Hypopi of Hypodectes propus (Acari: Hypoderatidae) in two southern crowned pigeons (Goura scheepmakeri).
Article Type: Report
Subject: Ectoparasitic infestations (Diagnosis)
Ectoparasitic infestations (Care and treatment)
Authors: Da Silva, Mari-Ann O.
Pence, Danny B.
Bertelsen, Mads F.
Pub Date: 06/01/2012
Publication: Name: Journal of Avian Medicine and Surgery Publisher: Association of Avian Veterinarians Audience: Academic Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2012 Association of Avian Veterinarians ISSN: 1082-6742
Issue: Date: June, 2012 Source Volume: 26 Source Issue: 2
Geographic: Geographic Scope: Denmark Geographic Code: 4EUDE Denmark
Accession Number: 298292705
Full Text: Abstract: Necropsy of 2 4-year-old southern crowned pigeons (Goura scheepmakeri) that died from a presumed case of botulism revealed hundreds of small, cyst-like structures in the pectoral subcutaneous tissues. The structures were identified as heteromorphic deutonymphs of Hypodectes propus (Order Astigmata) of the family Hypoderatidae. The immobile, immature hypopi were individually encapsulated, mostly in adipose tissue, and evoked only a mild inflammatory infiltration of predominately macrophages with some heterophilic granulocytes. The infection was not considered a serious health problem and was interpreted as an incidental finding. To our knowledge, this is a new host record for H propus.

Key words: Hypodectes propus, hypopi, subcutaneous, avian, southern crowned pigeon, Goura scheepmakeri

Clinical Report

A pair of 4-year-old southern crowned pigeons (Goura scheepmakeri) kept at the Copenhagen Zoo in Denmark died from a presumed case of botulism. Both birds were born in captivity. The male was hatched and raised at the Copenhagen Zoo, whereas the female was hatched in the Hong Kong Zoological and Botanical Gardens and was imported to Denmark via the Rotterdam Zoo approximately 6 months before its death. The pair were brooding their first egg when they died; the likely source of toxins was contaminated feed. In both cases, the birds were lethargic and demonstrated paralysis of the neck and partial paralysis of the wings. Supportive treatment with fluids, nonsteriodal anti-inflammatory drugs, and antibiotics was unsuccessful, and the birds died the next day after exhibiting clinical signs.

At necropsy, the carcasses of both pigeons appeared grossly normal. White, ovoid-cylindrical, cyst-like structures approximately 1 mm long were found in the subcutaneous adipose tissue covering the pectoral musculature and extending caudally along the sides of the body (Fig 1a). The female bird displayed hundreds of these structures, whereas the male had substantially more. On microscopic examination, the structures were classified as sack-like mites. The skin covering the affected areas appeared slightly swollen. The underlying subcutaneous connective tissue was swollen and hyperemic. No other significant macroscopic findings were found. Selected tissue samples of heart, lungs, liver, spleen, kidneys, gastrointestinal tract, and brain were collected in 10% formalin and processed routinely for histopathologic examination. Mites were collected and stored in 70% ethanol, and a subsample of mites was prepared for electron microscopy (Fig 2). Mites were subsequently mounted in Hoyer's media under Glyptal epoxy enamel--ringed OO-thickness cover glasses. They were identified as heteromorphic deutonymphs (hypopi) of Hypodectes propus (Nitzch, 1861). (1,2)

Microscopically, cross-sections of hypoderatid deutonymphs were present in the subcutaneous pectoral tissues throughout the affected areas (Fig lb). Mites were present predominantly in the subcutaneous adipose layer, but some were found in the dermis and underlying musculature. The cross-sectioned hypopi were individually encapsulated and had no contact with each other. Surrounding the deutonymphs were varying numbers of primarily macrophages and fewer heterophilic granulocytes. This inflammatory response was most pronounced in the more heavily infected male individual. Histopathologic abnormalities were not detected in any of the other sampled tissues.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Discussion

Due to their small size, astigmatic mites (Subclass Acari) are able to survive in habitats and ecological niches unavailable to larger arthropods, including a multitude of microhabitats on and in the bodies of the host animals. (3) Hypodectes propus is generally associated with pigeons, herons, and egrets. (3-6) This species has developed a complex symbiotic relationship with its hosts by exploiting resources of their subcutaneous adipose tissues? (1-3) During their sojourn within the host, the hypopi increase 10-fold in size (4,5) and become widely dispersed as a result of the migratory behavior of their hosts. (4,7) This phoretic relationship compensates for the disadvantages of small size in longdistance migration and the lack of morphologic adaptation (eg, wings) for independent migration. (6) To our knowledge, this is the first description of hypopi of H propus in the southern crowned pigeon (Order Columbiformes).

The deutonymph or hypopus is a developmental instar of mites, and in H propus it is one of 5 juvenile stages including the prelarva, larva, protonymph, deutonymph, and tritonymph. (5) The deutonymph differs from the other stages by the absence of functional mouthparts and an alimentary tract. (4) However, this stage is the only fully parasitic stage (5) and this stage obtains all the nutrition for the entire life cycle of the parasite (3,4) through its exoskeleton. (6,8) Deutonymphs penetrate the skin of their hosts a few days after young birds hatch in the nest. (1,3) The mechanism by which they enter the skin is still unknown. The hypopi persist and grow in the subcutaneous adipose tissue until the host reaches maturity and begins to incubate its eggs. (4) All other life stages are residents in the nests of their hosts. (4,9) It is considered that the development and exodus of the mature deutonymph from the host depends on the hormone prolactin in the host during brooding. (4) The inflammatory response to hypoderatid mites in the adipose and other subcutaneous tissues of various birds ranges from a few foamy macrophages and plasma cells in the vicinity of the living hypopi in some hosts to a severe and diffuse granulomatous inflammation in some heavily infected birds. (10) Dead and degenerating hypopi may be attended by a more organized fibroplasia with a surrounding cuff of Langhans' giant cells and masses of epithelioid histiocytes, lymphocytes, plasma cells, and eosinophils. (10) However, most studies indicate that hypopi have little effect on the health of the host and are usually regarded as incidental findings at necropsy. (9,10) In accordance with these studies, infection with H propus did not appear to be the cause of death of the crowned pigeons in this case.

Considering the behavior and life cycle of H propus, these southern crowned pigeons were most likely infected as chicks in their original environments. However, it is notable that none of the zoological gardens involved with this pair have previously seen cases of acariasis caused by H propus in any bird species. The exact source of infection is therefore unknown. Hypopi are resting deutonymphs and because they are hormonally activated, presumably may exist in a bird for long periods. This would explain their persistence for 3 years in the birds that had not previously nested.

Acknowledgments: We acknowledge the assistance of the late Mr Jose Bresciani of the University of Copenhagen for producing the electron microscopic images. We also thank Mr Rob Belterman of Rotterdam Zoo and Mr Leonard Ting of Hong Kong SAR Government.

References

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(2.) Fain A, Bafort J. Cycle evolutif et morphologie de Hypodectes (Hypodectoides) propus (Nitzsch) acarlen nidicole a deutonymphe parasite tissulaire des pigeons. Bull Acad Roy Sci Belgique. 1967;53: 501-533.

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(4.) Evans GO. Principles of Acarology. Cambridge, UK: CAB International; 1992.

(5.) Mullen GR, OConnor BM. Mites (Acari). In: Mullen GR, Durden LA, eds. Medical and Veterinary Entomology. San Diego, CA: Academic Press; 2002:449-516.

(6.) Philips JR. A review and checklist of the parasitic mites (Acarina) of the Falconiformes and Strigiformes. J Raptor Res. 2000;34(3):210-231.

(7.) Houck MA, OConnor BM. Ecological and evolutionary significance of phoresy in the Astigmata. Annu Rev Entomol. 1991;36:611-636.

(8.) Mironov SV, Kivganov DA. Descriptions of adult stages of new and little known mite species of the family Hypoderatidae (Acari: Astigmata) from nests of aquatic birds. Acarina. 2010;18(1):37-59.

(9.) Hendrix CM, Kwapien RP, Porch JR. Visceral and subcutaneous acariasis caused by hypopi of Hypodectes propus bulbuci in the cattle egret. J Wildl Dis. 1987;23(4):693-697.

(10.) Pence DB. Acariasis. In: Atkinson CT, Thomas N J, Hunter DB, eds. Parasitic Diseases of Wild Birds. Ames, IA: Wiley-Blackwell; 2008:527-536.

Mari-Ann O. Da Silva, DVM, Danny B. Pence, PhD, and Mads F. Bertelsen, DVM, DVSc, Dipl ACZM

From the Center for Zoo and Wild Animal Health, Copenhagen Zoo, Roskildevej 38, DK-2000 Frederiksberg, Denmark (Da Silva, Bertelsen); and 1616 Blackburn Fork Rd, Cookeville, TN 38501, USA (Pence).
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