Two new species of Caryospora Léger, 1904 (Apicomplexa, Eimeriidae) from accipitrid raptors

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Systematic Parasitology 46: 23–27, 2000. © 2000 Kluwer Academic Publishers. Printed in the Netherlands.

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Two new species of Caryospora L´eger, 1904 (Apicomplexa, Eimeriidae) from accipitrid raptors Jiˇr´ı Volf1 , Bˇretislav Koudela2 & David Modr´y1,2 1 Department of Parasitology, University

of Veterinary and Pharmaceutical Sciences Brno,Palack´eho 1/3, CZ - 612 42, Brno, Czech Republic 2 Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovsk´ ˇ e a 31, CZ-370 05, Cesk´ Budˇejovice, Czech Republic Accepted for publication 26th March, 1999

Abstract Two new species of Coccidia (Apicomplexa: Eimeriidae) are described from European accipitrid raptors (Falconiformes: Accipitridae). Oöcysts of Caryospora aquilae n. sp. found in faeces of the gold eagle Aquila chrysaetos are subspherical to broad ellipsoidal and measure 43 (40–49) × 37.5 (34–39) µm. Polar granule, oöcyst residuum and micropyle are absent. Each oöcyst contains one spherical to subspherical slightly polygonal sporocyst measuring 23.8 (23–25) × 23.3 (22–25) µm. Stieda and substieda bodies are absent. The sporocyst residuum is composed of numerous small granules less than 0.5 µm in diameter dispersed randomly among the sporozoites. Sporulated oöcysts of Caryospora circi n. sp. from faeces of the marsh harrier Circus aeruginosus are widely oval, measuring 24.5 (23–25) × 21.8 (21–24) µm. A polar granule, oöcyst residuum and micropyle are absent. Each oöcyst contains one spherical to subspherical sporocyst measuring 16.2 (15–17) × 15.6 (15–17) µm. A compact granular, spherical to subspherical sporocyst residuum, 10.4 (10–11) × 8.5 (7–9), was present in 76% of measured sporocysts. In 24% of sporocysts the granules of sporocyst residuum were scattered among the sporozoites.

Introduction Coccidian species of the genus Caryospora Léger, 1904 (Apicomplexa, Eimeriidae) found primarily in reptiles and raptorial birds are characterised by an oöcyst with a single, octozoic sporocyst. The species of the genus Caryospora represent the most common protozoan parasites found in raptors. At present, a total of ten species of the genus Caryospora are known from falconid and accipitrid raptors. In this paper, two new Caryospora species are described from accipitrid hosts kept in the Czech Republic and compared with those previously described raptor caryosporan species.

solution. The birds were adult and came from raptor rehabilitation centres, Zoos, and private raptor keepers. Coccidia were allowed to sporulate in a thin layer of 2.5% (w/v) aqueous potassium dichromate solution at laboratory temperature, c. 23 ◦ C and 30 sporulated oöcysts were measured using bright-field microscopy (100× objective) equipped with a calibrated ocular micrometer to obtain morphologic data. All measurements are given in micrometres (µm), as the mean followed by the range in parentheses. Isolated oöcysts were examined and photographed using Nomarski interference contrast microscopy.

Results Materials and methods Between September, 1996 and March, 1998, faecal samples of 10 golden eagles Aquila chrysaetos and 13 marsh harriers Circus aeruginosus were examined for parasites using faecal flotation in Sheather’s sugar

Among 10 examined golden eagles Aquila chrysaetos (Linnaeus), only one (10%) was found to be passing coccidian oöcysts. This bird was a long term captive. One of 13 (7.7%) examined marsh harriers Circus aeruginosus (Linnaeus) was repeatedly found

24 to be passing oöcysts of another coccidian species. The marsh harrier was a handicapped bird from nature. Both coccidian species are described below as new.

Caryospora aquilae n. sp. (Figures 1, 3) Description Oöcysts subspherical to broadly ellipsoidal, 43 (40–49) × 37.5 (34–39), with shape-index (SI; length/width) 1.15 (1.03–1.26). Oöcyst wall smooth, bi-layered, 2.2 (2.0–2.5), with inner layer c. 0.5 thick. Polar granule, oöcyst residuum and micropyle absent. Sporocysts spherical to subspherical, slightly polygonal, measuring 23.8 (23–25) × 23.3 (22– 25), SI 1.02 (1.00–1.45); Stieda and substieda bodies absent. Sporocyst wall smooth, thin. Sporozoites vermiform, 13.5 (13–14) × 4.5 (4–5) (in situ), lying randomly within sporocyst. Sporozoites contain posteriorly located spherical refractile body, 3 in diameter. On day 10 of sporulation, sporocyst residuum comprises numerous small granules < 0.5 in diameter, dispersed randomly among sporozoites. Type-host: Aquila chrysaetos (Linnaeus), golden eagle, (Falconiformes: Accipitridae); long-term captive. Type-locality: Private raptor collection, Cheb, Czech Republic. Data on origin unknown. Type-specimens: Phototypes are deposited in the Institute of Parasitology, Academy of Sciences of the ˇ Czech Republic in Ceské Budˇejovice, collection number Fc 1/96. Sporulation: Exogenous. About 90% of oöcysts were sporulated within 3 days. The remaining 10% failed to sporulate, and began to degenerate. Site of infection: Unknown; oöcysts found in faeces. Prevalence: One of 10 (10%) of the birds were infected.

Caryospora circi n. sp. (Figures 2, 4) Description Sporulated oöcysts widely oval, measuring 24.5 (23– 25) × 21.8 (21–24), with SI of 1.12 (1.04–1.19). Oöcyst wall bi-layered, smooth, colourless and 2 thick, with inner layer c. 0.5. Polar granule, oöcyst residuum and micropyle absent. Sporocysts spherical to subspherical, 16.2 (15–17) × 15.6 (15–17), with SI of 1.04 (1.00–1.07). Sporocyst wall smooth,

thin; Stieda and substieda bodies absent. Sporozoites elongate oval, measuring 10.4 (9–11) × 4.3 (4–5) (in situ), randomly arranged within sporocyst. Sporozoites with prominent parallel transverse striation and single spherical nucleus located centrally. On day 9 of sporulation, spherical to subspherical compact, granular sporocyst residuum, 10.4 (10–11) × 8.5 (7–9), present in 76% of measured sporocysts. In 24% of sporocysts, granules of sporocyst residuum are scattered among sporozoites. Type-host: Circus aeruginosus (Linnaeus), marsh harrier (Falconiformes: Accipitridae). Type-locality: Host caught in Rychaltice, district of Frýdek-Místek, Czech Republic; at time of examination kept in Raptor Rehabilitation Centre, Bartošovice na Moravˇe, Czech Republic. Type-specimens: Phototypes are deposited in the Institute of Parasitology, Academy of Sciences of the ˇ Czech Republic in Ceské Budˇejovice, collection number Ba 1/97. Sporulation: Exogenous. Oöcysts were fully sporulated within 4 days. Site of infection: Unknown; oöcysts found in faeces. Prevalence: One of 13 (7.7%) was infected.

Discussion To date, there are seven Caryospora spp. described (only five of them are named) from accipitrid birds. These are C. arcayae Volca´n & Medrano, 1984 from Buteo magnirostris (see Volca´n & Medrano, 1984) and B. platypterus (see Upton et al., 1990), C. kansasensis Upton, Campbell, Weigel & McKown, 1990 from B. swainsonii (see Upton et al., 1990), C. lindsayi Upton, Campbell, Weigel & McKown, 1990 from B. jamaicensis (see Upton et al., 1990), C. tremula (see Allen, 1933) from Cathartes aura (see Allen, 1933; Hoare, 1934; Lindsay et al., 1994) and C. uptoni Lindsay & Blagburn, 1986 from B. borealis (Lindsay & Blagburn, 1986; Lindsay et al., 1994). Additionally, two types of caryosporan oöcysts were reported from Milvus migrans by Yakimoff & Matschoulski (1936). Another five species are reported from raptors of the family Falconidae: C. boeri Klüh, 1994 from Falco tinnunculus (see Klüh, 1994), C. falconis Wetzel & Enigk, 1937 from F. peregrinus, F. subbuteo and F. tinnunculus (Wetzel & Enigk, 1937, 1939; Kutzer et al., 1980; Klüh, 1994) and Athene noctua as an experimental host (see Wetzel & Enigk, 1939),

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Figure 1–2. Nomarski interference contrast photographs of the sporulated oöcysts. Both to the same scale. 1. Longitudinal view of oöcyst of Caryospora aquilae n. sp.; note the granule of sporocyst residuum (SR). 2. Oöcyst of C. circi n. sp.; note the sporocyst residuum (SR) and the transverse striation of sporozoites (arrow). Scale-bar: 20 µm.

C. kutzeri Böer, 1982 from F. mexicanus, F. tinnunculus, F. biarmicus, F. jugger, F. cherrug, F. rusticolus, F. peregrinus and F. subbuteo (see Böer, 1982; Kutzer et al., 1980; Schellner & Rodler, 1971; Yakimoff & Matschoulski, 1936), C. megafalconis Klüh, 1994 from F. rusticolus, F. cherrug and, additionally, F. tinnunculus as an experimental host (see Klüh, 1994), and C. neofalconis, Böer 1982 from F. biarmicus, F. mexicanus, F. peregrinus, and F. subbuteo, plus F. tinnunculus as experimental hosts (Böer, 1982). Caryospora aquilae n. sp. appears to have larger oöcysts than any other of the above mentioned Caryospora spp. from accipitrid hosts. On the other hand, in comparison with caryosporans described from falconid hosts, the morphological data are similar as those of C. megafalconis. However, C. aquilae has a thicker oöcyst wall and shorter sporozoites than C. megafalconis. Additionally, sporocysts of C. aquilae fail to possess the compact spherical sporocyst residuum as described for C. megafalconis; however, the character of the sporocyst residuum may

change during the process of sporulation (Lindsay et al., 1994). Among the caryosporan species from accipitrid hosts, Caryospora circi n. sp. is most similar in size to C. uptoni, but it differs by having significantly smaller sporocysts. All of the above-mentioned species can be distinguished from C. circi by their larger oöcysts and sporocysts. Among the caryosporan parasites of falconid raptors, C. circi is similar to C. neofalconis. However, oöcysts and sporocysts of C. circi are apparently smaller and sporocysts are much more spherical than those of C. neofalconis. All other species of Caryospora described from falconids have oöcysts and sporocysts significantly larger than those of C. circi. The reported host range of any caryosporan species infecting raptors is not known to extend beyond generic boundaries. Although Wetzel & Enigk (1939) reported Athene noctua to be an experimental host of Caryospora falconis, these results are considered to be in error and the reported excretion of oöcysts was probably a consequence of a natural infection

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Figure 3. Composite line drawing of a sporulated oöcyst. of Caryospora aquilae n. sp. Scale-bar: 20 µm.

Figure 4. Composite line drawing of a sporulated oöcyst of Caryospora circi n. sp. Scale-bar: 10 µm.

27 by another caryosporan species (Upton et al., 1990). All other attempts at cross-generic transmission of caryosporans of birds of prey have failed (Allen, 1933; Cawthorn & Stockdale, 1982). However, crossinfections between congeneric hosts have been successful (Böer, 1982; Klüh, 1994). Based on these results, we consider the whole group of caryosporan species infecting birds of prey to be relatively host specific at host generic level. On the basis of both morphological differences and host specificity, Caryospora aquilae n. sp. and C. circi n. sp. cannot be confused with any of the abovementioned caryosporan species infecting raptors and consequently represent new taxa.

Acknowledgements We thank Jan Šlapeta for preparing the line drawing. We are indebted to all bird keepers and especially to Ing. Ivo Otáhal, from the Raptor Rehabilitation Centre Bartošovice, for helpful co-operation. This study was supported by grants from the Ministry of Education, Youth and Sports of the CR, no. 1087/1998 and no. 1243/1999.

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