). An additional factor besides genome similarity facilitating interspecies infestation is immunosuppression, which is supported by numerous observations and experimental studies (10, 54). In general, mite isolates have been classified into three main scabies groups of herbivore-hosted, carnivore-hosted and omnivore-hosted on the basis of their genetic homology (2). The exposure to prey-to-predator Sarcoptes mite infection has been studied especially for wolves, which prey on large herbivores (54). However, the possibility of cross-infection of other canids such as the rabbit-dog-rabbit system was also demonstrated (10). This supports the observations of possible interspecies transmission of mites between different carnivores and their prey (24, 25, 41). According to this theory, small mammals may therefore be responsible for the mass occurrence of scabies in foxes or badgers, for which rodents and other small mammals are the primary food source. European wolves less frequently prey on small rodents; therefore, they are less likely to be affected by alimentary infestation. However, in the absence of cervids, wolves may prey on alternative species including beavers (51), making a choice which may also be related to weather conditions (45, 48). Therefore, oral contact may be an underestimated route of scabies infestation in carnivores, especially when the primary prey are rodents. The hypothesis could not be confirmed in our case, however, as we did not observe cases of mange in herbivores or other mammal species. Such observations would have been merely incidental, however, because the camera trapping locations were designed to perform a survey of wolves.

Mange in wildlife reflects emerging worldwide challenges and pressure on nature (47). Sarcoptes scabiei and Demodex sp. are quite common parasites of the skin, and infestations with them are mostly-subclinical and very rarely life-threatening. The infestations may become severe when the host is immunosuppressed because of concurrent factors (56). The widespread use of macrocyclic lactones and acaricides based on active isoxazolinergic substances (fluralaner, sarolaner and afoxolaner) in pets means that both scabies and demodicosis are only marginal problems in domestic animals. Also in humans, clinical mite infestations are extremely rare in highly developed countries because hygiene measures are adequate to prevent them. The situation does not pertain to free-living animals, where these infestations are not countered by prophylaxis or treated. Epidemic mange in wildlife usually heralds an imbalance in nature that negatively influences the affected species. Concern over the disturbance of this balance falls within the concept of One Health, where nature, the environment and humans are one. The imbalance in the ecology of prey animals, access to food, shrinkage of the habitat, overcrowding and competition with other carnivores and humans (hunters) may trigger health and conservation-threatening processes for wolves, as apex predators. On the other hand, the role of predators and hunters may have a positive effect by removing infected animals, contributing to the elimination of carriers or reservoirs of pathogens from the environment. Scabies in Polish wildlife was mostly observed in foxes and badgers, which fared worse and suffered higher mortality when infested (41). The problem became apparent after the eradication of rabies in the main reservoir – foxes – at the beginning of the 21^st century. From then, the fox population has grown significantly. In scientific circles, it has been debated whether stopping one plague has unleashed another on foxes (58). The similarities in the mechanisms of occurrence of this type of ecosystem disturbance may have led to the mass occurrence of scabies. Therefore, those mechanisms were considered when studying the scabies epidemic in wolves. Mange in wolves has been observed to be limited to certain parts of their skin (41). The mortality due to mite skin infestation in wolves reported previously was also rather low (23, 41); however, mange epidemics such as the one described here have previously been noted in American grey wolves (18, 38). Mange is a contact disease, in which the survival of the aetiological agent depends on environmental conditions (11, 50). However, since the infestations usually have minor health consequences, the exposure risk will increase with animal density and alterations in animal ecology, health status and behaviour, as it also will because of the anthropogenic factors disturbing the habitat (56). We have concluded that changes in temperature and environmental humidity may allow the pathogen to persist longer in the environment, significantly worsening the threat.

Climate change has been discussed as a driver for scabies in humans (47) and wildlife (31, 66). Optimal humidity and temperature promote efficient reproduction and survival of mites in the environment (66). An indirect influence of climate change is on host health and susceptibility to adverse factors, where it induces heat stress and weakens the resilience of mammals (48). An increasing percentage coverage of water habitats by camera traps was associated with higher probabilities of apparent scabies in foxes (11). Białowieża Forest is characterised by a high percentage of wetlands, which together with milder winter temperatures favouring mite survival may have intensified the exposure of its wolves to mites and fostered mite transmission between them. Any animal infected with Sarcoptes or Demodex sp. is a potential reservoir of infestation for other hosts. In both infestations, direct contact is the most important route of infection. Therefore, these infestations spread particularly easily in animals living in groups such as packs (14) and are density dependent (4, 31). However, the several-day survival time of these pathogens outside the organism also allows indirect transmission. Animals using burrows abandoned by previously infected individuals even of other species (for example foxes or badgers) are at risk of infection. High humidity and lower temperatures, especially of a few degrees Celsius above zero, are factors that foster the survival of mites outside the host (50). Temperatures around 0°C are not lethal for mites, and only temperatures below -10°C are a limiting factor for their survival, killing them in just a few hours (8). Interestingly, Sarcoptes scabiei have been observed to survive outside of the skin inside the fox den longer during the winter (at a mean 12°C) than the summer (mean 29°C) (43). The humidity inside the den did not change throughout the year sufficiently to affect mite survival.

The disease severity and clinical course of both infestations are strictly dependent on the non-specific and specific immune response. This is particularly evident in the course of demodicosis. This invasion is assumed to occur in a significant proportion of the host population in an asymptomatic form. In contrast, its clinical form is closely associated with periodic immune decline or immunomodulatory disorders. For this reason, a Demodex species is considered a facultative parasite. These mites reside in hair follicles and sebaceous glands. Their abundance determines the asymptomatic or symptomatic nature of the invasion and is controlled by the reactivity of the immune system. Parasite overabundance leads to inflammatory reactions within the hair follicles, hair loss and infection with pathogenic bacterial flora. In the case of burrowing mites such as Sarcoptes sp., the presence of the parasites is frequently associated with skin lesions; therefore, they are considered obligate parasites. The infestation usually spreads from the muzzle area and area peripheral to the eye to cover the entire skin surface in the critical stage (32, 60). During the course of an infestation, numerous immune reactions occur in the host–parasite relationship, which on the one hand facilitate the development of the parasite in the host’s skin, and on the other have an inhibitory effect on inflammatory reactions. As a result, at the beginning of an infestation, host defence processes are suppressed (especially in the first four weeks of the infestation), allowing the initial maintenance of the mite population. Later, the increasing parasite loads release more antigenic substances which trigger an inflammatory response stimulated by a cytokine cascade (of interleukin (IL)-1α, IL-1β, IL-6, IL-8 and tumour necrosis factor α) and pro-inflammatory mediators (histamine and leukotrienes) (8, 9), which cause swelling, congestion, pain and pruritus (28, 29). One of the more notable effects of mite infestation is the stimulation of IL-20 release affecting keratinocyte proliferation, which leads to thickening and elasticity loss of skin. However, the inflammatory process is also inhibited by the IL-1 receptor agonist modulating the immune response and inflammatory reactions related to interleukin 1 (8). As a result, in individuals with an efficient immune system, the development of the infestation is somewhat balanced and its intensity and symptoms are usually only locally marked.

It has been observed that scabies in wolves is most often limited to certain parts of the animal’s skin (the hind legs, tail and head) (Video S2) and only in extreme cases affects all parts of the body (41, 49, 55). Immune response mechanisms can also explain one species’ greater susceptibility to scabies than another’s (44). It was recently demonstrated that S. scabiei infection induces more inflammatory cell infiltration in the skin of foxes than in that of wolves, which is related to less effective defence permitting severe hyperkeratotic lesions to develop in the smaller carnivores (44). Wolves also engage more macrophages as a result of skin infestation, which more effectively reduce the inflammation at the onset. However, in immunosuppressed animals, the disease can progress dynamically and cover the entire skin surface. The extensive inflammatory process further reduces the body’s ability to defend itself against other pathogens, resulting in the death of the animal from disease not necessarily directly caused by the infestation. The cases of Sarcoptes scabiei and Demodex co-infections in wolves described in this study are a model example of the development of an infestation in a debilitated animal. The season and age of the animals were previously observed to be risk factors for scabies (18, 23, 67). The infestation may be life threatening because of the extensive inflammatory process in afflicted animals, which have a negative energy balance associated with the damage to the protective skin barrier and hypothermia, these resulting in changes in behaviour and an inability to hunt which further exacerbate the energy deficiency. Interestingly, immunosuppression together with adverse climatic conditions may lead also to high mortality of sarcoptic animals in climates at the opposite extreme. Scabies infestations were observed in subadult giraffes in Kenya, which suffered from starvation because of drought, limited access to food and competition for it with the pastoral communities and their livestock (1). The survival of a wolf depends mostly on its ability to hunt and/or remain part of the pack. Solitary wolves have less chance to survive the winter. The most severely alopecic wolves observed in the BNP lived alone, and some used hay stacks as their individual resting place rather than the pack den. In the extreme cases, the sick wolves starved to death, despite seemingly remaining active and even playful until the end (Video 1). However, this impression was misleading and the wolves’ activity was due to the skin lesions’ extreme itchiness. Our observations suggest that these wolves only hunted small mammals or birds, similarly to foxes, which are the species mostly affected by scabies. This behaviour made their risk of scabies infestation many times higher than that of animals in the pack. The risk is further increased by the possibility of indirect transmission through mites surviving for several days outside the host in conditions of high humidity and moderate temperatures. Mild winter conditions are a factor favouring mite survival outside the host. Also, the lack of snow cover as another environmental condition of a mild winter made it difficult for wolves to find food, and changed them from predators to scavengers, and thus may indirectly have had a significant impact on the persistence of infestations in the host population. Furthermore, as described previously (37), the predation of red deer by wolves in the BF depends on the snow cover depth. In warmer months wolves would choose wild boar over deer (37). However, the wild boar population in the area has declined dramatically, which may have further depleted the wolves’ food base and exacerbated the poor health of the sarcoptic individuals.

An assessment of the epidemiological situation should also take into account the presence of other predators that may be both competitors and sources of infection. As shown recently for foxes in Spain (11), camera health monitoring should be considered an effective tool for the conservation of protected species such as the wolf and has the advantage of being non-invasive. The wolf’s conservation is a matter with a rising profile because the increasing population sizes of the species in many parts of Europe and environmental changes may promote the spread of pathogens and increase the risks of an epidemic, which is shown here at the micro-scale of the BFo. Furthermore, as predators, wolves are a good model species for exposure to infectious and non-infectious threats, as their food is mostly wildlife. An additional motivation for their surveillance is that wolves can potentially contribute to the spread of diseases, even those that are not a threat to them (5, 12, 13, 39, 40, 62, 65, 69).

An outbreak of severe cases of mange related to mixed infestation of Sarcoptes and Demodex mites, which caused higher wolf morbidity and mortality in the Białowieża Forest in the winter of 2021/2022, was the result of several cofactors. Climate alterations such as rises in air and ground temperatures, a decrease in humidity, a thinning of the snow cover and shortening of its period in recent years may have contributed to the emergence of mange by influencing the ecology and behaviour of wolves and their prey. Other potential drivers included the growth of the wolf population and the disturbances in their habitat by anthropogenic factors such as the migration crisis on the border between Poland and Belarus. The crisis, which started in 2021 with an influx of thousands of refugees from Asia and Africa through the BF, has also entailed increased activity by the military and border services. This could have affected the general health status of wolves by causing them stress-induced immunosuppression and increasing their susceptibility to sarcoptic mange in the favourable weather conditions.