DOI: 10.7589/2014-10-251 Journal of Wildlife Diseases, 51(3), 2015, pp. 651–663 # Wildlife Disease Association 2015 KNEMIDOKOPTINID (EPIDERMOPTIDAE: KNEMIDOKOPTINAE) MITE INFESTATION IN WILD RED-CROWNED PARAKEETS (CYANORAMPHUS NOVAEZELANDIAE): CORRELATIONS BETWEEN MACROSCOPIC AND MICROSCOPIC FINDINGS Bethany Jackson,1,2,7 Allen Heath,3 Cathy Harvey,4 Carly Holyoake,2 Richard Jakob-Hoff,1 Arvind Varsani,5,6 Ian Robertson,2 and Kris Warren2 1 Auckland Zoological Park, Motions Road, Western Springs, Auckland 1022, New Zealand 2 School of Veterinary and Life Sciences, College of Veterinary Medicine, Murdoch University, Murdoch 6150, Western Australia, Australia 3 Hopkirk Research Institute, Massey University, Private Bag 11008, Palmerston North 4442, New Zealand 4 New Zealand Veterinary Pathology, Auckland Zoological Park, Motions Road, Western Springs, Auckland 1022, New Zealand 5 School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand 6 Biomolecular Interaction Centre, University of Canterbury, Private Bag 4800, Christchurch, 8140, New Zealand 7 Corresponding author (email: [email protected]) ABSTRACT: During a study on health and disease in Red-crowned Parakeets (Cyanoramphus novaezelandiae) on Tiritiri Matangi Island and Little Barrier Island (Hauturu-o-Toi) in New Zealand between 2011 and 2013, an outbreak of feather loss prompted the collection of skin biopsies (n5135) under anesthesia from the head of captured birds. A subset of samples (n57) was frozen to obtain whole specimens for identification of ectoparasites. Mites (range 1–11) were observed in 79/135 (58.5%) skin biopsies, whereas feather loss was only found in 47/142 (33.1%) birds captured during the sampling period. Compact orthokeratotic hyperkeratosis and acanthosis were found in association with mites. Procnemidocoptes janssensi (Acari: Epidermoptidae, Knemidokoptinae) was identified from whole mites obtained from skin biopsies. We describe the presence, pathology, and stages of infestation for knemidokoptinid mange in a wild parrot population in New Zealand. Given the clinical and pathologic changes observed and poor knowledge of the parasite’s New Zealand host and geographic distribution, further work is recommended for this and sympatric parrots, to understand relationships between the host, parasite, environment, and expression of disease. Results from this study reinforce the value of including biopsy samples for the investigation of skin disease in wild birds, particularly to link etiologic agents with pathologic changes. Key words: Biopsy, Cyanoramphus novaezelandiae, disease outbreak, Knemidokoptinae, mange, mites, parrots, wildlife disease. INTRODUCTION close contact for transmission (Mu¨llenand Durden 2009). Mites are the primary cause of parasitic There are six genera and 17 species in skin and feather disease in birds (Harrison the Knemidokoptinae (Fain and Elsen and Lightfoot 2006; Fletcher 2008), having 1967; Fain 1974; Fain and Lukoschus evolved to adapt to different environments 1979; Mironov et al. 2005). Historically, and hosts. The most prevalent mites in the literature has focused on those of domestic birds are in the family Epider- significance to poultry and caged birds, moptidae, subfamily Knemidokoptinae including ‘‘scaly face’’ (Knemidocoptes (Harrison and Lightfoot 2006). These pilae; Lavoipierre and Griffiths 1951) in epidermoptid or skin mites cause mange budgerigars (Melopsittacus undulates; in a broad avian assemblage, including Yunker and Ishak 1957), depluming itch Passeriformes, Galliformes, and Psittaci- (Neocnemidocoptes gallinae and Picicne- formes (Wade 2006). Their morphology midocoptes laevis; Pence 1972) in poultry and biology resemble the mammalian and pigeons, respectively (Fain and Elsen parasites, Sarcoptidae, with all life stages 1967) and scaly leg (Knemidocoptes being present on the host and requiring mutans; Robin and Lanquetin 1859) in 651 652 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 3, JULY 2015 TABLE 1. Avian families commonly infested by the Knemidokoptinae, with species of mites found and area of the body affected during clinical disease. Translated and adapted to reflect current nomenclature (Fain and Elsen 1967). Host family Knemidokoptinae species reported Areas affected Galliformes Knemidokoptes mutans Legs Neocnemidocoptes gallinaea Body Columbiformes Picicnemidocoptes laevisb Body Psittaciformes Knemidokoptes pilae Beak, legs, and rarely skin of body Procnemidocoptes janssensi Body Passeriformes Knemidokoptes fossor Base of beak Knemidokoptes jamaicensis Legs Knemidokoptes intermedius Legs a Formerly reported as Neocnemidocoptes laevis gallinae. b Formerly reported as Neocnemidocoptes laevis laevis. poultry (Morishita et al. 2005). Knemido- clinical symptom is feather loss, not hyper- koptinid mange has been considered un- keratosis (Fain and Elsen 1967). common in wild birds (Mainka et al. Knemidokoptinid mange lesions are 1994); however, in the past 15 yr, there mostly confined to the stratum corneum, has been an increase in reports of these with mild to severe compact orthokerato- parasites in a range of wild birds (Mainka tic hyperkeratosis and acanthosis (Fletcher et al. 1994; Ladds 2009; Dabert et al. 2008). Often tunnels are formed within 2011; Dabert et al. 2013), particularly the crusts and filled with mites (Black- Passeriformes (Mason and Fain 1988; more 1963; Mason and Fain 1988), Jaensch et al. 2003; Holz et al. 2005; lending a honeycombed appearance that Low et al. 2007; Gaudioso et al. 2009). may be evident macroscopically. Dermal Clinical signs of knemidokoptinid mange changes are less common and may include vary based on the host and parasite species a perivascular mononuclear infiltrate (Ma- (see Table 1). Knemidokoptes pilae infesta- son and Fain 1988; Ladds 2009) or tion, most common in budgerigars, causes a heterophilic infiltrate (Fletcher 2008). hyperkeratotic encrustations on the beak, Subcorneal pustules and mites burrowing cere, and legs (Koski 2002) that may affect beneath the stratum corneum have also perching and behavior (Beck 2000) or cause been reported (Low et al. 2007). respiratory compromise in advanced cases Here, we present findings from an (Ladds 2009). Severe hyperkeratosis leading investigation of feather loss in two island to loss of whole digits and feet has been populations of Red-crowned Parakeet reported in American Robins (Turdus (RCP; Cyanoramphus novaezelandiae), migratorius)withKnemidokoptes jamaicen- where pathologic changes were linked to sis (Turk 1950), including reluctance to feed a knemidokoptinid mite. We describe (Pence et al. 1999). Clinical signs are normal RCP skin, the pathology and stages generally in featherless areas, such as the of mange in this species, and key features beak, legs, and feet, and characterized by that enabled identification and differenti- hyperkeratosis of varying severity (Wade ation of the mite species from similar 2006). Proliferative papillary-like lesions members of the Knemidokoptinae. (Kirmse 1966; Schulz et al. 1989) may be confused with other diseases, such as MATERIALS AND METHODS avianpox (Kirmse 1966). Exceptions to the hyperkeratotic presentation include de- Location and sampling design pluming itch of fowl and pigeons, where Sampling took place in March and Septem- lesions are found on the body and the main ber 2012 on Tiritiri Matangi Island (36u369 JACKSON ET AL.—KNEMIDOKOPTINID MITE MANGE OF WILD RED-CROWNED PARAKEETS 653 20S, 174u539240E), and June 2013 on H&E and examined under light microscopy. Little Barrier Island (LBI; Hauturu-o-Toi; Images were taken using a camera mount for 36u119320S, 175u49290E) in the Hauraki Gulf microscopes. Mites were only counted if of New Zealand. We captured RCP using sections of bodies (idiosoma) were visible. standard mist nets (932.6 m, 30-mm mesh, Mites were often visible across multiple Avinet, Freeville, New York, USA), placed in sections and easily identified as the same single-use cotton bags (Prospectors Earth individual based on size, location, and sur- Sciences, Baulkham Hills, New South Wales, rounding structures. These were not double Australia), and taken to a field processing counted. station. Birds were anesthetized with isoflur- ane at an initial flow rate of 5% in 1-L oxygen, Recovery and processing of mites reducing to 1–2% isoflurane in 1-L oxygen after approximately 30 s. A zero dead-space Frozen stored skin samples were examined circuit was used to minimize anesthetic risk under a dissecting microscope. Mites were (Advanced Anesthesia Specialists, Ryde, New recovered by placing skin samples on a glass South Wales, Australia). Samples were collect- slide, adding a drop of Hoyer’s medium, and ed for other studies (not reported here), dissecting out whole specimens using micro- including blood, feathers, and feces. A skin tools (Minitools, Australian Entomological biopsy (3–5 mm) was taken from the caudal Supplies, Coorabell, New South Wales, Aus- aspect of the base of the head, using fine sharp tralia). Each slide was examined by light scissors and forceps, and placed in 10% microscopy after clearing, with images and neutral buffered formalin. The site was measurements for later taxonomic purposes a common place for feather loss, could be taken of each mite. easily standardized across birds, and was in a better location for healing than other areas of Serial section examination the head. In a subset of seven severely affected To investigate mite distribution across the individuals from