Avian knemidokoptosis, caused by knemidokoptid mites (Knemidokoptinae: Epidermoptidae), has been reported in wild and domestic birds globally. We report two cases of severe knemidokoptosis in Dunnocks (Prunella modularis) from separate sites in Great Britain, where the disease has previously been reported predominantly in finches and, less frequently, in corvids.
Knemidokoptosis has been reported in a wide range of wild and domestic birds. The causative agents are mites of the subfamily Knemidokoptinae (Epidermoptidae), of which 15 species across six genera are currently recognized (Mironov et al. 2005). Knemidokoptes jamaicensis is the mite most frequently reported in wild birds, having been detected in more than 40 species of passerines globally (Dabert et al. 2013; Jackson et al. 2015; Janra et al. 2018).
The presentation of knemidokoptosis is variable, dependent upon host, parasite, and environmental factors (Pence 2008). Knemidokoptes jamaicensis can cause a disease known colloquially as “scaly leg,” characterized by hyperkeratotic dermatitis, most commonly affecting the distal legs and feet (Dabert et al. 2013).
Most reports of knemidokoptosis in wild birds involve gregarious passerines such as the American Robin (Turdus migratorius) and the Common Chaffinch (Fringilla coelebs; Pence et al. 1999; Lawson et al. 2018a). In Great Britain (GB), knemidokoptosis is widespread in chaffinches and also occurs, albeit less frequently, in European Greenfinches (Chloris chloris), European Goldfinches (Carduelis carduelis), Eurasian Bullfinches (Pyrrhula pyrrhula), Rooks (Corvus frugilegus), Eurasian Jackdaws (Corvus monedula), and Carrion Crows (Corvus corone; Pennycott 2016; Lawson et al. 2018a). Although most cases in wild birds appear to be mild or moderate, it has been proposed that severe lesions might predispose individuals to predation, other trauma, or coinfection (Pence 2008; Lawson et al. 2018a).
The Dunnock (Prunella modularis) is a small, omnivorous, predominantly solitary, ground-feeding passerine found throughout Europe and western Asia (Davies 1992). Dunnocks are frequently observed in peridomestic habitats and their population in GB is considered stable (Harris et al. 2020).
Here we report severe knemidokoptosis in an atypical species, involving two Dunnocks found dead in southern England that were submitted for postmortem examination as part of a GB wildlife disease surveillance scheme. The first bird (D1) was discovered in February 2019 and the second (D2) in January 2020, at separate sites, roughly 270 km apart.
Postmortem examinations were conducted following a standardized protocol (Lawson et al. 2010). Both birds were adult females in normal body condition, based on assessment of muscle mass and body weight. Severe skin lesions were evident in both cases. In D1, proliferative beige, powdery, scaley lesions with marked skin thickening were limited to both distal legs and feet (Fig. 1A). In D2, similar severe lesions were noted on the head and neck (Fig. 1B), with milder lesions affecting the ventrum and legs (Fig. 1C). Both birds exhibited digit loss: D1 had a single digit missing whereas D2 had lost the distal phalanges of three digits (Fig. 1A, C, respectively). In both birds, the cause of death appeared to be acute trauma, with gross lesions in both cases including rib fractures with associated pulmonary and subcutaneous hemorrhage. Based on the circumstances of carcass discovery, window collision or cat predation were considered to be the most likely causes of trauma.
Microscopic examination of crush preparations of skin lesions from both birds showed numerous Knemidokoptes sp. mites. Wet preparations of small intestinal contents revealed no metazoan or protozoan parasites. Bacteriological culture of the liver, small intestinal contents, and skin lesions yielded Staphylococcus aureus from all three sites in D2, but no significant growth from D1. Staphylococcus aureus is a commensal bacterium frequently isolated from the skin of birds, and opportunistic infection can occur where the integrity of the skin barrier is compromised (Benskin et al. 2009).
Histopathological examination of sections of affected skin from both birds revealed severe multifocal chronic dermatitis with epidermal hyperplasia and hyperkeratosis. Within the stratum corneum, Knemidokoptes sp. mites were admixed with multifocal aggregates of bacteria, indicating secondary bacterial infection (Fig. 2). Dermal involvement was apparent in both birds, with infiltration of predominantly mononuclear cells (lymphocytes and plasma cells) and fewer heterophils, eosinophils, and macrophages. In D2, liver, spleen, brain, heart, and lung were also examined, with no abnormalities or indication of comorbidities evident, except those associated with trauma or autolysis. The poor state of carcass preservation in D1 only allowed for histopathological examination of the skin.
Previously, passerine knemidokoptosis in GB has almost exclusively been reported in species of the families Fringillidae and, much less frequently, Corvidae. Over the period of August 2005 to January 2020, a total of 95 Dunnocks have been examined postmortem within this wildlife disease surveillance scheme, but the two described here are the first in which knemidokoptosis has been diagnosed.
The severe presentation of knemidokoptosis in these two cases probably predisposed both birds to trauma, through impairment of vision or locomotion. The etiological factors underlying this severe presentation could relate to the host, parasite, environment, or a combination thereof.
Host immunosuppression is one possible contributory factor; no evidence of nutritional debility, concurrent disease or underlying immunosuppressive viral infection (e.g., circovirus infection) was detected, although extensive histopathological examination was limited to only one of the birds and no specific virological examinations were performed. Techniques such as next generation sequencing or microarray could be used to investigate the occurrence of coinfections in future investigations. Both Dunnocks were found in winter, which might indicate an underlying seasonal immunosuppressive effect, as has been suggested in the epizootiology of salmonellosis in passerines in GB (Lawson et al. 2010).
Knemidokoptes jamaicensis is the most likely species of knemidokoptid mite to be involved in these cases, considering lesion morphology and host species (Pence 2008). Dabert et al. (2013), however, suggest that K. jamaicensis might comprise a multispecies complex, with variations in target host and virulence between multiple cryptic species. It is therefore possible that these Dunnocks were infected with a hypervirulent knemidokoptid. Further investigation using molecular techniques on knemidocoptic mites from the affected Dunnocks and from a range of wild birds could provide further insight into the taxonomy and diversity of these parasites in GB.
Both Dunnocks were found in the winter, when southern England experiences an influx of Common Chaffinches migrating from continental Europe (Wernham et al. 2002). With knemidokoptosis being widespread among chaffinches in GB, and a peak of infection known to occur in the winter months, it is possible that this creates a greater biotic reservoir of infection, heightening the risk of interspecific spillover from chaffinches to other passerines (Lawson et al. 2018a). This risk could be compounded by a concomitant increase in congregations of passerines using supplementary feeding stations during the winter months when natural food sources can be scarce (Lawson et al. 2018b).
We thank the members of the public who reported these two incidents. This work was supported by the Department for Environment, Food, and Rural Affairs and the Welsh Government through the Animal and Plant Health Agency's Diseases of Wildlife Scheme Scanning Surveillance Programme (project ED1600), the Esmée Fairbairn Foundation, the Banister Charitable Trust, and the Universities Federation for Animal Welfare.