Corvidae) Birds by Helminths in Spain

PARASITATION OF FALCONIFORM, STRIGIFORM AND PASSERIFORM (CORVIDAE) BIRDS BY HELMINTHS IN SPAIN

M.P. ILLESCAS GOMEZI, M. RODRIGUEZOSORI01 & F. ARANDA MAZA2 Ilnstituio de Parasirologfa «Lopez-Neyra», Consejo Superior de Investigaciones Cientificas (CS.I.C), Cl Ventanilla 11, 18001 Granada, Spain 2Agencia Ambiental (AMA), Granada, Spain

Received 20 November 1991; accepted 9 June 1992

REFERENCE: ILLESCASGOMEZ (M.P.), RODRIGUEZOSORIO (M.) & ARANDAMAZA (F.), 1993.- Parasitation of Falconiform, Strigiform and Passeriform (Corvidae) birds by helminths in Spain. Research and Reviews in Parasitology, 53 (3-4): 129-135. ABSTRACT:The health status of raptors and Passeriformes (Corvidae) by post-mortem examination of 125 birds, of which 57 belonged to the Order Passeriformes (Corvidae), 28 to the Order Strigiformes and 40 to the Order Falconiformes, was studied. Sixty percent of the hosts were infested with helminths,Passeriformes (Corvidae) being the most frequently parasitized (66,6%), followed by Strigiformes (64,3%) and Falconiformes (47,50/0). The different helminths and hosts are identified and location of the parasites noted. KEYWORDS: Parasitation, helminths, Falconiformes, Strigiformes, Passeriformes (Corvidae), Spain.

INTRODUCTION MATERIAL AND METHODS

Between 1985 and 1988 we studied 125 birds kept at the Center The study of birds of prey is one of the basic pillars for the Recovery of Raptors by the Granada-Almeria Environmen- of current environmental protection policies in developed tal Agency, and remitted post-mortem to the laboratory. Of these countries. All studies which provide information on their birds, 57 belonged to the Order Passeriformes (Corvidae), 28 to the biology, and on factors which affect their health, are of Order Strigiformes and 40 to the Order Falconiformes. prime importance in achieving an adequate ecological All birds were identified (PETERSON, Mou TFORT & HOlLO , balance; given the role raptors play in the food chain, 1980) and dissected in our laboratory, and gross lesions possibly caused by parasites were searched for macroscopically, paying particular change in their health status can have significant effects. attention to the air sacs and peritoneal cavity. The digestive tract Very little research has dealt with the parasitic fauna and viscera were then examined under binocular microscope. All in raptors and Passeriformes (Corvidae) (SEURAT, 1916; parasites found were identified according to conventional methods DOLLFUS, 1961; JAROS, VALENTA & ZAJlCEK, 1966; for the study of helminths. BARUS, 1966; BERNARD, 1969; WARD & FAIRCHILD, The research of trichinosis was only carried out in birds belong- 1972; KOBYSHEN, MARKOY &RYZHIKOY, 1973), and few ing to Falconiformes and Strigiformes. Trichinella spp. were studied using two techniques: a) microscopic examination of the diaphragm: studies have examined the diseases caused by helminths one 0,5 g segment of diaphragm per host was placed between glass in these hosts (KEYMER, 1972; COOPER, 1972; GREEN- plates in a trichinoscope and observed under low magnification; b) WOOD, 1977; WARD, 1979; COOPER & GREENWOOD, artificial pepsin digestion: according to the method of SUlZER 1981), owing in part to the problems involved in working (I965), the entire sediment was examined using 2,5 g of diaphragm. with protected species. In Spain, research on the parasitic fauna in raptors and Passeriformes (Corvidae) has been limited to descriptions RESULlS and reports of certain parasite species (LOPEZ-NEYRA, 1947; JIMENEZ MILLAN, 1961; VERICAD & SANCHEZ A total of 25 different host species were studied, in- ACEDO, 1973; MARTINEZ GOMEZ, HERNANDEZ cluding 4 Passeriformes (Corvidae), 5 Strigiformes and RODRIGUEZ & CALERO CARRETERO, 1974; JIMENEZ 16 Falconiformes. Helminthic parasites were found in all MILLAN & LOPEZ CABALLERO, 1975; GUTIERREZ et al., specimens except for Accipiter gentilis, Aqui/a crysaetus, 1982). Hieratus fasciatus, Circus pigargus, Circus cyaneus and In trichinosis studies only Trichinella pseudospiralis has Falco neumani, all members of the family Falconiformes been reported in bird raptors (ZIMMERMAN, 1969; HUB- (Table 1). BARD, 1969; NIPHADKAK, 1973; CALERO et al., 1978; Sixty per cent of the hosts studied were infested with SHAIKENOY, 1980; WHEELDON, 1983). helminths. The most common parasites belonged to the As part of a long-term programme carried out in col- Class Nematoda (42,40,70), followed by Class Cestoda laboration with the Granada-Almeria Environmental (14,4%), Class Acanthocephala (10,4%) and Class Agency, we investigated parasitation in a number of dif- Trematoda (9,6%). The highest rate of parasitization was ferent raptors and omnivorous Passeriformes. found in Passeriformes (Corvidae) (66,6%), followed by 130 M.P. ILLESCAS GOMEZ, M. RODRIGUEZ OSORIO & F. ARANDA MAZA

Strigiformes (64,3070) and Falconiformes (47,5070) DISCUSSION (Table 2). Examination for Trichinella spp. in all hosts, both by Little is known of the pathogenicity of helminth microscopic observation of the diaphragm and by ar- parasites in birds of prey. This may be due in part to the tificial pepsin digestion, failed to detect any parasites of fact that raptors are usually protected species. this genus. From a parasitological viewpoint, as noted in the results A total of 32 different helminth species was identified, section, our findings constitute the first report for the of which 4 belonged to the Class Cestoda, 1 to Trematoda, world of one host, the first for Spain of 11 hosts, and 4 to Acanthocephala and 23 to Nematoda. Table 3 gives the first report of parasitation in Spain by 10 helminth the taxonomic framing, the names of the hosts and species. parasites and the location of the latter. On the basis of research by KEYMER(1972) and WARD Table 4 lists new host species for the world, new host (1979), our findings provide evidence of the possible records for Spain and first findings of given helminth pathogenicity of some parasites. Infestation of the species for Spain (comparisons were respectively made digestive tract by species of Cestoda, Nematoda, with records appeared in the Helminthological Abstracts Trematoda or Acanthocephala (Table 3), which occurs and in the review of CORDERODELCAMPILLO et al., when very large numbers of parasites are present, leads ~980). ,J .: to intestinal oelusion, with harmful consequences for the bird's health. Serratospicu/um chungi is the causal agent of Ser- ratospiculiasis, and like Hamatospicu/um pauloi and Hosts No. Prevalence Dip/otriaena sp. inhabits the air sacs, where these parasites examined usually cause mild disease. When present in large numbers, however, they may cause more serious illness Corvus corax 3 2 (66,60/0) Passeriformes characterized by respiratory distress, vomiting and occa- (Corvidae) Corvus monedu/a 39 23 (58,9%) Garru/us g/andarius 8 7 (85,7%) sionally death. The parasites frequently perforate the air Pica pica 7 6 (85,7%) sac wall and reach the thoracic cavity. Strigiformes Tyto alba 10 5 (50,0%) Capillariasis, caused by species of the genus Capillaria, Bubo bubo 2 2 (100,0%) is an important cause of death in the avian orders studied. Athene noctua 13 8 (61,6%) Some species are located in the oesophagus, e.g. Capi//aria Asio f/amens I I (lOO,O%) dispar and Capillaria sp. Other members inhabit the in- Asio otus 2 2 (lOO,O%) Falconiformes Accipiter gentilis 3 - testine, e.g. Capillaria fa/conis and Capi//aria corvorum, Aquila he/iaca 2 I (50,0%) causing anorexia, bloody diarrhea, vomiting, and at times Aquila crysaetus I - death. Buteo buteo 8 5 (62,5%) The study of the bird raptors as hosts of Trichine//a Milvus milvus 2 2 (100,0%) sp. is important since, according to BOEV, BRITOV& Milvus nigrans I (lOO,O%) I ORLOV(1979), the maintenance of Trichinella in nature Hieratus pennatus 3 I (33,3%) Hieratus fasciatus I - depends on these raptors. Circus cyaneus 2 - Unfortunately, no statistical analysis of the results was Circus pigargus 2 - possible owing to-the low numbers of specimens of each Pernis apivorus 2 2 (100,0%) species examined, hence no attempt was made to calculate Falco subbuteo I I (100,0%) percentage of parasitization or density of parasites. Fa/co tinnuncu/us 3 (60,0%) 5 However, despite these significant limitations, our findings Falco peregrinus 4 2 (50,0%) Falco neumani 2 - hold interest inasmuch as we provide information on the Falco e/eonorae I I (lOO,O%) state of health of many avian species. We report a elear prevalence of helminth parasitization, as well as the wide Table 1.- Hosts examined and parasitized. variety of other parasites found. Earlier studies suggest

Passeriformes Strigiformes Falconiformes Total

No. hosts 57 28 40 125 No. parasitized 38 (66,6%) 18 (64,5%) 19 (47,5%) 75 (60,0%) by Nematodes 22 (38,5%) 17 (64,3%) 14 (35,0%) 53 (42,4%) Cestodes 18 (31,6%) 18 (l4,4%) Trematodes ,9 (15,8%) I (3,6%) 2 (5,0%) 12 (9,6%) Acanthocephala .,4 (7,0%) 3 (10,7%) 6 (15,0%) 13 (10,4%)

Table 2.- Parasitation by helminths in Passeriforrnes (Corvidae),Strigiformes and Falconiformes in Spain. Helminths of birds in Spain 131

Species Host Location References

CESTODES

Raillietina (R.) sartica C. corax Intest. SKRJABIN (1914) JOYEUX & TIMoN-DAvID (1934) Y AMAGUTI (1959)

Anomotaenia contricta C. monedula lntest. COHN (1901) JOYEUX & BAER (1936) METTRICK(1958) SPASSKAYA (1966)

Passerilepis stylosa P. pica lntest. JOYEUX & BAER (1936) LOPEZ-NEYRA (1942) METTRICK(1958) SPASSKAYA (1966) GABRION (1977)

Variolepis farciminosa G. glandarius lntest. KRABBE (1869) Y AMAGUTI (1940) LOPEZ-NEYRA (l947b) METTRICK (1958) SPASSKAYA (1966) STOIME OV, K'OSEV & BOVER (1976)

TREMATODES

Strigea falconis A. heliaca lntest. HARWOOD (1931) Y AMAGUT!(1958) MARTI EZ GOMEZ, HER ANDEZ RODRIGUEZ & CALERO CARRETERO (1974)

ACANTOCEPHALA

Mediorhynchus sp. G. glandarius lntest. YAMAGUTI(1963) DIAz COSIN (1970) DIAz COSIN (1971) STOIMENOV, K'OSEV & BOVER (1976) Centr. globocaudatus F tinnunculus Intest. LOPEZ-NEYRA (1947b) Y AMAGUTI (1963) DIAz COSI(1970) MART! EZ GOMEZ, HERNANDEZ RODRIGUEZ & CALERO CARRETERO (1974)

Centr. aluconis B. buteo lntest. LOPEZ-NEYRA (1947b) YAMAGUTI(1963)

Centrorhynchus sp. T. alba lntest. YAMAGUTI (1963) A. noctua WARD (1964)

NEMATODES

Capillaria falconis B. bubo lntest. READ (1949) A. otus LOPEZ-NEYRA (1947a) BARUS (1964) BARUS (1966)

Capillaria dispar B. buteo Oesoph. LOPEZ-NEYRA (1946) LOPEZ-NEYRA (1947a)

Capillaria corvorum C. monedula Intest. LOPEZ-NEYRA (1947a) P. pica JIMENEZ MILLAN (1961) WAKELlN (1967)

Capillaria sp. C. corax Oesoph. WAKELlN (1967) M. milvus BARUS & GARRIDO (1968)

Synhimantus affinis T. alba Oesoph. SEURAT (1916) CRAM (1927) LOPEZ-NEYRA (l947b)

Synhimanthus laticeps B. bubo Stom. SEURAT (1916) A. otus CRAM (1927) F tinnunculus 132 M.P. ILLESCAS GOMEZ, M. RODRIGUEZ OSORIO & F. ARANDA MAZA

Species Host Location References

Dispharynx nasuta A. noctua Provent. RASHEED (1960) FREITAS & SILVA (1960) BARUS (1966) JEHAN (1972)

Acuaria anthuris G. glandarius Provent. DOLLFUS et al.(1961) OSHMARIN (1963)

Cheilospirura gruveli G. glandarius C. tis. Y AMAGUTI(1961) CHABAUD, A DERSON & WILLMOTT (1975)

Habronema spinosa B. bubo Oesoph. GENDRE (1922) LOPEZ- EYRA (1947b) CHABAUD (1958) All (1961) MAWSON (1968)

Habronema mansoni B. buteo Stom. SEURAT (1914) GENDRE (1922) CRAM (1927) All (1961) MAWSON (1968)

Habronema leptoptera F. subbuteo Stom. GENDRE (1922) CRAM (1927) LOPEZ-NEYRA (l947b) CHABAUD (1958) All (1961) MAWSON (1968)

Microtetrameres sp. A. noctua lntest. CRAM (1927) Y AMAGUTI (1961) YORKE & MAPLESTONE (1962) OSHMARIN (1963)

Serratospiculum chungi F. peregrinus Air sac HOEPPLI & Hsu (1929) WEHR (1938) LOPEZ-NEYRA (1956) SONIN (1975)

Hamatospiculum pauloi T. alba Air sac CHABAUD, ANDERSON & WILLMOTT (1975) OLlVEIRA RODRIGUEZ & SOUZA FRA co (1964)

Diplotriaena sp. P. pica Air sac LOPEZ-NEYRA (1956) SONIN (1975)

SplendidoJilaria sp. G. glandarius Oesoph. YAMAGUTI (1961) JIMENEZ MILLAN & LOPEZ CABALLERO (1975)

Physaloptera apivori P. apivorus Stom. SEURAT(1914) SCHULTZ (1927) DESPORTES (1947) YAMAGUTI(1961)

Physaloptera alata F. eleonorae Oesoph. SEURAT (1914) LOPEZ-NEYRA (1947b) VERICAD & SANCHEZ ACEDO (1975) MICHALEK (1984)

Physaloptera sp. H. pennatus Oesoph. SEURAT (1914)

Subulura bolivari A. noctua Intest. LOPEZ-NEYRA (1922)

Porrocaecum sp. F. peregrinus Intest. LOPEZ-NEYRA (l947b) C. monedula ANADON (1954) BARUS (1966)

Porrocaecum angusticolle M. milvus Intest. CRAM (1927) M. nigrans Y AMAGUTI(1961) BARUS (1966)

Table 3.- Helminths, parasites, hosts and location. Helminths of birds in Spain 133

NEW HOSTS FOR THE WORLD HOST HELMINTH SPECIES Corvus corax Raillietina (R.) sartica

NEWHOSTS FOR SPAIN HOSTS HELMINTH SPECIES Corvus monedula Anomotaenia contricta Asio otus Synhimanthus laticeps Falco tinnunculus Synhimanthus laticeps Falco subbuteo Habronema letoptera Falco eleonorae Physaloptera alata Falco peregrinus Porrocaecum sp. Milvus milvus Porrocaecum angusticolle Milvus nigrans Porrocaecum angusticolle Garrulus glandarius Splendidofilaria sp. Hieratus pen natus Physaloptera sp. Falco tinnunculus Centrorhynchus globocaudatus

NEW HELMINTH SPECIES FOR SPAIN Capillaria falconis Capillaria dispar Dispharynx nasuta Habronema mansoni Microtetrameres sp, Serratospiculum chungi Hamatospiculum pauloi Diplotriaena sp. Physaloptera apivorus Acuaria anthuris

Table 4.- New reports of helminth parasites.

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