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Parasites of birds of prey: Their diagnosis and treatment
Parasites of Birds of Prey: Their Diagnosis and Treatment Stephen A. Smith, D VM, PhD
The health and survival of both free-living and captive birds of prey can be severely jeopardized by numerous species of parasites, including a diverse variety of protozoans, helminths, and arthropods. Most parasitic infections cause little or no harm to healthy individuals but can become a significant problem for raptors that are stressed by captivity, illness, or injury. Thus, it is important to correctly recognize, diagnose, and control those parasitic species that are capable of resulting in pathological conditions. Copyright 9 1996 by W. B. Saunders Company. Key words: Raptor, parasites, pathology, treatment.
ontinued interest in raptor rehabilitation and the breeding of captive birds of prey has brought concern for their veterinary care to the forefront. The health and vigor of both free-living and captive birds o f prey can be severely compromised by a wide variety of internal and external parasites, including numerous species of protozoans, helminths, and arthropods. 1-5 Most parasitic infections in wild birds of prey usually cause little or no distress to healthy individuals. However, parasites can become a significant health problem for raptors that are held in prolonged captivity in confined housing and for raptors that have recently come into captivity that are stressed by injury, illness, or exposure to the new environment. Thus, it is important to recognize, diagnose, and control those parasitic species that are capable of producing clinical disease in the raptorial host. The purpose of this contribution is to describe the more c o m m o n parasites, discuss their clinical significance, and provide information on their control and treatment.
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Protozoans A n u m b e r of protozoan blood parasites have been d o c u m e n t e d in birds of prey and include various species of Haemoproteus (Fig 1), Leucocytozoon (Fig 2), and Plasmodium. 6-s These parasites are e n c o u n t e r e d fairly commonly in some wild populations of raptorial birds, although their
importance is not well understood. Transmission of these protozoans is usually via some f o r m of biting arthropod, but there is little information available as to the exact species of vector involved for each specific parasite. Very little pathogenicity has been consistently attributed to many of these h e m o p r o t o z o a n species, but. there are an increasing n u m b e r of accounts suggesting that high parasitemias can have detrimental affects on the health of raptors. Clinical signs include listlessness, weakness, and a n e m i a ) Another protozoan parasite that often has clinical significance in raptors, especially captive falcons and free-living goshawks and owls, 1~ is the flagellate Trichomonas sp, which causes a disease syndrome commonly r e f e r r e d to as "frounce." This protozoan produces raised, yellow, caseous plaques on the tongue and oropharyngeal surfaces. Large lesions often make swallowing difficult for the bird and sometimes results in the raptor being reluctant to feed, which can ultimately lead to starvation. In addition to invading the tissues of the oropharynx, this parasite has also been reported to occur in the anterior portions of the gastrointestinal tract (esophagus, ventriculus, and proventriculus) and disseminated t h r o u g h o u t the parenchyma of the liver of raptors.X x An additional group of protozoan parasites reported from birds of prey includes n u m e r o u s species of intestinal and renal coccidia of the genera Eimeria spp, Caryospora spp, and Frenkelia sp. 12,13 Although no obvious pathology appears to result from coccidia] infections occurring in the kidneys o f raptors, there are several reports
From the Department of Biomedical Sciences and Pathobiology, Virginia-Maryland Regional College of Veterinar~ Medicine, Virginia PolytechnicInstitute and State University, Blacksburg, VA. Address reprint requests to Stephen A. Smith, DVM, PhD, Department of Biomedical Sciences and Pathobiology, VirginiaMaryland Regional Collegeof VeterinaryMedicine, VirginiaPolytechnic Institute and State University, Blacksburg, VA 24061-0442. Copyright9 1996by W. B. Saunders Company. 1055-937X/96/0502-000655.00/0
Seminars in Avian and Exotic Pet Medicine, Vol 5, No 2 (April), 1996: pp 97-105
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Figm'e 1. Hemoproteussp (arrow) in a red blood cell of a Great Horned Owl. W&G stain, bar = 10 urn. of mortality being associated with intestinal infections of coccidia. 12 Clinical signs of intestinal coccidiosis include watery, mucoid, or bloody diarrhea with n u m e r o u s small spherical oocysts. O t h e r protozoan parasites of unknown significance r e p o r t e d f r o m birds of prey include b o t h Sarcocystis sp and Babesia s p . 14
Helminths The helminths (or platyhelminths) can be further subdivided into the nematodes, trematodes, cestodes, a n d acanthocephalans. T h e nematodes r e p r e s e n t the largest group of these internal parasites that infect birds of prey and include ascarids, capillarids, spirurids, a n d tracheal and air sac nematodes. The n e m a t o d e s are
Figure 2. Leucocytozoonsp in an extremely deformed white blood cell of a great horned owl. This hemoprotozoan may also invade red blood cells. W&G stain, bar = 10 urn.
also generally the m o s t potentially p a t h o g e n i c of the c o m m o n raptorial parasites. Most adult nematode species occur mainly in the gastrointestinal tract of the bird, but some may occur in the respiratory, cardiovascular, and ocular systems as well. Ascarids are one of the m o r e c o m m o n n e m a todes occurring in raptors and include species of Ascaridia, Contracaecum, and Porrocaecum.15,16 These are the largest of the nematodes inhabiting the gastrointestinal tract of birds of prey, often measuring 30 to 100 m m in length. Ascarids generally occur in the small intestine, particularly the d u o d e n u m , but may also be found in the proventriculus, ventriculus, and large intestine. In small numbers, these parasites are generally not overtly pathogenic and usually cause only occasional unthriftiness and slight weight loss. However, in large numbers, ascarids may p r o d u c e obvious clinical disease and death. Obstruction of the intestinal tract with large n u m b e r s of ascarids has b e e n described in British Kestrels (Falco tinnunculus), whereas perforation of the small intestine has b e e n r e p o r t e d in two juvenile Great H o r n e d Owls (Bubo virginianus) in which each bird contained m o r e than 120 mature ascarids in the ventriculus and small intestine, several of which had p e r f o r a t e d the intestinal wall and were partially located in the abdominal cavity of the b i r d ) Ascarids may have either a direct or an indirect life cycle involving an a r t h r o p o d paratenic (transport) or intermediate host. Ascarid eggs are of two distinct m o r p h o logical types: one similar to the ovum of the poultry ascarid (Ascaridia galli), and the o t h e r similar to the canine r o u n d w o r m (Toxascaris leonina) (Fig 3).1 Capillaria spp (threadworms) a p p e a r to be the most c o m m o n type of n e m a t o d e parasitizing b o t h captive and free-living birds of prey. Smith 3 r e p o r t e d 54% of the free-living hawks, falcons, and eagles and 78% of the free-living owls examined in that study as being parasitized by CapiUaria spp. Included in this diverse g r o u p of tissue-inhabiting n e m a t o d e s are species that infect the mouth, o r o p h a r y n x , esophagus, crop, small intestine, a n d cecum of raptors. Intestinal infections of CapiUaria spp are usually asymptomatic, but with heavy infections the bird may demonstrate clinical signs of diarrhea, anorexia, emaciation, and listlessness. O t h e r species of capillarids can p r o d u c e significant tissue d a m a g e
Parasites of Birds of Prey
Figure 3. Common nematode eggs found in the mutes of birds of prey. The egg in the upper right is typical of an ascarid (ie, Porrocaecumsp), whereas the middle egg is typical of a capillarid. The pseudoparasite in the lower left is an egg from the mouse urinary bladder nematode (Trich0m0s0ides crassicauda), which is passed unchanged through the digestive tract of the raptor. Bar = 50 um. by burrowing into the mucosa causing varying degrees of inflammation and e d e m a (Fig 4). C o o p e r 17 attributed two cases of " f r o u n c e " (a superficial oropharyngeal disease usually attributed to the p r o t o z o a n Trichomonas sp) in falcons to Capillaria contorta. H e described the presence of a white necrotic exudate and diptheritic m e m b r a n e s in the buccal cavity and p h a r y n x of a Peregrine Falcon (Falco peregrinus) and a RedH e a d e d Merlin (Falco chicquera ruficollis) caused by the mucosal migration of these parasites. A
Figure 4. Histological section demonstrating the tissue migration of CapiUariaspp in the mucosal lining of the esophagus of a Red-Tailed Hawk. Note the typical capillarid egg next to the cross-section of the mature nematode. H&E stain, bar = 50 urn.
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similar observation was m a d e by Trainer et al is who r e p o r t e d a "caseous growth" in the throat o f two gyrfalcons (Falco rusticolus) to be caused by a CapiUaria sp infection. Clausen and G u d m o n s son, 19 in the examination of the cause of death of gyrfalcons f r o m Iceland, found 36% h a d died as a direct result of an u p p e r alimentary tract infection of C contorta. The eggs of these avian capillarids most closely resemble the ova of trichurids f r o m domestic animals but are often m o r e elongated in shape (Fig 3). In addition to finding the eggs in the mutes (fecal material) of raptors, eggs may also be c o m m o n l y observed in scrapings of suspected lesions in the oral m u c o s a o f the bird. A n u m b e r of species of spirurids, c o m m o n l y called stomach worms, occur in the l u m e n and submucosa of the proventriculus and ventriculus of birds of prey. Habronema sp has b e e n described f r o m the ventriculus of n u m e r o u s species of raptors including hawks, kestrels, eagles, and owls, 20'2I whereas Hatertia sp has been described f r o m the proventriculus of an i m m a t u r e Prairie Falcon (Falco mexicanus). 22 Several species of Microtetrameres have b e e n reported in the proventriculus of the Great H o r n e d Owl, goshawk (Accipiter gentilis) and Golden Eagle (Aquila chrysaetos), ~ Red-Tailed Hawk (Buteo jamaicensis), 3 and Snowy Owl (Nyctea scandiaca), t5 whereas Tetrameres sp has b e e n reported from the Barred Owl (Strix varia). 24 In these later species of stomach worms, the adult female w o r m resides within the l u m e n of the glandular tissue of the proventiculus causing apparently little or no i n f l a m m a t o r y reaction, whereas the male generally inhabits only the lumen of the proventriculus (Fig 5). Ova of these n e m a t o d e parasites are of the typical spirurid type containing an embryonated larvae. An insect paratenic host is probably required for the transmission of this parasite. Tracheobronchial infections with Syngamus sp a n d Cyathostoma sp have been reported in numerous species of raptors, 25,26but their prevalence in free-living raptor populations appears to be very low. These parasites are usually few in n u m b e r but can cause inflammation and sometimes partial or complete obstruction of the trachea, p r o d u c i n g clinical signs of dyspnea and openm o u t h e d breathing. Nematodes of the genus Cyathostoma were r e p o r t e d as the p r i m a r y cause of a fatal parasitic p n e u m o n i a in a free-living Saw-Whet Owl (Aegolius acadicus), two free-living
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Figttre 5. Histological section demonstrating a typical spirurid nematode, Microtetrameres sp, within the lumen of the glands of the proventriculus of a RedTailed Hawk. Note the lack of a host inflammatory response. H&E stain, bar = 50 urn. Screech Owls (Otus asio), and four captive-bred juvenile Burrowing Owls (Speotyto cunicularia).26 Younger birds a n d smaller-sized birds are generally m o r e severely affected than larger adult birds. T h e eggs are large, double-operculate, ellipsoidal ova similar to Syngamus trachea of domestic poultry. A paratenic host, such as an earthworm, is required for the completion of the life cycle. Serratospiculum amaculata is primarily a parasite of falcons but may also occur in o t h e r species of raptors. This elongate n e m a t o d e is often f o u n d coiled in the air sacs, serous m e m b r a n e s
o f the viscera, or in the connective tissue of the abdominal or thoracic cavity of birds. Clinical signs may include respiratory difficulty caused by pathological changes and thickening of the air sacs. S. amaculata has b e e n r e p o r t e d f r o m b o t h Peregrine Falcons and Prairie Falcons, 99,27 the Bald Eagle (Haliaeetus leucocephalus), 21 a n d a Cooper's Hawk (Accipiter cooperii).28 This parasite does not a p p e a r to b e particularly pathogenic in low numbers; however, a n u m b e r of mortalities in prairie falcons as a result of this parasite have b e e n described by both Bigland et al 2s a n d Kocan and Gordon. 29 Ward and Fairchild 22 rep o r t e d several cases of suspected Serratospiculum sp infection in prairie falcons where the air sacs of one dyspneic bird were filled with h u n d r e d s of adult nematodes. Ova are small, thin-shelled eggs that are e m b r y o n a t e d when passed in the mutes of the bird. Because the adult n e m a t o d e s inhabit the air sacs, the ova must be c o u g h e d up and swallowed to insure transmission. In the r e p o r t of the Prairie Falcons where S amaculata was considered the major contributing cause of death, smears of necrotic foci in the liver, spleen, and h e a r t and of necrotic lesions in the crop and esophagus all contained large n u m b e r s of larvated ova and free larvae of this parasite. '~7 Therefore, additional clinical signs of this type of infection may include general unthriftiness and emaciation caused by the invasion and inflammation of the gastrointestinal tract. O t h e r n e m a t o d e s that have b e e n r e p o r t e d in birds of prey include Physaloptera sp in the ventriculus of Red-Tailed Hawks, Sharp-Shinned Hawks (Accipiter striatusi), Cooper's Hawk, and Red-Shouldered Hawks (Buteo lineatus). 3~ In addition, Thelazia sp has b e e n r e p o r t e d in the orbit of the eye of a Swainson's Hawk (Buteo swainsonii), ~2 and filarial n e m a t o d e s have b e e n described f r o m the heart of a Peregrine Falcon. ss A n u m b e r of accounts also describe filarial worms in the blood of various birds of prey, but the clinical significance of these parasites are n o t known. Small n u m b e r s of any of these less c o m m o n parasites have b e e n generally observed as incidental findings at necropsy and have n o t b e e n associated with any significant pathology. T r e m a t o d e parasites, especially strigeid and diplostomatid trematodes, occur c o m m o n l y in birds of prey. 34-s6These helminths generally parasitize the d u o d e n u m and are rarely considered pathogenic even in large numbers. However,
Parasites of Birds of Prey
Dedrick a7 described a fatal clinical syndrome in a Prairie Falcon characterized by p o o r condition and diarrhea associated with a strigeid trematode infection. Likewise, emaciation and ultimately death in a Bald Eagle f r o m a massive trematode infection has b e e n reported, and Greenwood et aP 8 concluded that the death o f a Saker Falcon (Falco cherrug) was caused by severe intestinal trematodiasis. In addition to the strigeid and diplostomatid trematodes, several species of dicrocoelid trematodes have been r e p o r t e d in raptors, especially f r o m the liver and bile ducts of the American Kestrel (Falco sparverius). An unidentified species of t r e m a t o d e has also been observed in the bile ducts of a 6-week-old freeliving screech owl. 3 Although rarely diagnosed by fecal examination, these liver a n d bile duct trematodes p r o d u c e an ovum that is similar to but smaller than the typical t r e m a t o d e ovum and may often be asymmetrical with a distinct protuberance at one end. 1 Cestodes are generally u n c o m m o n in birds of prey and when observed are considered to be relatively nonpathogenic. These parasites are usually located in the small intestine with their scolices firmly e m b e d d e d in the intestinal mucosa. Small n u m b e r s of tapeworms are generally well-tolerated by healthy individuals, whereas clinical signs of a heavy cestode infection are often nonspecific a n d range f r o m no obvious clinical signs to mild diarrhea and weakness. Rarely do cestodes occur in large e n o u g h numbers to cause intestinal obstruction or death of the bird. Some of the m o r e c o m m o n genera of cestodes occurring in birds of prey include Taenia, Cladotenia, Choanotaenia, Paruterina, and Paradilepis, all of which have a typical taenioid type of o v a . 39"44 In addition to fecal analysis, diagnosis of a cestode infection can often be m a d e by observing the small light-colored proglottids a r o u n d the vent or in the mutes of the bird. Infections with acanthocephalans, c o m m o n l y called T h o r n y - H e a d e d Worms, in birds of prey are relatively rare, with the notable exception of one survey in which 57% of the free-living Falconiformes and 60% of the free-living Strigiformes e x a m i n e d in Louisiana were infected. 45 These parasites are generally f o u n d in the distal small intestine of the bird with the proboscis firmly e m b e d d e d in the intestinal mucosa. Kocan and Locke 2a r e p o r t e d 7% of necropsied bald
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eagles were infected with acanthocephalans, and Kollias et a146 f o u n d 29% of various species of raptors were infected. These parasites usually cause minimal pathology other than a localized i n f l a m m a t o r y response at the site of attachment. However, in extremely heavy infections, the parasites may actually penetrate the intestinal wall and cause a generalized peritonitis resulting in the death of the raptor.
Arthropods Birds of prey may h a r b o r a wide variety of external a r t h r o p o d parasites, including numerous species of lice, a few species of H i p p o b o s c i d Flies, and occasional species of fleas, mites, and ticks. Similar to the helminths, most adult birds of prey can normally a c c o m m o d a t e small numbers of these parasites without any noticeable harmful effects. However, when a bird is debilitated, cannot p r e e n properly, or is placed in a very confined enclosure, the n u m b e r s o f these parasites may rapidly multiply to levels that further stress or complicate any preexisting condition. Lice that occur on raptors, as with all avian species, are biting or chewing lice belonging to the order MaUophaga. A large n u m b e r o f species have b e e n described from birds of prey, m o s t belonging to the genera Laemobothrion, Degeeriella, Falcolipeurus, and Kurodaia. 475~Most of the r e p o r t e d species are fairly host specific. Like o t h e r species o f chewing lice, these ectoparasites spend their entire life cycle on the bird of prey and can generally only survive a short time off the host. Eggs are generally firmly attached in clusters at the base of the shafts of body or tail feathers. Transmission is generally by direct contact with a n o t h e r suitable avian host a n d has b e e n r e p o r t e d to occur during mating, feeding of young, or during c o m m u n a l roosting of b!rds. Most birds of prey normally h a r b o r a small n u m b e r o f lice without any detrimental effect, however, large infestations of lice can cause increased restlessness, loss of sleep, increased p r e e n i n g activity, and decreased appetite. As a result of the irritation caused by the activity of the lice, the condition of the feathers may rapidly deteriorate because of excessive preening, scratching, and sometimes even feather plucking. 51 Feathers may eventually b e c o m e so
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weakened by excessive p r e e n i n g that they become highly susceptible to breakage. Hippoboscid Flies are fairly c o m m o n on birds of prey. These ectoparasites, being related to sheep keds but having wings, are rarely observed unless they crawl or fly off during handling of the bird (Fig 6). Hippoboscids are generally nonpathogenic to the raptorial host, but may be involved in the transmission of some of the blood-borne p r o t o z o a n parasites such as Haemoproteus. Myiasis, caused by other species of flies such as Calliphora spp and Protocaliphora spp, is generally only a p r o b l e m for eyesses (nestling raptors), but infestations will occasionally be observed in birds of prey secondary to chronic, o p e n traumatic injuries. 1,2 A variety of fleas, mites, ticks, and flies occur infrequently on birds of prey. Most of these external parasites are generally nest dwellers, and are, therefore, m o r e c o m m o n on eyesses and in nesting material. Large numbers of mites and larval ticks may cause severe irritation for the raptor and can result in excessive p r e e n i n g activity and feather damage. Infestations of Ornithodoros aquilae on a Prairie Falcon, Ptilonyssid Mites on American Kestrels, and Domestic Poultry Mites (Dermanyssus gaUinae and Ornithodoros sylviarum) on various species of captive raptors have all b e e n d o c u m e n t e d . 2 An unusual occurrence of tile Scaly-Leg Mite (Knemidokoptes mutans) also has b e e n reported f r o m the G r e a t H o r n e d Owl, the Snowy Owl, and accipiters. 2,52 In the case of the Great H o r n e d Owl, the
2: "22
Figure 6. This common type of Winged Hippoboscid Fly is frequently found crawling between the feathers on birds of prey. The ectoparasite is generally nonpathogenic but may be involved in the transmission of avian hemoprotozoans. Bar = 10 ram.
infestation caused bilateral foot lesions characterized by severe proliferative papillary hyperkeratosis with m o d e r a t e soft-tissue swelling. Black flies (Simulium sp) have b e e n r e p o r t e d infesting nestling raptors a n d may be i m p o r t a n t in b o t h the production of anemic conditions in the birds and in the transmission of the hemosporidian, Leucocytozoon sp. Simuliid flies also have b e e n r e p o r t e d infesting adult kestrels and Red-Tailed Hawks, but the clinical significance of these infestations is not known. In addition, ectoparasites from prey items will occasionally transfer to the raptor while the bird is feeding, but these t e m p o r a r y migrants usually do not survive long on the new host and generally do not pose a threat to the health of the raptor.
Pseudoparasites Finally, it is i m p o r t a n t to r e m e m b e r that examination of the mutes of a bird of prey will often demonstrate parasite ova that do not actually originate f r o m an infection of the bird. Eggs of parasitic mites also are often observed during routine fecal examination of raptors. It is ass u m e d that these mite eggs are swallowed by the bird during n o r m a l p r e e n i n g activity or represent contamination of the mutes from the cloacal area. Nevertheless, the discovery of mite eggs during a fecal examination is an indication that the bird should be examined for the possibility of a mite infestation. A n o t h e r example o f a pseudoparasitism involves the ability of parasite ova of prey that has b e e n eaten by a bird of prey to be passed u n c h a n g e d through the bird's digestive system. Both free-living birds that eat parasitized wild-caught prey items, as well as captive birds that are fed c o n t a m i n a t e d food items such as road kills, trapped animals, or parasitized laboratory-raised animals can be so affected. Eggs of Trichosomoides crassicauda, a c o m m o n n e m a t o d e parasite of the urinary bladder of laboratory-reared rodents, are sometimes observed during fecal examination of captive raptors fed laboratory rats (Fig 3).3 O n e way of d e t e r m i n i n g the original source of an u n k n o w n parasite egg in the mutes of a raptor is to r e p e a t the fecal examination in 2 to 3 days. If the egg originated f r o m a prey item, the egg should no longer be f o u n d in the fecal material assuming the contaminated diet of the bird has b e e n controlled or eliminated; whereas if the egg
Parasites of Birds of Prey
originated f r o m parasites o f the bird o f prey it will m o s t likely be p r e s e n t in s u b s e q u e n t fecal examinations.
Control and Treatment A variety o f anthelmintics a n d insecticides have b e e n r e p o r t e d for the removal o f internal a n d external parasites f r o m birds o f prey. ~'5~ However, because very little specific research has b e e n c o n d u c t e d o n the use a n d efficacy o f these chemicals in raptors (ie, the majority o f dosage regimens b e i n g extrapolated f r o m n o n r a p t o r i a l species a n d sometimes even n o n a v i a n species), caution s h o u l d always be exercised w h e n considering their usage. As with any animal, the physical c o n d i t i o n a n d health o f the bird o f prey m u s t be carefully c o n s i d e r e d before initiation o f treatment. In addition, e x t r e m e caution s h o u l d be used w h e n treating a sick, debilitated o r stressed bird as well as juvenile birds o f prey. Most n e m a t o d e s can be safely treated with any o n e o f a variety o f anthelmintics (Table 1). Ascarids in birds o f prey have b e e n successfully treated with piperazine, levamisote, thibendazole, mebendazole, a n d ivermectin. Both thiabendazole a n d levamisole have b e e n r e p o r t e d as b e i n g effective against Capillaria spp, b u t a seco n d administration o f anthelmintic 7 to 10 days after the initial t r e a t m e n t is often necessary to completely eliminate the infection. Two treatm e n t s o f ivermectin administered 3 to 4 weeks apart has b e e n used successfully to treat capillarid infections in raptors. 46 F e n b e n d a z o l e has also b e e n r e p o r t e d as being effective in eliminating b o t h capillarids a n d ascarids f r o m birds o f prey. M e b e n d a z o l e has b e e n suggested as a t r e a t m e n t for Microtetrameres sp a n d o t h e r spirurid n e m a t o d e s in raptors since it has b e e n used successfully to c o n t r o l s t o m a c h w o r m infections in o t h e r species of birds. Infections o f Serratospiculum amaculata have b e e n effectively treated with either t h i a b e n d a z o l e or levamisole, a n d infections o f Syngamus sp have b e e n treated with either t h i a b e n d a z o l e or m e b e n d a z o l e . A l t h o u g h most anthelmintics a p p e a r to be relatively safe a n d effective against the m o s t c o m m o n n e m a todes in raptors, it appears that f e n b e n d a z o l e , levamisole, o r ivermectin work best in raptors, a l t h o u g h levamisole may be slightly m o r e efficacious in the t r e a t m e n t o f ascarids. T h e anthelmintic s h o u l d be administered orally to the bird a n d
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Table 1. Recommended Antiparasiticals for Treating Endoparasites in Birds of Prey 3,53
Antiparasitical Agent
Dosage
Recommended Usage
Chloroquine/ Drug combi- Treat avian malaria Primaquine nation of 25 with initial dose of treamaent mg/kg/0.75 25 mg/kg chloromg/kg for quine and 0.75 initial dose, mg/kg primaquine then three PO, then three doses of 15 additional doses of mg/kg of 15 mg/kg chlorochloroquine PO only at quine only 12, 24, and 48 h. Fenbendazole 25 mg/kg PO Treat for 3 consecutive days.. 30-50 mg/kg Treat only once at this PO dosage. Ivermectin 0.2 mg/kg PO Dilute ivermectin or IM (Ivomec; Merck Sharp & Dohme, Rahway, NJ) 1:9 with water and use 0.2 rnl/kg. Repeat treatment in 34 weeks,
Levamisole Mebendazole
10-20 mg/kg PO 50 mg/kg PO
Metronidazole 30-65 mg/kg PO Piperazine Praziquantel Sulfadimethoxine
Thiabendazole
100 mg/kg PO 50 mg/kg PO or SQ 55 mg/kg PO
100 mg/kg PO
Treat for 2 consecutive days. Repeat in 10-14 days if necessary. Treat once daily for 5-7 days as necessary for trichmoniasis. Repeat in 7-10 days if necessary. Use for cestodes and trematodes. Treat one time at 55 mg/kg, then reduce dose to 25 mg/kg daily as needed for coccidia. Repeat in 10-14 days if necessary.
Abbreviations: PO, by month; IM, intramuscularly; SO.~subcutaneously. NOTE. Remember that caution must be used when treating debilitated, sick, or juvenile birds of prey. Treatment should be initiated when there is little food in the stomach of the bird. the t r e a t m e n t r e p e a t e d if necessary at the p r o p e r time interval. Anthelmintics s h o u l d be administered w h e n there is little or no f o o d in the c r o p or s t o m a c h o f the bird to decrease the a m o u n t o f d r u g inactivation a n d to r e d u c e the possibility o f v o m i t i o n or regurgitation by the bird. Because b o t h t r e m a t o d e s a n d cestodes rarely cause clinical disease in free-living birds o f prey,
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t r e a t m e n t o f i n f e c t e d raptors may be m o r e palliative t h a n necessary. However, since severe o r fatal i n f e c t i o n s d o occasionally o c c u r in captive, ill, or stressed birds, G r e e n w o o d et a145 have s u g g e s t e d that the t r e a t m e n t of i n t e s t i n a l t r e m a t o d i a s i s i n these birds may b e i n d i c a t e d . Both t r e m a t o d e s a n d cestodes have b e e n effectively a n d safely t r e a t e d with p r a z i q u a n t e l . U n f o r t u n a t e l y , t h e r e is n o k n o w n effective t r e a t m e n t for a c a n t h o c e p h a lan parasites i n b i r d s at the p r e s e n t time. T r e a t m e n t for clinical cases of avian m a l a r i a with q u i n a c r i n e h y d r o c h l o r i d e or c h o r l o q u i n e p h o s p h a t e have b e e n r e p o r t e d as e f f e c t i v e ) I n a d d i t i o n , b o t h R e d i g 53,~4 a n d R e m p l e 55 p r o v i d e extensive i n f o r m a t i o n o n the parasite, diagnosis, a n d various t r e a t m e n t a n d p r o p h y l a t i c p r o t o c o l s u s i n g a c h o r o q u i n e - p r i m i q u i n e c o m b i n a t i o n for m a l a r i a in raptors. Successful t r e a t m e n t o f a Trichomonas sp i n f e c t i o n c a n b e rapidly a c c o m p l i s h e d with m e t r o n i d o z o l e as l o n g as the lesions are n o t too extensive a n d have n o t i n v a d e d the palate. Raptors t r e a t e d with sulfa d r u g s for intestinal coccidiosis d e m o n s t r a t e d clinical i m p r o v e m e n t after 5 to 7 days of therapy. 1 T r e a t m e n t o f e x t e r n a l parasites o n birds o f prey c a n be successfully a c c o m p l i s h e d with a n u m b e r of c o m m e r c i a l l y available insecticides. 51 T r e a t m e n t with volatile substances, such as chlor o f o r m o r ether, are n o t r e c o m m e n d e d since their use is c o n s i d e r a b l y m o r e h a z a r d o u s to b o t h the b i r d a n d applicator. A louse, mite, o r tick i n f e s t a t i o n s h o u l d b e t r e a t e d with a n insecticidal dust or powder, these chemicals b e i n g the simplest a n d safest c o m p o u n d s to use (Table 2). A light d u s t i n g of a n y of these chemicals is fairly easy to apply to t h e b i r d a n d work i n a m o n g the feathers a n d i n d u c e s a m i n i m a l a m o u n t of stress f r o m h a n d l i n g o f the bird. T r e a t m e n t s h o u l d i n c l u d e a n y visibly affected b i r d a n d all o t h e r s i n
Table 2. Antiparasiticals Commonly Used for Treating Ectoparasites on Birds of Prey51 Antiparasitical Agent
Dosage
Carbaryl
0.5%
Malathion Pyrethrin
RecommendedUsage
Lightly dust bird, repeat in 10 to 14 days 5.0% Lightly dust bird, repeat in 10 to 14 days 0.5-2.0% Lightly dust bird, repeatin 10 to 14 days
NOTE. Caution nmst be used when treating stressed, sick or juvenile birds of prey.
close association with the i n f e s t e d bird. B e c a u s e a r t h r o p o d eggs are g e n e r a l l y resistant to m o s t insecticides, all b i r d s s h o u l d be r e t r e a t e d i n 10 to 14 days to kill a n y newly h a t c h e d individuals, regardless o f the ectoparasite involved o r the insecticide c h o s e n . As with the a n t h e l m i n t i c s , extreme caution should be used when treating a sick or d e b i l i t a t e d raptor. I n eyesses a n d j u v e n i l e birds o f prey, it is o f t e n p r e f e r a b l e to r e m o v e a n y ectoparasites by h a n d a n d avoid a p o t e n t i a l l y lethal insecticide e x p o s u r e .
References 1. Ward FP: Parasites and their treatment in birds of prey, in Fowler ME (ed): Zoo and Wild Animal Medicine (ed 2). Philadelphia, PA, Saunders, 1986, pp 425-430 2. Cooper JE: Veterinary Aspects of Captive Birds of Prey (ed 2). Gloucestershire, England, Standfast Press, 1985, pp 82-96 3. Smith SA: Diagnosis and treatment of helminths in birds of prey, in Redig PT, CooperJE, RempleJD, et al (eds): Raptor Biomedicine. Minneapolis, MN, University of Minnesota Press, 1993, pp 21-27 4. Taft SJ, Snchow K, VanHorn M: Helminths of some Minnesota and Wisconsin raptors. J Helminthol Soc Wash 60:260-263, 1993 5. KinsellaJM, Foster GW, Forrester DJ: Parasitic helminths of six species of hawks and falcons in Florida. J Raptor Res 29:117-122, 1995 6. Stabler RM, Holt PA: Hematozoa from Colorado birds. II. Falconiformes and Strigiformes. J Parasitol 51:927928, 1965 7. Pierce MA, Cooper JE: Haematozoa of birds of prey in Great Britain. Vet Rec 100:493, 1977 8. Greiner EC, Kocan AA: Leucocytozoon (Haemosporidia: Leucocytozoidae) of the Falconiformes. Can J Zool 55:761-770, 1977 9. Kingston N, RempleJD, Burnham W, et al: Malaria in a captive-produced F1 gyrfalcon and in two F1 peregrine falcons.J Wildl Dis 12:562-565, 1976 10. Jessup DA: Trichomoniasis in great horned owls. Mod Vet Prac 61:601-604, 1980 11. Pokras MA, Wheeldon EB, Sedgwick CJ: Trichomoniasis in owls:Report on a number of clinical cases and a survey of the literature, in Cooper JE, Greenwood AG (eds): Recent Advances in the Study of Raptor Disease. West Yorkshire, England, Chiron Publications Ltd, 1981, pp 107-110 12. MatheyWJ: Isospora buteonis Henry 1932 in an American kestrel (Falco sparve~ius) and a golden eagle (Aquila chrysaetos). Bull Wildl Dis Assoc 2:20, 1966 13. Cawthorn RJ: Cyst-forming coccidia of raptors: Significant pathogens of not?, in Redig PT, CooperJE, Remple JD, et al (eds): Raptor Biomedicine. Minneapolis, MN, Universityof Minnesota Press, 1993, pp 14-20 14. Lindsay DS, Blagburn BL: Caryospora uptoni and Frenkelia sp.-like coccidial infections in red-tailed hawks (Buteo borealis).J Wildl Dis 25:407-409, 1989
Parasites of Birds of Prey
15. Ramalingam S, Samuel MW: Helntinths in the great horned owl, Bubo virginianus, and snowy owl, Nyctea scandiaca, of Alberta. CanJ Zoo156:2454-2456, 1978 16. Hoberg EP, Miller GS, Wallner-Pendleton E, et al: Helminth parasites of northern spotted owls (Strix occidentalis caurina) from Oregon.J Wildl Dis 25:246-251, 1989 17. CooperJE: Oesophageal capillariasis in captive falcons. Vet Rec 84:634-636, 1969 18. Trainer DO, Folz SD, Samuel WM: Capillariasis in the gyrfalcon. Condor 70:276-277, 1968 19. Clausen B, Gudmunsson F: Causes of mortality among free-ranging gyrfalcons in Iceland. J Wildl Dis 17:105109, 1981 20. Chandler AC: A new spiruroid nematode, Habronema americanum, from the broad-winged hawk, Buteo platyptev'us.J Parasito127:184-185, 1941 21. Kocan AA, Locke LN: Some helminth parasites of the American bald eagle.J Wildl Dis 10:8-10, 1974 22. Ward FP, Fairchild DG: Air sac parasites of the genus Serratospiculum in falcons.J Wildl Dis 8:165-168, 1972 23. Schell SC: Four new species of Microtetrameres (Nematoda: Spiruroidea) from North American birds. Trans Am Microsci Soc 72:227-236, 1953 24. Pence DB, Mollhagen T, Forrester DF: Tetrameres(Gynaecophila) strigiphilasp. n. from the Florida barred owl, Strix varia georgica, with notes on the status of the subgenus Gynaecophila (Nematoda: Tetrameridae). J Parasitol 61: 494-498, 1975 25. Ryzhikov KM: The biology of a nematode Cyathostoma bronchialis (Syngamidae: Strongylata). Helminthologia 17:241-244, 1980 26. Hunter DB, McKeever K, Bartlett C: Cyathostoma infections in screech owls, saw-whet owls, and burrowing owls in southern Ontario, in Redig PT, CooperJE, RempleJD et al (eds): Raptor Biomedicine. Minneapolis, MN, University of Minnesota Press, 1993, pp 54-56 27. Bigland CH, Lni SK, Perry ML: Five cases of Serratospiculure amaculata (Nematoda: Filaroidea) infection in prairie falcons (Falcomexicanus). Avian Dis 8:412-419, 1964 28. Sterner MC, Espinosa RH: Serratospiculum amaculata in a Cooper's hawk (Accipitercooperii).J Wildl Dis 24:378-379, 1988 29. Kocan AA, Gordon LR: Fatal air sac infection with Serratospiculum amaculata in a prairie falcon. J Am Vet MedAssoc 169:908, 1976 30. Morgan BB: Physalopterabuteonisn. sp., a nematode from the eastern red-tailed hawk. Trans Am Microsci Soc 67:183-186, 1948 31. Wood M: Intestinal parasites in sharp-shinned hawks. The Auk 48:265-266, 1931 32. Herde KE: A new spiruroid nematode, Thelazia buteonis, from Swainson's hawk.J Parasitol 28:241-244, 1942 33. Crisp E: Filaria in the heart of a peregrine falcon. Trans Path Soc Lond 5:345, 1854 34. Chandler AC, Rausch R: A study of strigeids from owls in north central United States. Trans Am Microsci Soc 66:283-292, 1947 35. Dubois G, Rausch RL: A contribution to the study of North American strigeids (Trematoda). Am Mid Nat 43:1-31, 1950
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36. LittleJW, Hopkins SH: Trematodes from the barred owl, Strix varia, in Texas: Brachylaima mcintoshiHarkema, 1939 and Neodiplostomum reflexum Chandler and Rausch, 1947. Proc OMa Acad Sci 55:154-156, 1975 37. Diedrick ML: Note on a strigeid trematode-An intestinal parasite of a prairie falcon. J North Am Falconer's Assoc 4:12-14, 1965 38. Greenwood AG, Furley CW, CooperJE: Intestinal trematodiasis in falcons (Order Falconiformes). Vet Rec 114: 477-478, 1984 39. Alvey CH, Kintner KE: Taenia asiota n. sp. from the screech owl.J Parasito120:327-328, 1934 40. Mclntosh A: A new taenioid cestode, Cladotaenia foxi, from a falcon. Proc Helminthol Soc Wash 7:71-74, 1940 41. Schmidt FL: A new cestode, Cladotaenia ohlahomensis, from a hawk. Trans Am Microsci Soc 59:519-522, 1940 42. Mettrick DF: Some cestodes from birds of prey of the family Aquilidae. Proc Helminthol Soc Wash 30:237-244, 1963 43. Rausch R: Observations on cestodes in North American owls with the description of Choanotaeniaspeo~ytonisn. sp. (Cestoda: Dipylidiinae). Am Mid Nat 40:462-471, 1948 44. Rausch R: Paradilepis simoni n. sp., a cestode parasitic in the osprey (Cestoda: Dilepididae). Zoologica: N Y 34:1-4, 1949 45. Nickol BB: Acanthocephala of Louisiana birds. Doctoral thesis, Louisiana State University, Dissertation Abstr 27(9B), 1967 46. Kollias GV, Greiner EC, Heard D: The efficacy ofivermectin and praziquantel against gastrointestinal nematodes and trematodes in raptors. Proceedings of the First International Conference of Zoological and Avian Medicine, 1987 (abstr) 47. Nelson RC, Price RD: The Laemobothrion (Mallophaga: Laemobothriidae) of the Falconiformes. J Med Entomol 3:249-257, 1965 48. Clay T: Three new species of Degeeriella N e u m a n n (Mallophaga) from the Falconiformes (Aves). Proc Royal Entomol Soc Lond (B) 27:1-7, 1958 49. Clay T: A new species of Degeeriella N e u m a n n (Mallophaga) from the Falconiformes. Proc Royal Entomol Soc Lond (B) 31:159-162, 1962 50. Emerson KC: A new species of Mallophaga from the barred owl. Entomol News 21:169-172, 1960 51. Smith SA, Smith BJ: Lice in birds of prey. Comp Ailim Pract 2:35-37, 1988 52. Schulz TA, StewartJS, Fowler ME: Knemidokoptes mutans (Acari: Knemidocoptidae)"in a great horned owl (Bubo virginianus). J Wildl Dis 25:430-432, 1989 53. Redig PT: Medical Management of Birds of Prey (ed 3). St. Paul, MN, The Raptor Center, 1993, pp 169-180 54. Redig PT: Summertime disease control: Malaria. Hawk Chalk 32:56-58, 1993 55. Remple JD: Avian malaria with comments on other haemosporidia in large falcons, in Cooper JE, Greenwood AG (eds) : Recent Advances in the study of Raptor Diseases. West Yorkshire, England, Chiron Publications Ltd, 1981, 107-110
The health and survival of both free-living and captive birds of prey can be severely jeopardized by numerous species of parasites, including a diverse variety of protozoans, helminths, and arthropods. Most parasitic infections cause little or no harm to healthy individuals but can become a significant problem for raptors that are stressed by captivity, illness, or injury. Thus, it is important to correctly recognize, diagnose, and control those parasitic species that are capable of resulting in pathological conditions. Copyright 9 1996 by W. B. Saunders Company. Key words: Raptor, parasites, pathology, treatment.
ontinued interest in raptor rehabilitation and the breeding of captive birds of prey has brought concern for their veterinary care to the forefront. The health and vigor of both free-living and captive birds o f prey can be severely compromised by a wide variety of internal and external parasites, including numerous species of protozoans, helminths, and arthropods. 1-5 Most parasitic infections in wild birds of prey usually cause little or no distress to healthy individuals. However, parasites can become a significant health problem for raptors that are held in prolonged captivity in confined housing and for raptors that have recently come into captivity that are stressed by injury, illness, or exposure to the new environment. Thus, it is important to recognize, diagnose, and control those parasitic species that are capable of producing clinical disease in the raptorial host. The purpose of this contribution is to describe the more c o m m o n parasites, discuss their clinical significance, and provide information on their control and treatment.
C
Protozoans A n u m b e r of protozoan blood parasites have been d o c u m e n t e d in birds of prey and include various species of Haemoproteus (Fig 1), Leucocytozoon (Fig 2), and Plasmodium. 6-s These parasites are e n c o u n t e r e d fairly commonly in some wild populations of raptorial birds, although their
importance is not well understood. Transmission of these protozoans is usually via some f o r m of biting arthropod, but there is little information available as to the exact species of vector involved for each specific parasite. Very little pathogenicity has been consistently attributed to many of these h e m o p r o t o z o a n species, but. there are an increasing n u m b e r of accounts suggesting that high parasitemias can have detrimental affects on the health of raptors. Clinical signs include listlessness, weakness, and a n e m i a ) Another protozoan parasite that often has clinical significance in raptors, especially captive falcons and free-living goshawks and owls, 1~ is the flagellate Trichomonas sp, which causes a disease syndrome commonly r e f e r r e d to as "frounce." This protozoan produces raised, yellow, caseous plaques on the tongue and oropharyngeal surfaces. Large lesions often make swallowing difficult for the bird and sometimes results in the raptor being reluctant to feed, which can ultimately lead to starvation. In addition to invading the tissues of the oropharynx, this parasite has also been reported to occur in the anterior portions of the gastrointestinal tract (esophagus, ventriculus, and proventriculus) and disseminated t h r o u g h o u t the parenchyma of the liver of raptors.X x An additional group of protozoan parasites reported from birds of prey includes n u m e r o u s species of intestinal and renal coccidia of the genera Eimeria spp, Caryospora spp, and Frenkelia sp. 12,13 Although no obvious pathology appears to result from coccidia] infections occurring in the kidneys o f raptors, there are several reports
From the Department of Biomedical Sciences and Pathobiology, Virginia-Maryland Regional College of Veterinar~ Medicine, Virginia PolytechnicInstitute and State University, Blacksburg, VA. Address reprint requests to Stephen A. Smith, DVM, PhD, Department of Biomedical Sciences and Pathobiology, VirginiaMaryland Regional Collegeof VeterinaryMedicine, VirginiaPolytechnic Institute and State University, Blacksburg, VA 24061-0442. Copyright9 1996by W. B. Saunders Company. 1055-937X/96/0502-000655.00/0
Seminars in Avian and Exotic Pet Medicine, Vol 5, No 2 (April), 1996: pp 97-105
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Figm'e 1. Hemoproteussp (arrow) in a red blood cell of a Great Horned Owl. W&G stain, bar = 10 urn. of mortality being associated with intestinal infections of coccidia. 12 Clinical signs of intestinal coccidiosis include watery, mucoid, or bloody diarrhea with n u m e r o u s small spherical oocysts. O t h e r protozoan parasites of unknown significance r e p o r t e d f r o m birds of prey include b o t h Sarcocystis sp and Babesia s p . 14
Helminths The helminths (or platyhelminths) can be further subdivided into the nematodes, trematodes, cestodes, a n d acanthocephalans. T h e nematodes r e p r e s e n t the largest group of these internal parasites that infect birds of prey and include ascarids, capillarids, spirurids, a n d tracheal and air sac nematodes. The n e m a t o d e s are
Figure 2. Leucocytozoonsp in an extremely deformed white blood cell of a great horned owl. This hemoprotozoan may also invade red blood cells. W&G stain, bar = 10 urn.
also generally the m o s t potentially p a t h o g e n i c of the c o m m o n raptorial parasites. Most adult nematode species occur mainly in the gastrointestinal tract of the bird, but some may occur in the respiratory, cardiovascular, and ocular systems as well. Ascarids are one of the m o r e c o m m o n n e m a todes occurring in raptors and include species of Ascaridia, Contracaecum, and Porrocaecum.15,16 These are the largest of the nematodes inhabiting the gastrointestinal tract of birds of prey, often measuring 30 to 100 m m in length. Ascarids generally occur in the small intestine, particularly the d u o d e n u m , but may also be found in the proventriculus, ventriculus, and large intestine. In small numbers, these parasites are generally not overtly pathogenic and usually cause only occasional unthriftiness and slight weight loss. However, in large numbers, ascarids may p r o d u c e obvious clinical disease and death. Obstruction of the intestinal tract with large n u m b e r s of ascarids has b e e n described in British Kestrels (Falco tinnunculus), whereas perforation of the small intestine has b e e n r e p o r t e d in two juvenile Great H o r n e d Owls (Bubo virginianus) in which each bird contained m o r e than 120 mature ascarids in the ventriculus and small intestine, several of which had p e r f o r a t e d the intestinal wall and were partially located in the abdominal cavity of the b i r d ) Ascarids may have either a direct or an indirect life cycle involving an a r t h r o p o d paratenic (transport) or intermediate host. Ascarid eggs are of two distinct m o r p h o logical types: one similar to the ovum of the poultry ascarid (Ascaridia galli), and the o t h e r similar to the canine r o u n d w o r m (Toxascaris leonina) (Fig 3).1 Capillaria spp (threadworms) a p p e a r to be the most c o m m o n type of n e m a t o d e parasitizing b o t h captive and free-living birds of prey. Smith 3 r e p o r t e d 54% of the free-living hawks, falcons, and eagles and 78% of the free-living owls examined in that study as being parasitized by CapiUaria spp. Included in this diverse g r o u p of tissue-inhabiting n e m a t o d e s are species that infect the mouth, o r o p h a r y n x , esophagus, crop, small intestine, a n d cecum of raptors. Intestinal infections of CapiUaria spp are usually asymptomatic, but with heavy infections the bird may demonstrate clinical signs of diarrhea, anorexia, emaciation, and listlessness. O t h e r species of capillarids can p r o d u c e significant tissue d a m a g e
Parasites of Birds of Prey
Figure 3. Common nematode eggs found in the mutes of birds of prey. The egg in the upper right is typical of an ascarid (ie, Porrocaecumsp), whereas the middle egg is typical of a capillarid. The pseudoparasite in the lower left is an egg from the mouse urinary bladder nematode (Trich0m0s0ides crassicauda), which is passed unchanged through the digestive tract of the raptor. Bar = 50 um. by burrowing into the mucosa causing varying degrees of inflammation and e d e m a (Fig 4). C o o p e r 17 attributed two cases of " f r o u n c e " (a superficial oropharyngeal disease usually attributed to the p r o t o z o a n Trichomonas sp) in falcons to Capillaria contorta. H e described the presence of a white necrotic exudate and diptheritic m e m b r a n e s in the buccal cavity and p h a r y n x of a Peregrine Falcon (Falco peregrinus) and a RedH e a d e d Merlin (Falco chicquera ruficollis) caused by the mucosal migration of these parasites. A
Figure 4. Histological section demonstrating the tissue migration of CapiUariaspp in the mucosal lining of the esophagus of a Red-Tailed Hawk. Note the typical capillarid egg next to the cross-section of the mature nematode. H&E stain, bar = 50 urn.
99
similar observation was m a d e by Trainer et al is who r e p o r t e d a "caseous growth" in the throat o f two gyrfalcons (Falco rusticolus) to be caused by a CapiUaria sp infection. Clausen and G u d m o n s son, 19 in the examination of the cause of death of gyrfalcons f r o m Iceland, found 36% h a d died as a direct result of an u p p e r alimentary tract infection of C contorta. The eggs of these avian capillarids most closely resemble the ova of trichurids f r o m domestic animals but are often m o r e elongated in shape (Fig 3). In addition to finding the eggs in the mutes (fecal material) of raptors, eggs may also be c o m m o n l y observed in scrapings of suspected lesions in the oral m u c o s a o f the bird. A n u m b e r of species of spirurids, c o m m o n l y called stomach worms, occur in the l u m e n and submucosa of the proventriculus and ventriculus of birds of prey. Habronema sp has b e e n described f r o m the ventriculus of n u m e r o u s species of raptors including hawks, kestrels, eagles, and owls, 20'2I whereas Hatertia sp has been described f r o m the proventriculus of an i m m a t u r e Prairie Falcon (Falco mexicanus). 22 Several species of Microtetrameres have b e e n reported in the proventriculus of the Great H o r n e d Owl, goshawk (Accipiter gentilis) and Golden Eagle (Aquila chrysaetos), ~ Red-Tailed Hawk (Buteo jamaicensis), 3 and Snowy Owl (Nyctea scandiaca), t5 whereas Tetrameres sp has b e e n reported from the Barred Owl (Strix varia). 24 In these later species of stomach worms, the adult female w o r m resides within the l u m e n of the glandular tissue of the proventiculus causing apparently little or no i n f l a m m a t o r y reaction, whereas the male generally inhabits only the lumen of the proventriculus (Fig 5). Ova of these n e m a t o d e parasites are of the typical spirurid type containing an embryonated larvae. An insect paratenic host is probably required for the transmission of this parasite. Tracheobronchial infections with Syngamus sp a n d Cyathostoma sp have been reported in numerous species of raptors, 25,26but their prevalence in free-living raptor populations appears to be very low. These parasites are usually few in n u m b e r but can cause inflammation and sometimes partial or complete obstruction of the trachea, p r o d u c i n g clinical signs of dyspnea and openm o u t h e d breathing. Nematodes of the genus Cyathostoma were r e p o r t e d as the p r i m a r y cause of a fatal parasitic p n e u m o n i a in a free-living Saw-Whet Owl (Aegolius acadicus), two free-living
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Figttre 5. Histological section demonstrating a typical spirurid nematode, Microtetrameres sp, within the lumen of the glands of the proventriculus of a RedTailed Hawk. Note the lack of a host inflammatory response. H&E stain, bar = 50 urn. Screech Owls (Otus asio), and four captive-bred juvenile Burrowing Owls (Speotyto cunicularia).26 Younger birds a n d smaller-sized birds are generally m o r e severely affected than larger adult birds. T h e eggs are large, double-operculate, ellipsoidal ova similar to Syngamus trachea of domestic poultry. A paratenic host, such as an earthworm, is required for the completion of the life cycle. Serratospiculum amaculata is primarily a parasite of falcons but may also occur in o t h e r species of raptors. This elongate n e m a t o d e is often f o u n d coiled in the air sacs, serous m e m b r a n e s
o f the viscera, or in the connective tissue of the abdominal or thoracic cavity of birds. Clinical signs may include respiratory difficulty caused by pathological changes and thickening of the air sacs. S. amaculata has b e e n r e p o r t e d f r o m b o t h Peregrine Falcons and Prairie Falcons, 99,27 the Bald Eagle (Haliaeetus leucocephalus), 21 a n d a Cooper's Hawk (Accipiter cooperii).28 This parasite does not a p p e a r to b e particularly pathogenic in low numbers; however, a n u m b e r of mortalities in prairie falcons as a result of this parasite have b e e n described by both Bigland et al 2s a n d Kocan and Gordon. 29 Ward and Fairchild 22 rep o r t e d several cases of suspected Serratospiculum sp infection in prairie falcons where the air sacs of one dyspneic bird were filled with h u n d r e d s of adult nematodes. Ova are small, thin-shelled eggs that are e m b r y o n a t e d when passed in the mutes of the bird. Because the adult n e m a t o d e s inhabit the air sacs, the ova must be c o u g h e d up and swallowed to insure transmission. In the r e p o r t of the Prairie Falcons where S amaculata was considered the major contributing cause of death, smears of necrotic foci in the liver, spleen, and h e a r t and of necrotic lesions in the crop and esophagus all contained large n u m b e r s of larvated ova and free larvae of this parasite. '~7 Therefore, additional clinical signs of this type of infection may include general unthriftiness and emaciation caused by the invasion and inflammation of the gastrointestinal tract. O t h e r n e m a t o d e s that have b e e n r e p o r t e d in birds of prey include Physaloptera sp in the ventriculus of Red-Tailed Hawks, Sharp-Shinned Hawks (Accipiter striatusi), Cooper's Hawk, and Red-Shouldered Hawks (Buteo lineatus). 3~ In addition, Thelazia sp has b e e n r e p o r t e d in the orbit of the eye of a Swainson's Hawk (Buteo swainsonii), ~2 and filarial n e m a t o d e s have b e e n described f r o m the heart of a Peregrine Falcon. ss A n u m b e r of accounts also describe filarial worms in the blood of various birds of prey, but the clinical significance of these parasites are n o t known. Small n u m b e r s of any of these less c o m m o n parasites have b e e n generally observed as incidental findings at necropsy and have n o t b e e n associated with any significant pathology. T r e m a t o d e parasites, especially strigeid and diplostomatid trematodes, occur c o m m o n l y in birds of prey. 34-s6These helminths generally parasitize the d u o d e n u m and are rarely considered pathogenic even in large numbers. However,
Parasites of Birds of Prey
Dedrick a7 described a fatal clinical syndrome in a Prairie Falcon characterized by p o o r condition and diarrhea associated with a strigeid trematode infection. Likewise, emaciation and ultimately death in a Bald Eagle f r o m a massive trematode infection has b e e n reported, and Greenwood et aP 8 concluded that the death o f a Saker Falcon (Falco cherrug) was caused by severe intestinal trematodiasis. In addition to the strigeid and diplostomatid trematodes, several species of dicrocoelid trematodes have been r e p o r t e d in raptors, especially f r o m the liver and bile ducts of the American Kestrel (Falco sparverius). An unidentified species of t r e m a t o d e has also been observed in the bile ducts of a 6-week-old freeliving screech owl. 3 Although rarely diagnosed by fecal examination, these liver a n d bile duct trematodes p r o d u c e an ovum that is similar to but smaller than the typical t r e m a t o d e ovum and may often be asymmetrical with a distinct protuberance at one end. 1 Cestodes are generally u n c o m m o n in birds of prey and when observed are considered to be relatively nonpathogenic. These parasites are usually located in the small intestine with their scolices firmly e m b e d d e d in the intestinal mucosa. Small n u m b e r s of tapeworms are generally well-tolerated by healthy individuals, whereas clinical signs of a heavy cestode infection are often nonspecific a n d range f r o m no obvious clinical signs to mild diarrhea and weakness. Rarely do cestodes occur in large e n o u g h numbers to cause intestinal obstruction or death of the bird. Some of the m o r e c o m m o n genera of cestodes occurring in birds of prey include Taenia, Cladotenia, Choanotaenia, Paruterina, and Paradilepis, all of which have a typical taenioid type of o v a . 39"44 In addition to fecal analysis, diagnosis of a cestode infection can often be m a d e by observing the small light-colored proglottids a r o u n d the vent or in the mutes of the bird. Infections with acanthocephalans, c o m m o n l y called T h o r n y - H e a d e d Worms, in birds of prey are relatively rare, with the notable exception of one survey in which 57% of the free-living Falconiformes and 60% of the free-living Strigiformes e x a m i n e d in Louisiana were infected. 45 These parasites are generally f o u n d in the distal small intestine of the bird with the proboscis firmly e m b e d d e d in the intestinal mucosa. Kocan and Locke 2a r e p o r t e d 7% of necropsied bald
101
eagles were infected with acanthocephalans, and Kollias et a146 f o u n d 29% of various species of raptors were infected. These parasites usually cause minimal pathology other than a localized i n f l a m m a t o r y response at the site of attachment. However, in extremely heavy infections, the parasites may actually penetrate the intestinal wall and cause a generalized peritonitis resulting in the death of the raptor.
Arthropods Birds of prey may h a r b o r a wide variety of external a r t h r o p o d parasites, including numerous species of lice, a few species of H i p p o b o s c i d Flies, and occasional species of fleas, mites, and ticks. Similar to the helminths, most adult birds of prey can normally a c c o m m o d a t e small numbers of these parasites without any noticeable harmful effects. However, when a bird is debilitated, cannot p r e e n properly, or is placed in a very confined enclosure, the n u m b e r s o f these parasites may rapidly multiply to levels that further stress or complicate any preexisting condition. Lice that occur on raptors, as with all avian species, are biting or chewing lice belonging to the order MaUophaga. A large n u m b e r o f species have b e e n described from birds of prey, m o s t belonging to the genera Laemobothrion, Degeeriella, Falcolipeurus, and Kurodaia. 475~Most of the r e p o r t e d species are fairly host specific. Like o t h e r species o f chewing lice, these ectoparasites spend their entire life cycle on the bird of prey and can generally only survive a short time off the host. Eggs are generally firmly attached in clusters at the base of the shafts of body or tail feathers. Transmission is generally by direct contact with a n o t h e r suitable avian host a n d has b e e n r e p o r t e d to occur during mating, feeding of young, or during c o m m u n a l roosting of b!rds. Most birds of prey normally h a r b o r a small n u m b e r o f lice without any detrimental effect, however, large infestations of lice can cause increased restlessness, loss of sleep, increased p r e e n i n g activity, and decreased appetite. As a result of the irritation caused by the activity of the lice, the condition of the feathers may rapidly deteriorate because of excessive preening, scratching, and sometimes even feather plucking. 51 Feathers may eventually b e c o m e so
Stephen A. Smith
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weakened by excessive p r e e n i n g that they become highly susceptible to breakage. Hippoboscid Flies are fairly c o m m o n on birds of prey. These ectoparasites, being related to sheep keds but having wings, are rarely observed unless they crawl or fly off during handling of the bird (Fig 6). Hippoboscids are generally nonpathogenic to the raptorial host, but may be involved in the transmission of some of the blood-borne p r o t o z o a n parasites such as Haemoproteus. Myiasis, caused by other species of flies such as Calliphora spp and Protocaliphora spp, is generally only a p r o b l e m for eyesses (nestling raptors), but infestations will occasionally be observed in birds of prey secondary to chronic, o p e n traumatic injuries. 1,2 A variety of fleas, mites, ticks, and flies occur infrequently on birds of prey. Most of these external parasites are generally nest dwellers, and are, therefore, m o r e c o m m o n on eyesses and in nesting material. Large numbers of mites and larval ticks may cause severe irritation for the raptor and can result in excessive p r e e n i n g activity and feather damage. Infestations of Ornithodoros aquilae on a Prairie Falcon, Ptilonyssid Mites on American Kestrels, and Domestic Poultry Mites (Dermanyssus gaUinae and Ornithodoros sylviarum) on various species of captive raptors have all b e e n d o c u m e n t e d . 2 An unusual occurrence of tile Scaly-Leg Mite (Knemidokoptes mutans) also has b e e n reported f r o m the G r e a t H o r n e d Owl, the Snowy Owl, and accipiters. 2,52 In the case of the Great H o r n e d Owl, the
2: "22
Figure 6. This common type of Winged Hippoboscid Fly is frequently found crawling between the feathers on birds of prey. The ectoparasite is generally nonpathogenic but may be involved in the transmission of avian hemoprotozoans. Bar = 10 ram.
infestation caused bilateral foot lesions characterized by severe proliferative papillary hyperkeratosis with m o d e r a t e soft-tissue swelling. Black flies (Simulium sp) have b e e n r e p o r t e d infesting nestling raptors a n d may be i m p o r t a n t in b o t h the production of anemic conditions in the birds and in the transmission of the hemosporidian, Leucocytozoon sp. Simuliid flies also have b e e n r e p o r t e d infesting adult kestrels and Red-Tailed Hawks, but the clinical significance of these infestations is not known. In addition, ectoparasites from prey items will occasionally transfer to the raptor while the bird is feeding, but these t e m p o r a r y migrants usually do not survive long on the new host and generally do not pose a threat to the health of the raptor.
Pseudoparasites Finally, it is i m p o r t a n t to r e m e m b e r that examination of the mutes of a bird of prey will often demonstrate parasite ova that do not actually originate f r o m an infection of the bird. Eggs of parasitic mites also are often observed during routine fecal examination of raptors. It is ass u m e d that these mite eggs are swallowed by the bird during n o r m a l p r e e n i n g activity or represent contamination of the mutes from the cloacal area. Nevertheless, the discovery of mite eggs during a fecal examination is an indication that the bird should be examined for the possibility of a mite infestation. A n o t h e r example o f a pseudoparasitism involves the ability of parasite ova of prey that has b e e n eaten by a bird of prey to be passed u n c h a n g e d through the bird's digestive system. Both free-living birds that eat parasitized wild-caught prey items, as well as captive birds that are fed c o n t a m i n a t e d food items such as road kills, trapped animals, or parasitized laboratory-raised animals can be so affected. Eggs of Trichosomoides crassicauda, a c o m m o n n e m a t o d e parasite of the urinary bladder of laboratory-reared rodents, are sometimes observed during fecal examination of captive raptors fed laboratory rats (Fig 3).3 O n e way of d e t e r m i n i n g the original source of an u n k n o w n parasite egg in the mutes of a raptor is to r e p e a t the fecal examination in 2 to 3 days. If the egg originated f r o m a prey item, the egg should no longer be f o u n d in the fecal material assuming the contaminated diet of the bird has b e e n controlled or eliminated; whereas if the egg
Parasites of Birds of Prey
originated f r o m parasites o f the bird o f prey it will m o s t likely be p r e s e n t in s u b s e q u e n t fecal examinations.
Control and Treatment A variety o f anthelmintics a n d insecticides have b e e n r e p o r t e d for the removal o f internal a n d external parasites f r o m birds o f prey. ~'5~ However, because very little specific research has b e e n c o n d u c t e d o n the use a n d efficacy o f these chemicals in raptors (ie, the majority o f dosage regimens b e i n g extrapolated f r o m n o n r a p t o r i a l species a n d sometimes even n o n a v i a n species), caution s h o u l d always be exercised w h e n considering their usage. As with any animal, the physical c o n d i t i o n a n d health o f the bird o f prey m u s t be carefully c o n s i d e r e d before initiation o f treatment. In addition, e x t r e m e caution s h o u l d be used w h e n treating a sick, debilitated o r stressed bird as well as juvenile birds o f prey. Most n e m a t o d e s can be safely treated with any o n e o f a variety o f anthelmintics (Table 1). Ascarids in birds o f prey have b e e n successfully treated with piperazine, levamisote, thibendazole, mebendazole, a n d ivermectin. Both thiabendazole a n d levamisole have b e e n r e p o r t e d as b e i n g effective against Capillaria spp, b u t a seco n d administration o f anthelmintic 7 to 10 days after the initial t r e a t m e n t is often necessary to completely eliminate the infection. Two treatm e n t s o f ivermectin administered 3 to 4 weeks apart has b e e n used successfully to treat capillarid infections in raptors. 46 F e n b e n d a z o l e has also b e e n r e p o r t e d as being effective in eliminating b o t h capillarids a n d ascarids f r o m birds o f prey. M e b e n d a z o l e has b e e n suggested as a t r e a t m e n t for Microtetrameres sp a n d o t h e r spirurid n e m a t o d e s in raptors since it has b e e n used successfully to c o n t r o l s t o m a c h w o r m infections in o t h e r species of birds. Infections o f Serratospiculum amaculata have b e e n effectively treated with either t h i a b e n d a z o l e or levamisole, a n d infections o f Syngamus sp have b e e n treated with either t h i a b e n d a z o l e or m e b e n d a z o l e . A l t h o u g h most anthelmintics a p p e a r to be relatively safe a n d effective against the m o s t c o m m o n n e m a todes in raptors, it appears that f e n b e n d a z o l e , levamisole, o r ivermectin work best in raptors, a l t h o u g h levamisole may be slightly m o r e efficacious in the t r e a t m e n t o f ascarids. T h e anthelmintic s h o u l d be administered orally to the bird a n d
103
Table 1. Recommended Antiparasiticals for Treating Endoparasites in Birds of Prey 3,53
Antiparasitical Agent
Dosage
Recommended Usage
Chloroquine/ Drug combi- Treat avian malaria Primaquine nation of 25 with initial dose of treamaent mg/kg/0.75 25 mg/kg chloromg/kg for quine and 0.75 initial dose, mg/kg primaquine then three PO, then three doses of 15 additional doses of mg/kg of 15 mg/kg chlorochloroquine PO only at quine only 12, 24, and 48 h. Fenbendazole 25 mg/kg PO Treat for 3 consecutive days.. 30-50 mg/kg Treat only once at this PO dosage. Ivermectin 0.2 mg/kg PO Dilute ivermectin or IM (Ivomec; Merck Sharp & Dohme, Rahway, NJ) 1:9 with water and use 0.2 rnl/kg. Repeat treatment in 34 weeks,
Levamisole Mebendazole
10-20 mg/kg PO 50 mg/kg PO
Metronidazole 30-65 mg/kg PO Piperazine Praziquantel Sulfadimethoxine
Thiabendazole
100 mg/kg PO 50 mg/kg PO or SQ 55 mg/kg PO
100 mg/kg PO
Treat for 2 consecutive days. Repeat in 10-14 days if necessary. Treat once daily for 5-7 days as necessary for trichmoniasis. Repeat in 7-10 days if necessary. Use for cestodes and trematodes. Treat one time at 55 mg/kg, then reduce dose to 25 mg/kg daily as needed for coccidia. Repeat in 10-14 days if necessary.
Abbreviations: PO, by month; IM, intramuscularly; SO.~subcutaneously. NOTE. Remember that caution must be used when treating debilitated, sick, or juvenile birds of prey. Treatment should be initiated when there is little food in the stomach of the bird. the t r e a t m e n t r e p e a t e d if necessary at the p r o p e r time interval. Anthelmintics s h o u l d be administered w h e n there is little or no f o o d in the c r o p or s t o m a c h o f the bird to decrease the a m o u n t o f d r u g inactivation a n d to r e d u c e the possibility o f v o m i t i o n or regurgitation by the bird. Because b o t h t r e m a t o d e s a n d cestodes rarely cause clinical disease in free-living birds o f prey,
Stephen A. Smith
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t r e a t m e n t o f i n f e c t e d raptors may be m o r e palliative t h a n necessary. However, since severe o r fatal i n f e c t i o n s d o occasionally o c c u r in captive, ill, or stressed birds, G r e e n w o o d et a145 have s u g g e s t e d that the t r e a t m e n t of i n t e s t i n a l t r e m a t o d i a s i s i n these birds may b e i n d i c a t e d . Both t r e m a t o d e s a n d cestodes have b e e n effectively a n d safely t r e a t e d with p r a z i q u a n t e l . U n f o r t u n a t e l y , t h e r e is n o k n o w n effective t r e a t m e n t for a c a n t h o c e p h a lan parasites i n b i r d s at the p r e s e n t time. T r e a t m e n t for clinical cases of avian m a l a r i a with q u i n a c r i n e h y d r o c h l o r i d e or c h o r l o q u i n e p h o s p h a t e have b e e n r e p o r t e d as e f f e c t i v e ) I n a d d i t i o n , b o t h R e d i g 53,~4 a n d R e m p l e 55 p r o v i d e extensive i n f o r m a t i o n o n the parasite, diagnosis, a n d various t r e a t m e n t a n d p r o p h y l a t i c p r o t o c o l s u s i n g a c h o r o q u i n e - p r i m i q u i n e c o m b i n a t i o n for m a l a r i a in raptors. Successful t r e a t m e n t o f a Trichomonas sp i n f e c t i o n c a n b e rapidly a c c o m p l i s h e d with m e t r o n i d o z o l e as l o n g as the lesions are n o t too extensive a n d have n o t i n v a d e d the palate. Raptors t r e a t e d with sulfa d r u g s for intestinal coccidiosis d e m o n s t r a t e d clinical i m p r o v e m e n t after 5 to 7 days of therapy. 1 T r e a t m e n t o f e x t e r n a l parasites o n birds o f prey c a n be successfully a c c o m p l i s h e d with a n u m b e r of c o m m e r c i a l l y available insecticides. 51 T r e a t m e n t with volatile substances, such as chlor o f o r m o r ether, are n o t r e c o m m e n d e d since their use is c o n s i d e r a b l y m o r e h a z a r d o u s to b o t h the b i r d a n d applicator. A louse, mite, o r tick i n f e s t a t i o n s h o u l d b e t r e a t e d with a n insecticidal dust or powder, these chemicals b e i n g the simplest a n d safest c o m p o u n d s to use (Table 2). A light d u s t i n g of a n y of these chemicals is fairly easy to apply to t h e b i r d a n d work i n a m o n g the feathers a n d i n d u c e s a m i n i m a l a m o u n t of stress f r o m h a n d l i n g o f the bird. T r e a t m e n t s h o u l d i n c l u d e a n y visibly affected b i r d a n d all o t h e r s i n
Table 2. Antiparasiticals Commonly Used for Treating Ectoparasites on Birds of Prey51 Antiparasitical Agent
Dosage
Carbaryl
0.5%
Malathion Pyrethrin
RecommendedUsage
Lightly dust bird, repeat in 10 to 14 days 5.0% Lightly dust bird, repeat in 10 to 14 days 0.5-2.0% Lightly dust bird, repeatin 10 to 14 days
NOTE. Caution nmst be used when treating stressed, sick or juvenile birds of prey.
close association with the i n f e s t e d bird. B e c a u s e a r t h r o p o d eggs are g e n e r a l l y resistant to m o s t insecticides, all b i r d s s h o u l d be r e t r e a t e d i n 10 to 14 days to kill a n y newly h a t c h e d individuals, regardless o f the ectoparasite involved o r the insecticide c h o s e n . As with the a n t h e l m i n t i c s , extreme caution should be used when treating a sick or d e b i l i t a t e d raptor. I n eyesses a n d j u v e n i l e birds o f prey, it is o f t e n p r e f e r a b l e to r e m o v e a n y ectoparasites by h a n d a n d avoid a p o t e n t i a l l y lethal insecticide e x p o s u r e .
References 1. Ward FP: Parasites and their treatment in birds of prey, in Fowler ME (ed): Zoo and Wild Animal Medicine (ed 2). Philadelphia, PA, Saunders, 1986, pp 425-430 2. Cooper JE: Veterinary Aspects of Captive Birds of Prey (ed 2). Gloucestershire, England, Standfast Press, 1985, pp 82-96 3. Smith SA: Diagnosis and treatment of helminths in birds of prey, in Redig PT, CooperJE, RempleJD, et al (eds): Raptor Biomedicine. Minneapolis, MN, University of Minnesota Press, 1993, pp 21-27 4. Taft SJ, Snchow K, VanHorn M: Helminths of some Minnesota and Wisconsin raptors. J Helminthol Soc Wash 60:260-263, 1993 5. KinsellaJM, Foster GW, Forrester DJ: Parasitic helminths of six species of hawks and falcons in Florida. J Raptor Res 29:117-122, 1995 6. Stabler RM, Holt PA: Hematozoa from Colorado birds. II. Falconiformes and Strigiformes. J Parasitol 51:927928, 1965 7. Pierce MA, Cooper JE: Haematozoa of birds of prey in Great Britain. Vet Rec 100:493, 1977 8. Greiner EC, Kocan AA: Leucocytozoon (Haemosporidia: Leucocytozoidae) of the Falconiformes. Can J Zool 55:761-770, 1977 9. Kingston N, RempleJD, Burnham W, et al: Malaria in a captive-produced F1 gyrfalcon and in two F1 peregrine falcons.J Wildl Dis 12:562-565, 1976 10. Jessup DA: Trichomoniasis in great horned owls. Mod Vet Prac 61:601-604, 1980 11. Pokras MA, Wheeldon EB, Sedgwick CJ: Trichomoniasis in owls:Report on a number of clinical cases and a survey of the literature, in Cooper JE, Greenwood AG (eds): Recent Advances in the Study of Raptor Disease. West Yorkshire, England, Chiron Publications Ltd, 1981, pp 107-110 12. MatheyWJ: Isospora buteonis Henry 1932 in an American kestrel (Falco sparve~ius) and a golden eagle (Aquila chrysaetos). Bull Wildl Dis Assoc 2:20, 1966 13. Cawthorn RJ: Cyst-forming coccidia of raptors: Significant pathogens of not?, in Redig PT, CooperJE, Remple JD, et al (eds): Raptor Biomedicine. Minneapolis, MN, Universityof Minnesota Press, 1993, pp 14-20 14. Lindsay DS, Blagburn BL: Caryospora uptoni and Frenkelia sp.-like coccidial infections in red-tailed hawks (Buteo borealis).J Wildl Dis 25:407-409, 1989
Parasites of Birds of Prey
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