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1993 Enteric Coccidia (Apicomplexa) in the Small Intestine of the Northern Spotted Owl (Strix occidentalis caurina) Eric P. Hoberg Animal Parasitic Disease Laboratory, Agricultural Research Service, United States Department of Agriculture, [email protected]

R. J. Cawthorn University of Prince Edward Island

O. R. Hedstrom Oregon State University

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Hoberg, Eric P.; Cawthorn, R. J.; and Hedstrom, O. R., "Enteric Coccidia (Apicomplexa) in the Small Intestine of the Northern Spotted Owl (Strix occidentalis caurina)" (1993). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 825. http://digitalcommons.unl.edu/parasitologyfacpubs/825

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Journal of Wildlife Diseases, 29(3), 1993, pp. 495-497

Enteric Coccidia (Apicomplexa) in the Small Intestine of the Northern Spotted Owl (Strix occidentalis caurina)

E. P. Hoberg,’4 R. J. Cawthorn,2 and 0. R. Hedstrom,3 ‘Biosystematic Parasitology Laboratory, Agricultural Research Service, U.S. Department of Agriculture, Beltsville Agricultural Research Center, Beltsville, Maryland 20705,

USA; 2 Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Chartottetown, Prince Edward Island, Canada CiA 4P3; College of Veterinary Medicine, Oregon State University, Corvallis, Oregon 97331, USA. Corresponding author

ABSTRACT: Sporulated oocysts (mean dimen- Corvallis, Oregon, USA) in November sions = 13.0 x 10.8 tm) and sporocysts (11.3 x 1985. The owl, found dead near Med- 5.5 Mm) of a coccidian resembling Frenkelia sp. ford, Oregon (approximately 42#{176}16’N; or Sarcocystis sp. were present in the lamina 122#{176}50’W), had been wearing a radio propria of the small intestine of a naturally- infected northern spotted owl (Strix occiden- transmitter for the preceding 4 mo as part talis caurina) collected near Medford, Oregon of a study of juvenile dispersal in western (USA). Dimensions of these oocysts and sporo- Oregon (Miller and Meslow, 1985). The cysts appear to be considerably smaller than owl was necropsied within 2 days of death, those from other sarcocystid species with avian definitive hosts. Additionally, numerous devel- having been transported from the field on opmental stages and unsporulated oocysts (mean ice and stored at 4 C for a short period dimensions 22.8 x 17.8 Mm) of a possible species immediately prior to examination. Fresh of Isospora also were observed in the intestinal tissues and feces were not examined. Tis- epithelium. This constitutes the first report of sue specimens from the liver, spleen, kid- enteric coccidia from spotted owls. Neither par- asite appeared to cause the death of the bird. ney, lung, heart, brain, small intestine, and Key words: Strix occidentalis caurina, gizzard were fixed in 10% neutral buffered northern spotted owl, Frenkelia sp., Sarcocystis formalin, embedded in paraffin, sectioned sp., intestinal coccidia. at 5 m, and stained with hematoxylin and The northern spotted owl (Strix occi- eosin. A few sporulated oocysts containing dentalis caurina) has been the focus of a sporocysts and sporozoites of a Frenkelia- continuing ecological confrontation in the like parasite (or Sarcocystis) were ob- old-growth forests of the Pacific Northwest served in the small intestine (Figs. 1, 2). (USA) (Simberloff, 1987). Although de- Numerous developmental stages of an- tailed knowledge of the biology of spotted other unidentified coccidian also were owls has developed as a consequence of found in intestinal epithelium (Figs. 1 to this debate (Forsman et a!., 1984; Guti#{233}r- 4). Because Frenkelia and Sarcocystis are rez and Carey, 1985), until recently there known only from the subepithelium, these has been a paucity of information con- stages may represent a species of Isospora. cerning parasitism. Hoberg et a!. (1989) Representative tissue sections were depos- and Guti#{233}rrez (1989) conducted studies of ited in the U.S. National Parasite Collec- parasitic helminths and hemoprotozoans, tion (No. 82810), U.S. Department of Ag- respectively, but there have been no pre- riculture, Agricultural Research Service, vious reports of enteric coccidia from spot- Biosystematic Parasitology Laboratory, ted owls as summarized by Cawthorn et Beltsvi!le, Maryland (USA). a!. (1984) and Levine (1986). The level of infection by the Frenkelia- In the present study we report the dis- like organism appeared to be minimal. Few covery of at least two genera of enteric sporulated oocysts (containing two sporo- coccidia from a juvenile female spotted cysts each with four sporozoites) were ob- owl submitted to the Veterinary Diagnos- served in the lamina propria. Thin-walled tic Laboratory (VDL, College of Veteri- oocysts (n = 10) (Figs. 1, 2) measured 12.4 nary Medicine, Oregon State University, to 15.5 m (mean ± SD = 13 ± 0.997) x

495 496 JOURNAL OF WILDLIFE DISEASES, VOL. 29, NO. 3, JULY 1993

the villi. Microgametocytes, macrogame- tocytes, along with developing oocysts (with poorly differentiated walls), and un- sporulated oocysts were observed (Figs. 1 to 4). These latter stages were distinctly larger than those attributed to the Fren- kelia-like organism. Microgametocytes (n

= 10) measured 7.8 to 10.4 m (mean ±

SD = 9.8 ± 0.91) in diameter (Fig. 3);

developing oocysts (n = 10) with distinctly granular margins were 15.5 to 18.6 m (17.2 ± 1.09) in diameter (Figs. 1, 3, 4); and unsporulated oocysts with well differ-

entiated walls (n = 10) were 20.2 to 27.9 m (22.8 ± 2.64) x 17.8 to 23.3 m (19.7 ± 1.75) (Figs. 1, 4). Oocysts and deve!- opmental stages were distributed largely near the tips of the villi and were not ob- served in the crypts. Development and sporulation in situ are

FIGURES 1 to 4. Enteric stages of a Frenkelia sp.- characteristic of species of Frenkelia and like organism and an unidentified coccidian shown Sarcocystis in avian definitive hosts (Caw- in tissue sections from the intestinal epithehium of a thorn et a!., 1984; Lindsay et a!., 1987; northern spotted owl, Strix occidentalis caurina. All Lindsay and Blagburn, 1989). Life cycle preparations are with hematoxyhin and eosin. Figure studies and experimental transmission 1. Sporulated oocyst of a Frenkelia-like coccidian (open arrow) and developing and unsporulated 00- would be necessary for generic and spe- cysts of an unidentified coccidian (black arrows). Bar cies-level identification of the sarcocystid

= 25 m. Figure 2. Sporulated oocyst of a Frenkelia- from spotted owls. However, based on like organism (open arrow) with two sporocysts visible comparisons of the oocysts and sporocysts within the oocyst wall; also, developing oocyst of an these specimens apparently are not a nom- unidentified coccidian (black arrow). Bar = 10 Mm. Figure 3. Microgametocyte (open arrow) and oocyst inal species among these genera. The two lacking differentiated wall (black arrow) attributable valid species of Frenkelia (F. glareoli, F. to an unidentified coccidian. Bar = 15 m. Figure 4. microti) typically occur in Buteo spp. in Unsporulated oocyst of an unidentified coccidian the Palearctic and Holarctic regions, re- (black arrow). Bar = 15 .&m. spectively. Sporocysts of F. microti in North America are larger and differ in

9.3 to 12.4 (10.8 ± 0.776); sporocysts (n = shape index (1.1 to 1.5) from those found 3) were 11 to 12 m (11.3 ± 0.577) x 5 in spotted owls (Upton and McKown, to 6 m (5.5 ± 0.701) and had a shape 1992). Although four of the five species of index (length/width) of 1.83 to 2.4; spo- Sarcocystis from raptors occur in strigi- rozoites could not be accurately measured. forms (S. rauschorum, S. dispersa, S. scot- A Steida body or sporocyst residuum was ti, and S. sebeki) the oocysts and sporocysts not observed. Few unsporulated oocysts of these generally are larger and less elon- were observed and microgametocytes and gate than those reported in the present asexual stages attributable to this coccidian study (Cawthorn et a!., 1984). were not identified. Transmission of the Frenkelia-like or- Another coccidian was even more nu- ganism from spotted owls is likely to in- merous in the intestinal vil!i. Parasites were volve rodent intermediate hosts. Microtine located above the nucleus of the epithelial rodents (Phenacomys longicaudus, Cleth- cells and primarily at or near the tips of rionomys spp.), sciurids (Glaucomys sa- SHORT COMMUNICATIONS 497

brinus), and cricetids (Neotoma spp.) are cyclic transmission between varying lemmings among the primary prey taken by these (Dicrostonyx richardsoni) and snowy owls (Nyc- tea scandiaca). Canadian Journal of Zoology 62: owls, although the diet includes 31 species 217-225. of mammals (Forsman et al., 1984). Ex- FORSMAN, E. D., E. C. MESLOW, AND H. M. WIGHT. amination of these small mammals in the 1984. The distribution and biology of the spot- Pacific Northwest is required to determine ted owl in Oregon. Wildlife Monographs 87: 1- their role in the life cycle. 64. GUTIERREZ, H. J. 1989. Hematozoa from the spotted Infection with either the Frenkelia -like owl. Journal of Wildlife Diseases 25: 614-618. organism or the unidentified coccidian did AND A. B. CAREY (editors). 1985. Ecology not appear to contribute to the death of and management of the spotted owl in the Pacific the owl; although oocysts and develop- Northwest. General Technical Report PNW-185. mental stages were relatively numerous U.S. Department of Agriculture Forest Service, Pacific Northwest Forest and Range Experiment within the mucosa! enterocytes or along Station, Portland, Oregon, 119 pp. the mucosal surface, we observed no sig- HOBERG, E. P., G. S. MILLER, E. WALL- nificant inflammatory response. However, NER-PENDLETON, AND 0. H. HEDSTROM. 1989. intestinal infection by species of Sarcocys- Helminth parasites of northern spotted owls (Strix occidentalis caurina) from Oregon. Journal of tis may be associated with clinical disease Wildlife Diseases 25: 246-251. and death in some raptors (Cawthorn et LEVINE, N. D. 1986. The taxonomy of Sarcocystis al., 1984). Consequently, these and other (Protozoa, Apicomplexa) species. The Journal of parasites should continue to be studied as Parasitology 72: 372-382. a potential contributing factor influencing LINDSAY, D. S., AND B. L. BLAGBURN. 1989. Car- the population biology of threatened and yospora uptoni and Frenkelia sp.-hike coccidial infections in red-tailed hawks (Buteo borealis). endangered species (Guti#{233}rrez, 1989). Journal of Wildlife Diseases 25: 407-409. We thank G. S. Miller at the Oregon S. I. AMBRUS, AND B. L. BLAGBURN. 1987. Cooperative Wildlife Research Unit, De- Frenkelia sp.-hike infection in the small intestine partment of Fisheries and Wildlife, Ore- of a red-tailed hawk. Journal of Wildlife Diseases gon State University for originally making 23: 677-679. MILLER, C. S., AND E. C. MESLOW. 1985. Dispersal this owl available for examination. The data for juvenile spotted owls: The problem of necropsy was conducted by E. Wallner- small sample size. In Ecology and management Pendleton at VDL, College of Veterinary of the spotted owl in the Pacific Northwest, R. Medicine, Oregon State University. His- J. Guti#{233}rrezand A. B. Carey (eds.). General Tech- tological preparations were provided by nical Report PNW-185. U.S. Department of Ag- riculture Forest Service, Pacific Northwest Forest the staff of the VDL. Critical comments and Range Experiment Station, Portland, Ore- which improved the manuscript were gon, pp. 69-73. kindly provided by R. Fayer and M. Jen- SIMBERLOFF, D. 1987. The spotted owl fracas: Mix- kins, U.S. Department of Agriculture, Ag- ing academic, applied and political ecology. ricultural Research Service, Beltsville, Ecology 68: 766-772. UPTON, S. J., AND H. D. MCKovN. 1992. The red- Maryland. tailed hawk, Buteo jamaicensis, a native defin- itive host of Frenkelia microti (Apicomplexa) in LITERATURE CITED North America. Journal of Wildlife Diseases 28: CAWTHORN, H. J., A. A. GAJADHAR, AND R. J. BROOKS. 85-90. 1984. Description of Sarcocystis rauschorum sp. n. (Protozoa: Sarcocystidae) with experimental Received for publication 30 March 1990.