VDIXXX10.1177/1040638715581677Acariasis in finchesRettenmund et al. research-article5816772015

Brief Communication

Journal of Veterinary Diagnostic Investigation 5–­1 Microlichus americanus acariasis in saffron © 2015 The Author(s) Reprints and permissions: sagepub.com/journalsPermissions.nav finches (Sicalis flaveola) with dermatitis and DOI: 10.1177/1040638715581677 feather loss jvdi.sagepub.com

Christy L. Rettenmund,1 Robert J. Ossiboff, Denise McAloose, Wayne Knee, Susan E. Wade, Jean A. Paré

Abstract. Over a 5-year period, 13 saffron finches ( flaveola) housed in mixed aviaries at the Bronx Zoo (Bronx, New York) were examined with feather loss and dermatitis, primarily affecting the nape, neck, and dorsum. Feather loss, hyperkeratosis, epidermal hyperplasia, and mixed granulocytic and mononuclear inflammation were identified in biopsies from live and tissue sections from necropsy specimens. In 10 of 13 cases, sections of arthropod parasites were seen histologically within feather follicles and along the surface of affected skin. Based on morphological characteristics, mites recovered from samples of formalin-fixed skin in 4 birds were identified as Microlichus americanus, an epidermoptid mite infrequently reported from wild birds and hippoboscid flies. Gross and histological lesions strongly implicate M. americanus as the cause of dermatitis affecting practically all saffron finches in the collection.

Key words: Acariasis; avian; dermatitis; Emberizidae; Epidermoptidae; folliculitis; Microlichus americanus; mites; ; saffron finches; Sicalis flaveola; Thraupidae.

The saffron finch (Sicalis flaveola) is a small, bright yellow veterinary treatment when abnormal feathering over the nape neotropical passerine native to South America, ranging from and crown was first seen (finches 1 and 2). Ten other birds to . Introduced populations also exist in (finches 3–12) were on exhibit in a large free-flight mixed other locales, including Puerto Rico, Jamaica, and Hawaii. aviary and were either examined opportunistically when The birds travel in pairs or small flocks, forage on the ground trapped (finches 3 and 4) or were found dead (finches 5–12). for insects and seeds, and visit feeders in suburban back- A single saffron finch was housed in a third exhibit yards.14 Based on molecular studies, saffron finches and before it was moved to a smaller enclosure for treatment of other species in the Sicalis were recently transferred bacterial dermatitis (finch 13). from the Emberizidae family (buntings and New World spar- Four live saffron finches were clinically evaluated at the rows) to the Thraupidae family and are now taxonomically Bronx Zoo for dermatitis (finches 1–4). All birds initially affiliated with (Remsen JV, et al., Version 03-06- had feather loss along the nape and neck, with thickened 2015, A classification of the bird species of South America, and rugose skin in the affected region (Fig. 1A). No other Part 10, Proposal 93. Available from: http://www.museum. clinical signs or abnormal physical examination findings lsu.edu/~Remsen/SACCBaseline10.htm). were noted in any of these birds. Finches 1 (female) and In October 2009, a group of 15 smuggled, presumably 2 (male) were adults, estimated to be ~3 years old, were wild-caught saffron finches were confiscated in Connecticut. housed together as a pair, and had almost identical feather No notable skin lesions were observed on arrival and loss along the nape of the neck, exposing yellow-orange, throughout a 30-day quarantine period at the Wildlife Con- corrugated skin. Skin biopsies were obtained from both birds servation Society’s (WCS) Central Park Zoo (New York). under anesthesia with isofluranea in oxygen via facemask. Following quarantine, the birds were placed in various exhibits at the Bronx Zoo (Bronx, New York) where many bred successfully. From 2010 through 2014, most finches From the Wildlife Conservation Society, Zoological Health Program, Bronx, NY (Rettenmund, Ossiboff, McAloose, Paré); Canadian National developed progressive feather loss over the nape, crown, and Collection of Insects, Arachnids and Nematodes; Agriculture and Agri- neck (Fig. 1A, inset) and of those, 13 were individually Food Canada, Ottawa, Ontario, Canada (Knee); Department of Population examined by WCS clinical veterinarians (finches 1–4) and/ Medicine and Diagnostic Sciences, College of Veterinary Medicine, or pathologists (finches 1, 5–13). The index cases were 2 Cornell University, Ithaca, NY (Wade). finches housed together in a small exhibit with multiple other 1Corresponding Author: Christy L. Rettenmund, 2300 Southern bird species. The birds were moved into a small box cage for Boulevard, Bronx, NY 10460. [email protected]

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Figure 1. Dermatitis associated with Microlichus americanus infestation in saffron finches (Sicalis flaveola). A, photographs of affected saffron finches showing feather loss and hyperkeratosis of the skin of the back of the head, nape and dorsum. Sutures are present at previous biopsy sites. B, photomicrograph of an affected feather follicle. The epidermis and follicular epithelium are hyperplastic (EH) with hyperkeratosis (HK) and the accumulation of inflammatory debris within the feather follicle and the keratin. Sections of arthropod fragments (arrows) are present within the follicle. Hematoxylin and eosin (HE). 100×. C, dermal inflammatory infiltrates included mononuclear cells (lymphocytes and plasma cells, denoted by asterisks) and granulocytes (eosinophils and heterophils, denoted by arrows). HE. 400×. Inset: positive staining granulocyte granules, consistent with eosinophils. Luna stain. 1,000×. D, arthropods (arrows) were also infrequently present along the surface of the epidermis with associated epidermal hyperplasia (EH), eosinophilic inflammation (arrowhead), and intercellular edema. HE. 400×.

Despite treatment with ivermectinb (0.2 mg/kg orally every treatments were discontinued. Finch 1 died 1 month after 10 days for 3 doses initially, then every 14 days for 6 addi- discontinuing treatments and was submitted for postmor- tional doses), lesions on the head and neck progressed in tem examination, at which time no mite fragments were both birds. When yeast were identified on histology, a com- present in the skin sampled (see below). Finch 2 was lost to bination of itraconazolec (10 mg/kg orally every 24 hr for follow-up. 120 days on food) and topical 1% chlorhexidined solution Finches 3 and 4, adult males housed in a large free-flight (every 24 hr for 120 days) were initiated followed by a aviary, were noted to have feather loss of unknown duration course of treatment with voriconazolee (10 mg/kg orally and were examined when opportunistically caught. Both every 24 hr on food for 45 days), but none of these treat- birds had feather loss on the back of the head, nape, and neck ments resulted in any improvement. After 8 months, all with thickening but no discoloration of the underlying skin.

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The birds were anesthetized with isofluranea in oxygen via facemask for collection of skin biopsies of the affected region and were treated with ivermectinb (0.4 mg/kg topi- cally every 14 days for 3 treatments). Finch 3 regrew all the feathers over the head, nape, and neck within 4 weeks post- treatment. Finch 4 was found dead of traumatic injuries after the third ivermectin treatment with minimal signs of feather regrowth. During the period between January 2010 and July 2014, 15 saffron finches that were found dead on exhibit were sub- mitted for postmortem evaluation. Ten of these birds were found to have dermatitis including the previously described finch 1 and 9 additional birds (finches 5–13; 4 fledglings, 5 adults). The nape and neck were typically affected. Histo- logic features of skin from the biopsied and necropsied birds Figure 2. Dorsal view of a female Microlichus americanus were similar. The epidermis and follicular epithelium were digested with potassium hydroxide from affected, formalin-fixed moderately thickened (hyperplasia), and the stratum cor- saffron finch (Sicalis flaveola) skin. Bar = 100 μm. neum was moderately to markedly thickened by compact to basket-weave, orthokeratotic keratin (hyperkeratosis; Fig. 1B). Follicular ostia were frequently void of feathers and slide warmer at 45°C for 2 hr; parasite identification was per- often dilated by orthokeratotic hyperkeratosis. Granulocytic formed using morphology based on published species and mononuclear inflammatory cells were present within the descriptions. Mites were present in all samples (Fig. 2). Mor- dermis and surrounding dermal vessels amid variable phological features, including a long dorsal palpal tibial seta amounts of fibrosis. Granulocytes also multifocally infil- with a conical base, chitinous crescentic band posterior to the trated the epidermis and follicular epithelium (Fig. 1C), anus uninterrupted, shape of epimera I–IV, extent of punc- occasionally forming small aggregates (Fig. 1D). Histo- tured area of the epimera, and length and width of the body, chemical staining (Luna stain) highlighted a granulocyte were all diagnostic for a small mite, Microlichus americanus 1,4 subpopulation with red-orange granule reactivity, consistent (order Sarcoptiformes, family Epidermoptidae). with eosinophils (Fig. 1C, inset). In 11 of the 13 (84.6%) The Epidermoptidae is a family of mites that occur in or examined cases, complete or partial arthropod segments on the skin of birds, and many species can cause avian were present within feather follicles (Fig, 1B) or, rarely, mange. The family was recently expanded to include scaly along the surface of the stratum corneum (Fig, 1D). In finch face and leg mites in the Knemidokoptinae subfamily, for- 8,10 12, a focal, chronic epidermal ulcer was present in the skin of merly the Knemidokoptidae family. Mites of the genera the caudal dorsum that was histologically characterized by Microlichus and Myialges are closely related and can cause similar inflammation and the presence of associated arthro- dermatitis in birds. These mites have evolved a peculiar rela- pod segments. Serial sections of skin samples of finches 4 and tionship with ectoparasitic insects that feed on their avian 13 did not reveal mite fragments. In conjunction with the host. While male and juvenile mites live on the skin surface mites, surface-associated bacteria (n = 5) or ovoid yeast (n = in epidermal burrows or feather follicles of the bird, mature 3) were noted in a subset of cases. In one of the cases where gravid females disperse on avian ectoparasites, typically hip- no mites were identified (finch 13), granulomatous dermati- poboscid flies. Female Myialges mites are hyperparasites tis with intralesional, acid-fast–positive bacilli, consistent that attach to flies, feed on fly hemolymph, and lay clusters with cutaneous mycobacteriosis, was diagnosed. Acid-fast– of eggs on their hosts that hatch into larvae. In contrast, positive bacilli and/or granulomatous dermatitis were not females of genus Microlichus studied to date are merely pho- noted in any other finch. retic and use hippoboscid flies for dispersal to other avian Other postmortem findings in these 10 finches included hosts, and, as such, the host range of Microlichus is a func- 1,8,9,12 air sacculitis and/or pneumonia (n = 3), proventricular para- tion of their hippoboscid hosts. sitism and inflammation (n = 2), hepatitis (n = 1), and trauma There are several species in the genus Microlichus. Micro- (n = 1). Dermatitis was not believed to be the cause of death lichus americanus is closely related to and may be a subspe- 4 in any bird, although debilitation secondary to chronic skin cies of Microlichus avus. These minute mites (length of inflammation may have predisposed the birds to other dis- 170–390 µm) are easily overlooked on visual inspection, 1,4,5 ease conditions. Seven birds were in good body condition, especially in the absence of skin lesions. Accounts of while 3 birds were noted to be thin. avian dermatitis caused by M. americanus, or other Microli- Samples of formalin-fixed skin from 4 birds (finches 5, 6, chus species, are rare compared with those caused by Myial- 8, and 10) were submitted for digestion using 3 g of potas- ges spp. and knemidokoptine mites. Both M. avus and M. sium hydroxide dissolved in 2 mL of water and placed on a americanus have been associated with similar skin lesions in

Downloaded from vdi.sagepub.com by guest on April 12, 2015 4 Rettenmund et al. birds, including crateriform ulcers, feather loss, and severe reported to harbor M. americanus mites with no obvious skin mange.1,4,12 Microlichus americanus dermatitis was reported inflammation, and it may be that estrildid and viduid finches in 2 captive but recently imported birds at the Antwerp Zoo, are more tolerant of this mite than saffron finches.7 However, a California quail (Lophortyx californicus; syn. Callipepla given the peculiar mode of dispersal of M. americanus, we californica) and a baywing (Molothrus badius), as well as hypothesize that transmission of mites from saffron finches from an asymptomatic wild rusty blackbird (Euphagus caro- to other aviary bird species was negligible due to the lack of linus) and a wild grey catbird (Dumetella carolinensis) in the hippoboscid vectors. Acariasis in both adult saffron finches United States.4 Microlichus americanus has also been recov- and captive-born progeny suggests that direct transmission ered from polyxenous hippoboscid flies (Ornithomyia frin- among saffron finches occurred when birds were in close gillina) collected from a Swainson’s thrush (or, olive-backed contact, as in the nest. thrush; Catharus ustulatus swainsoni), a common grackle Three birds (finches 1–3) with acariasis were treated with (Quiscalus quiscula), and a field sparrow (Spizella pusilla) ivermectin, but in only 1 bird (finch 1) were posttreatment in Rhode Island.12 Microlichus mite infestation without visi- biopsies obtained. Mites were not present in tissue sections ble skin lesions has been reported in several other avian spe- posttreatment (finch 1) and 1 finch (finch 3) regrew all feath- cies, and M. americanus in particular has been found on ers, suggesting ivermectin was efficacious in eradicating the asymptomatic spectacled weavers (Ploceus ocularis), lesser mites. However, resolution of clinical signs and regrowth of masked weavers (Ploceus intermedius), and red bishops feathers was not noted in finches 1 and 2 despite 8 months of (Euplectes orix) in Africa.1–3,6,7,11,13 treatment. Severe, extensive, and likely irreversible damage In none of the few documented M. americanus reports is to follicles, as identified histologically, and secondary bacte- dermatitis described in multiple birds within a flock or col- rial and fungal infection may explain why feather loss and lection. In contrast, 10 of 15 (66.7%) saffron finches submit- dermatitis persisted. Treatment with 0.2 to 0.4 mg/kg of iver- ted to the WCS pathology department for postmortem mectin every 14 days for 2 to 3 treatments seemed to be evaluation between 2010 and mid-2014 had gross or histo- effective. logic evidence of acariasis. The distribution of feather loss, In summary, this report documents chronic acariasis and epidermal hyperplasia, hyperkeratosis, and inflammation dermatitis in a captive population of saffron finches, charac- over the head, nape, and dorsum was strikingly similar in all terized by active eosinophilic, heterophilic, and lymphoplas- birds. This may reflect a site predilection of the mites, or macytic infiltration of the skin and feather follicles, with more likely an inability or restricted ability for the birds to intralesional mites. Microlichus americanus was strongly preen or reach this area. Crateriform lesions, although previ- incriminated as the cause of disease in these birds. ously reported in birds with Microlichus acariasis, were rare in the birds in this study (1/13, 7.7%).1,4 Acknowledgments The saffron finches in this case series were either confis- We thank the Wildlife Conservation Society’s Department of Orni- cated birds, for which there was no prior history, or the prog- thology, Special Exhibits, and clinical medical staffs for eny of those birds. It is suspected that the finches were their exceptional care, Alfred Ngbokoli and Daniel Friedman for infested with mites on arrival despite the absence of observ- slide preparation, and the additional pathologists who provided able lesions. Characteristic skin lesions were only noted in diagnostic support in the above cases (Drs. Alisa Newton, Ken Con- these finches after they were moved to various indoor exhib- ley, and Carlos Rodriguez). its and aviaries. The absence of hippoboscid flies in an indoor captive setting may have hindered dispersal of gravid female Sources and manufacturers mites and led to unusually heavy individual mite burdens, a. MWI Veterinary Supply Inc., Boise, ID. which resulted in increased expression of pathogenicity or b. Norbrook Laboratories Ltd., Co. Down, Ireland. morbidity. Affected saffron finches were housed in exhibits c. Centocor Ortho Biotech Products, Ravitan, NJ. with a variety of other small , including red- d. Fort Dodge Animal Health, New York, NY. cheeked cordonbleu finches (Uraeginthus bengalus), red- e. Sigma-Aldrich, St. Louis, MO. headed finches (Amadina erythrocephala), red-faced crimson-wing finches (Cryptospiza reichenovii), African fire Declaration of conflicting interests finches (Lagonosticta rubricata), strawberry finches (or, red The author(s) declared no potential conflicts of interest with respect avadavat; Amandava amandava), Togo paradise whydahs to the research, authorship, and/or publication of this article. (Vidua togoensis), and bananaquits (Coereba flaveola), as well as several ground-dwelling birds such as blue ground Funding doves (Claravis pretiosa), tambourine doves (Turtur tympa- The author(s) disclosed receipt of the following financial support nistria), crested partridges (Rollulus rouloul), and cinnamon for the research, authorship, and/or publication of this article: teals (Anas cyanoptera), none of which ever showed evi- Financial support was provided by the Wildlife Conservation Soci- dence of dermatitis. African ploceid weavers have been ety for the publication of this article.

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References 8. Mironov SV, et al. Phylogeny and evolution of parasit- 1. Baker AS. Order Astigmata. In: Mites and Ticks of Domestic ism in feather mites of the families Epidermoptidae and : An Identification Guide and Information Source. Dermationidae (Acari: Analgoidea). Zool Anz 2005;243: London, England: The Stationery Office, 1999:63–65. 155–179. 2. Brown NS, Wilson GI. A comparison of the ectoparasites of 9. Mueller NS, et al. Host records and phenology of louse-flies on the house sparrow (Passer domesticus) from North America Wisconsin birds. Transactions 1969;57:189–207. and Europe. Am Midl Nat 1975;94:154–165. 10. O’Connor BM. Cohort Astigmatina. In: Krantz GW, Walter 3. Doster GL, et al. Ectoparasites collected from bobwhite quail in DE, ed. A Manual of Acarology. 3rd ed. Lubbock, TX: Texas the southeastern United States. J Wildl Dis 1980;16:515–520. Tech University Press, 2009:586. 4. Fain A. A review of the family Epidermoptidae Trouessart par- 11. Philips JR. A review and checklist of the parasitic mites asitic on the skin of birds (Acarina: Sarcoptiformes). Brussels: (Acarina) of the Falconiformes and Strigiformes. J Raptor Res Paleis der Academien, 1965:1–176 (Part I); 1–144 (Part II). 2000;34:210–231. 5. Furman DP, Tarshis IB. Mites of the genera Myialges and 12. Phillips JR, Fain A. Acarine symbionts of louseflies (Diptera: Microlichus (Acarina: Epidermoptidae) from avian and insect Hipposboscidae). Acarologia (Paris) 1991:32:377–384. hosts. J Parasitol 1953;39:70–78. 13. Radford CD. The mites (Acarina: Analgesidae) living on or 6. Keymer IF, et al. A survey and review of parasitic diseases of in the feathers of birds. Parasitology 1953;42:199–230. wild and game birds in Great Britain. Vet Rec 1962;74:887–894. 14. Rising JD. Family Emberizidae (buntings and new world spar- 7. Lindholm AK, et al. Persistence of passerine ectopara- rows). In: del Hoyo J, et al., ed. Handbook of the Birds of the sites of the diederik cuckoo Chrysococcyx caprius. J Zool World. Vol. 16, Tanagers to New World Blackbirds. Barcelona, 1998;244:145–153. Spain: Lynx Edicions, 2011:633–634.

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