Hypoderma

Hypoderma

Biology
The six species widely recognised in the genus Hypoderma, commonly called heel flies, warble flies or cattle grubs, are restricted to the Holarctic region where they parasitise various Bovidae and Cervidae. The adult flies are either medium to large sized (11-18 mm) bumble-bee mimics (H. bovis, H. lineatum, H. tarandi), or slightly smaller (11-14 mm) and less hairy flies.

Most information on oestrid biology comes from studies of the three species of major economic importance, H. bovis and H. lineatum on cattle and H. tarandi on reindeer. Adults are especially active on warm, sunny days. Despite their inability to feed, H. tarandi are capable of lengthy flights, an adaptation to pursuit of their migratory reindeer hosts (Nilssen and Anderson, 1995). Females of Hypoderma lay their eggs on the hairs of the host’s lower body and legs, either singly (H. bovis) or in batches of up to 15, laid side by side along the same hair shaft (H. lineatum, H. tarandi). In H. lineatum, at least, females actively select hairs of a particular diameter on which to deposit eggs. Thus, while the mean diameter of randomly selected hairs was 0.04 mm, that of hairs with eggs was 0.07 mm and thicker hairs tended to have more eggs (Jones, 2000). Such selection may be an adaptation to shorten incubation and promote hatching. Karter et al. (1992) showed that, under controlled conditions in the laboratory, H. tarandi oviposit close to the base of newly grown hairs and that newly hatched larvae show a positive thermotaxis. They concluded that these behaviours would also promote near maximum hatchability, a short incubation period and high transmission efficiency. A specialised basal attachment organ with a prominent clasper is found on the eggs, enabling them to lock firmly around the hair shaft and attachment is further enhanced by an adhesive material (Cogley et al., 1981). After hatching, the first instar larvae penetrate the skin and undergo a migration through the body tissues to overwintering sites. Routes of migration and sites for overwintering differ between species of Hypoderma. Larvae of H. bovis migrate along nerves to the spinal cord and overwinter within the epidural fat around the thoracic and lumbar vertebrae. Larvae of H. lineatum migrate along connective tissues and between the fascial planes of muscles to overwinter within the submucosa of the oesophagus. Migration routes of H. lineatum are characterized by yellow or greenish gelatinous, edematous areas with an overwhelming eosinophil infiltration (Panciera et al., 1993). The larvae resume migration the following spring and move to the back where a small, subcutaneous swelling develops and the growing larva cuts a hole to the skin surface. The larva orientates in the swelling, the “warble”, so that its posterior respiratory spiracles are placed at the opening of the hole, enabling the larva to breath as it grows, feeding on cellular debris and exudates. Larvae exit their warbles after 30-60 days, falling to the ground where they pupariate. After eclosion, the adults live for only a few days. Those of H. bovis live on average for 3-4 days and the females are reproductively well adapted to this short, non-feeding life style - they emerge from the puparium with all their eggs fully developed, and the capacity to immediately mate and then oviposit on cattle (Scholl & Weintraub, 1988). Mating takes place away from the host, at aggregation points where females are intercepted in flight or when they land close to a male (Anderson et al., 1994).

Veterinary and medical significance
The species of major economic importance are H. bovis and H. lineatum. Their impact is due to the breathing holes of the warbles, which are enlarged during development and significantly degrade the value of the hide, resulting in serious losses to the cattle industry of the Holarctic region (Scholl, 1993). Cattle grubs were estimated to cause annual losses (excluding control) of over US$600 million in the United States (Drummond et al., 1981). Recent data from northern China indicate annual losses to hides of US$15,000,000 (Yin et al., 2003). Hides of reindeer are similarly affected by H. tarandi, with records from Alaska of up to 2000 warble scars per hide (Washburn et al., 1980). In the Magadan region of the far east of the former USSR, 23% of deer hides were downgraded due to warble fly damage (Shumilov and Nepoklonov, 1983). This reflects the high prevalence of infestations by all species of Hypoderma in endemic areas. For cattle warbles, prevalence in Europe ranges from 0% to over 80%, depending on the levels of control (Colebrook and Wall, 2004). In China the infestation rate in Yaks is generally 80-90% but can rise to 100% (Yin et al., 2003). In northern Norway, Folstad et al. (1991) recorded 99.9% prevalence of infection of reindeer with H. tarandi. Prevalences of H. diana and H. actaeon in deer are typically over 50% and up to 90-100% (Colebrook and Wall, 2004). Compared to losses to the hide industry, other production losses due to hypodermosis are probably small, e.g., losses due to decreased weight gain and milk production, but these are more difficult to quantify. The persistence of the females, in particular those of H. bovis, in laying from 300 to 800 eggs induces a dramatic escape response in cattle, termed “gadding”. This behaviour is thought to be a potential cause of injury, spontaneous abortion and reduced milk production but, again, the losses are difficult to quantify. Occasionally, mammals other than the natural hosts can be infested by larvae of Hypoderma, including humans. Hypodermosis in man most frequently features skin allergies accompanied by blood eosinophil differential counts varying from subnormal to 60% above the normal (Boulard & Petithory, 1977). A rare case of hypereosinophilia of a two-year-old boy was reported by Navajas et al., (1998) with fever, muscle pain and heart, CNS and skin involvement. The condition resolved completely when several larvae of H. bovis were removed from scalp nodules. The severity of human infections varies with the site of the larvae, from a "creeping myiasis" caused by subdermal migrations (Uttamchandani et al., 1989), to ophthalmomyiasis interna resulting in visual loss (Edwards et al, 1984, Kearney et al., 1991), to rare intracerebral myiasis (Kalelioglu et al., 1989) which has also been reported in calves (Caracappa et al., 1996).

Hosts and Distribution

Primary Source
Adapted from:

• Colwell, D.D., M. Hall, P.J. Scholl. (2006). A synopsis of the biology, host, distribution, disease and management of the genera. Pages 218-304 in Colwell, D.D., Hall, M., Scholl, P.J. (eds). The Oestrid Flies: Biology, Host-Parasite Relationships, Impact and Management. CAB International, Oxford, UK. x + 359 pp.

References

• Anderson, J.R., Nilssen, A.C. and Folstad, I. (1994) Mating behaviour and thermoregulation of the reindeer warble fly, Hypoderma tarandi L. (Diptera: Oestridae). Journal of Insect Behaviour 7: 679-706.
• Boulard, C. and Petithory, J. (1977) Serological diagnosis of human hypodermosis: a preliminary report. Veterinary Parasitology 3: 259-263.
• Caracappa, S., Loria G.R., Donn, A., Manfredi, M.T. and Guarda, F. (1996) Hypoderma bovis neuropathology in veal calves: case report. European Jouranl of Veterinary Pathology 2: 35-38.
• Cogley, T.P., Anderson, J.R., and Weintraub (1981) Ultrastructure and function of the attachment organ of warble fly eggs (Diptera: Oestridae: Hypodermatinae). International Journal of Insect Morphology and Embryology 10: 7-18.
• Colebrook, E. and Wall, R. (2004) Ectoparasites of livestock in Europe and the Mediterranean region. Veterinary Parasitology 120: 251-274.
• Drummond, R.O., Lambert, G., Smalley, H.E.Jr. and Terrill, C.E. (1981) Estimated losses of livestock to pests. In, CRC Handbook of Pest Management in Agriculture (D. Pimentel, ed.). Pp. 111-127. Boca Raton, CRC Press, 597 pp.
• Edwards, K.M., Meredith, T.A., Hagler, W.S. and Healy, G.R. (1984) Ophthalmomyiasis interna causing visual loss. American Journal of Ophthalmology 97: 605-610.
• Folstad, I., Nilssen, A.C., Halvorsen, O. and Andersen, J. (1991) Parasite avoidance: the cause of post-calving migrations in Rangifer? Canadian Journal of Zoology 69: 2423-2429.
• Kalelioglu, M., Aktürk, G., Aktürk, F., Komsuoglu, S.S., Kuzeyli, K., Tigin, Y., Karaer, Z. and Bingöl, R. (1989) Intracerebral myiasis from Hypoderma bovis larva in a child. Journal of Neurosurgery 71: 929-931.
• Karter, A.J., Folstad, I. and Anderson, J.R. (1992) Abiotic factors influencing embryonic development, egg hatching, and larval orientation in the reindeer warble fly, Hypoderma tarandi. Medical and Veterinary Entomology 6: 355-362.
• Kearney, M.S., Nilssen, A.C., Lyslo, A., Syrdalen, P. and Dannevig, L. (1991) Ophthalmomyiasis caused by the reindeer warble fly larva. Journal of Clinical Pathology 44: 276-284.
• Navajas, A., Cardenal, I., Piñan, M.A., Ortiz, A., Astigarraga, I and Fdez-Teijeiro, A. (1998) Hyperosinophilia due to myiasis. Acta Haematologica 99 27-30.
• Nilssen, A.C. and Anderson, J.R. (1995) Flight capacity of the reindeer warble fly, Hypoderma tarandi (L.), and the reindeer nose bot fly, Cephenemyia trompe (Modeer) (Diptera: Oestridae). Canadian Journal of Zoology 73: 1228-1238.
• Panciera, R.J., Ewing, S.A., Johnson, E.M., Johnson, B.J. and Whitenack, D.L. (1993) Eosinophilic mediastinitis, myositis, pleuritis, and pneumonia of cattle associated with migration of first-instar larvae of Hypoderma lineatum. Journal of Veterinary Diagnostic Investigation 5: 226-231.
• Scholl, P.J. (1993) Biology and control of cattle grubs. Annual Review of Entomology 39: 53-70.
• Scholl, P.J. and Weintraub, J. (1988) Gonotrophic development in Hypoderma lineatum and H. bovis (Diptera: Oestridae), with notes on reproductive capacity. Annals of the Entomological Society of America 81: 318-324.
• Shumilov, M.F. and Nepoklonov, A.A. (1983) Ecology and control of the reindeer warble fly in the Magadan region, USSR. Pp. 50-53 in, Veterinarnaya Entomologiya i Akarologiya, Nepoklonov, A.A. (Ed.), Moscow, USSR.
• Uttamchandani, R.B., Trigo, L.M., Poppiti, R.J., Rozen, S. and Ratzan, K.R. (1989) Eosinophilic pleural effusion in cutaneous myiasis. Southern Medical Journal 82: 1288-1291.
• Washburn, R.H., Klebesadel, L.J., Palmer, J.S., Luick, J.R. and Bleicher, D.P. (1980) The warble-fly problem in Alaska reindeer. Agroborealis
• 12: 23-28. Yin, H., Ma, M., Yuan, G., Huang, S., Liu, Z., Luo, J. and Guan, G. (2003) Hypodermosis in China. Journal of Animal and Veterinary Advances 2: 179-183.