j. Raptor Res. 28(4):226-231 ¸ 1994 The Raptor ResearchFoundation, Inc.

BLOOD PARASITES OF RAPTORS IN FLORIDA

DONALDJ. FORRESTER,SAM R. TELFORD,.JR. AND GARRYW. FOSTER Departmentof InfectiousDiseases, College of VeterinaryMedicine, Universityof Florida, Gainesville,FL 32677 U.S.A.

GORDON F. BENNETT InternationalReference Centre for Arian tiaematozoa,Memorial Universityof Newfoundland, St. John's,Newfoundland, A 7B 3X9, Canada

ABSTRACT.--Fifteenspecies of bloodprotozoans and an unidentifiedmicrofilaria were foundin thin blood films from 55 strigiformsand 138 falconiformsexamined in Florida. All four of the speciesof strigiforms sampledwere infected,with an overall hemoparasiteprevalence of 63%, excludingnestlings. Seven of 11 speciesof falconiformssampled were parasitized,with a prevalenceof 33%, excludingnestlings. Mixed infectionsof two or more speciesoccurred in 28 , 22 had two speciesof hemoparasites,three had three ,and three had four species.Among the infectionsof hemoparasites, species were most common(67%), followedby (22%), (9%), Trypanosoma(1%), and microfilariae(1%). A Plasmodium(Novyella) sp., previouslyknown only from a (Strix varia) in Georgia,was presentin the greathorned owl (Bubovirginianus), bald eagle(Haliaeetus leucocephalus), and broad-wingedhawk (Buteoplatypterus) in Florida. The identificationof Leucocytozoonziemanni is the first recordof this speciesin barn owls (Tyto alba) from North America and Trypanosomaconfusum is reportedfor the first time in a barred owl. KEY WORDS:Falconiformes; Florida; hemoparasites; prevalence; raptors; Strigiformes.

Par&sitossanguineos de rapacesen Florida RESUMEN.--Quinceespecies de protozoossanguineos y una "microfilaria"fueron encontrados en delgados frotis de sangreobtenidos en 55 Strigiformesy 138 Falconiformesde Florida. Las cuatro especiesde Strigiformesmuestreadas estaban infectadas con una prevalenciadel 63% de hemopar/tsitos,excluidos los polluelos.Siete de 11 especiesde Falconiformesmuestreados estaban parasitados con una prevalenciadel 33%, excluidoslos pollos.Infecciones mezcladas de doso m/rsespecies afectaron a 28 aves,tres tenlan cuatro especiesde par•isitos.Entre las infeccionespor hemoparSsitos,Haemoproteus fue la especiem•is comfin(67%), seguidode Plasmodium(22%), Leucocytozoon(9%), Trypanosoma(1%) y micofilariae(1%). Plasmodium(Novyella) sp., previamenteconocido s61o para Strix varia en Georgia, estabapresente en Bubovirginianus, tialiaeetus leucocephalus yen Buteoplatypterus en Florida.La identificaciGnde Leucocytozoon ziemanni,es el primer registrode estaespecie en Tyto alba presenteen America del Norte. Trypanosoma confusumes reportadopor primera vez en Strix varia. [TraducciGn de Ivan Lazo]

Strigiformsand falconiformsare prominentcom- data with informationon parasiteinfections of rap- ponentsof the avifauna of Florida, yet their blood tors from other geographicareas. Some host records parasitesare poorly known. We are aware of only in the presentpaper have been included also in a three publicationsdealing with this topicin Florida. brief and limited format in a host-parasitecatalogue Greiner et al. (1981) reporteda parasiteresembling (Bishop and Bennett 1992) and in a taxonomicre- Plasmodiumpolare in a bald eagle (Haliaeetusleu- view of the haemoproteidsof falconiforms(Peirce et cocephalus);Sykes and Forrester (1983) examined al. 1990). blood films from 19 snail kites (Rostrhamussociabilis) without finding hemoparasites;and Dooris et al. METHODS (1981) found no blood parasitesin 30 burrowing We obtainedblood films from 55 strigiforms(four spe- owls (Speotytocunicularia). cies)and 138 falconiforms(11 species)from 1973-91. All birds sampled were fledgedjuveniles or adults with the The objectivesof the presentstudy were to deter- exceptionof 44 bald eaglesand one eastern screech-owl mine the speciesand prevalenceof blood parasites (Otusasio) which were nestlings(<8 wk of age). Exact presentin raptorsin Florida, and to comparethese ageswere not known. Of the 147 fledgedraptors for which

226 DECEMBER 1994 RAPTOR BLOOD PARASITES 227 we have preciselocality information(the locality was un- 22 had two species,three had three species,and three known for one eagle), 121 were from northern Florida had four species. (localities north of Manatee, Polk, Osceola, and Brevard counties) and 26 were from southern Florida (localities An apparentlyundescribed Plasmodium (Novyel- south of the above listed counties). la) specieswas seen in three birds: a great horned Thin blood smearswere prepared from cardiac or pe- owl (Bubovirginianus), a bald eagle, and a broad- ripheral blood,fixed in absolutemethanol, and stainedby winged hawk (Buteoplatypterus). Gametocytes of standard Giemsa technique for 1 hr at pH 7.0, or in the case of fixed but unstained slides which had been stored this parasitehad notably crenulatemargins. Schiz- for severalmonths, by Giemsa in an acidicacetone-based ontswere tiny with four nuclei,were fan-shapedor buffer at pH 6.4 for 1.5-2 hr (Kimsey 1992). Material cruciform, measured 3.5-4.5 x 2-4 •tm and were obtainedfrom the Collegeof Veterinary Medicine, Uni- found in mature erythrocytes. versityof Florida, was comprisedof coverslipsmears that had been stained by the Wright-Giemsa method. Slides DISCUSSION were examined at 400 x to determineprevalences of par- asites.Measurements of parasiteswere done with a cal- The samePlasmodiurn (Novyella) species reported ibrated ocular micrometer under oil immersion (1000 x ). from a barred owl (Strix varia) from southern Geor- The taxonomiccharacters used for identification of par- gia by Telford and Forrester(1992) is reportedhere asiteswere thoseutilized by Telford (1988) for Plasmodium from three additional hosts. The characteristic schiz- species,by Forrester et al. (1977), Bennett and Peirce (1988), Peirceet al. (1990), and Bishopand Bennett (1989) ontswere commonin the greathorned owl, very rare for Haemoproteusspecies, by Greiner and Kocan (1977) in the bald eagle, and absentin the broad-winged and Bennett et al. (1991) for Leucocytozoonspecies, and hawk. Identification of the infection in the latter host by Baker (1976) and Telford et al. (1991) for trypano- was basedupon a high proportion of gametocytes somes.Statistical comparisons of samplemeans were made which had irregular or crenulatemargins. by Student'st-test, and of sample proportionsby chi- square (a = 0.05). Greiner et al. (1981) reported the presenceof Representativeblood films have been depositedin the distinctivegametocytes with crenulatemargins in a collection of the International Reference Centre for Avian bald eagleinfected by parasitesresembling P. polare, Haematozoa, Memorial University, St. John's, New- but were uncertainwhether they representeda sep- foundland (AccessionNos. 68665, 116415-116441, and 125553-125556). arate taxon or were possiblysenescent. We were able to study blood films from the bald eagle ex- RESULTS amined by Greiner et al. (1981). The gametocytes Hemoparasiteswere foundin all speciesof raptors with crenulatemargins were the mostcommon form examinedexcept the black vulture (Coragypsatra- present in a ratio to those of P. polare that exceeded tus),turkey vulture ( Cathartesaura), osprey(Pandion 50:1, which would argue against senescence.Dis- haliaetus),and merlin (Falcocolumbarius) (Table 1). coveryof a few tiny schizontssimilar to thosefound The 44 nestling bald eagles and the one nestling in the barredowl from Georgia (Telford and Forres- easternscreech-owl were negativeand were not in- ter 1992) and the great horned owl (this paper) eludedin statisticalanalyses or comparisonsbecause providedadditional evidenceof their conspecificity of their young age and becausenestlings were not with this undescribedspecies. These probably are •ncludedin the samplesof other species.Overall, not immature schizontsof P. polare becausein this strigiformsshowed a significantlygreater prevalence species,nuclear division does not begin until the of hemoparasitesthan did falconiforms(63 vs. 33ø70, trophozoitesare nearly twice the size of the Plas- chi-square,P < 0.01). rnodiurn(Novyella) sp. schizonts.The identification Haemoproteusspecies were most common(67%), of P. polare-likeparasites in the bald eagleby Grei- followedby Plasmodium(22%), Leucocytozoon(9%), ner et al. (1981) is appropriate,given the paucity of Trypanosoma(1%), and microfilariae (1%). Fifty- data available for this speciesof Plasrnodiurn. eight infectionswere found in strigiforms:44 Hae- We have identifiedthe haemoproteidfrom eastern tooproteus(76%), 11 Plasmodium(19%), one Leu- screech-owlsas H. syrnii, but it is possiblethat it cocytozoon(2%), one Trypanosoma(2%), and one representsanother, possibly undescribedspecies. microfilarial infection (2%). There were 43 infec- Gametocytesin screech-owlswere smaller and less tions in falconiforms:25 Haemoproteus(58%), 11 heavily pigmentedthan thoseof H. syrnii in barred Plasmodiurn(26%), and sevenLeucocytozoon (16%), owls and great horned owls. These variations may but no trypanosomesor microfilariae.Mixed infec- have been due to strain differences or host effects, tions of two or more speciesoccurred in 28 birds: but further studiesare needed.Both H. syrnii and 228 FORRESTERET AL. VOL. 28, NO. 4 DECEMBER 1994 RAPTOR BLOOD PARASITES 229

Table 2. Prevalencesof the commongenera of bloodparasites in raptorsfrom North Americaand the Neotropical region.

PER- NUMBER CENT PERCENT POSITIVE FOR OF BIRDS POSI- EXAMINED TIVE pa H b L c T d SOURCE

Strigiformes North America 118 51 7 21 37 3 Greiner et al. (1975) Maryland-New Jersey 28 18 4 7 7 4 Williams and Bennett (1978) Florida 54 63 17 56 2 2 This study Louisiana 34 68 0 73 12 0 Olsen and Gaunt (1985) Neotropics 44 25 9 18 +e +e White et al. (1978) Falconiformes North America 309 40 3 23 21 3 Greiner et al. (1975) Maryland-New Jersey 33 33 0 33 9 0 Williams and Bennett (1978) New Jerseyarea f 249 59 1 22 43 1 Kirkpatrick and Lauer (1985) Florida 93 33 11 26 8 0 This study Louisiana 21 24 0 14 9 0 Olsen and Gaunt (1985) Neotropics 119 30 8 19 1 2 White et al. (1978) Plasmodium. Haemoproteus. Leucocytozoon. Trypanosoma. Prevalencesnot given by author. New Jersey,Pennsylvania, Delaware, and Virginia.

H. noctuaehave been reported previously from east- muliid vectors by falconiformsbecause of their ern screech-owls(Bishop and Bennett 1989). broaderranges, in comparisonto the more sedentary Trypanosomaconfusum is known from severalstri- strigiforms.It is possiblealso that strigiformbehav- giforms (Bennett et al. 1982, Bishop and Bennett ior patterns(foraging at night and using secluded, 1992), but has not been reportedpreviously from shadyperches during day) exposethem more fre- the barred owl. An unidentifiedtrypanosome found quently to a variety of vectorspecies (and hencea by Wetmore(1941) in the barredowl wasprobably larger variety of hemoparasites)than do those of T. confusum.Although Baker (1976) hasdefined the falconiforms(daytime activity period and elevated trypanosome from the New World as T. confusum, perchesat night). the parasiteis morphologicallyindistinguishable from The overall prevalenceof Plasmodiumspecies in Trypanosomaavium of Old World strigids.Bennett both strigiforms and falconiforms in Florida was (1961, 1970) showedthat the trypanosomeorigi- greater than that recordedin other comparablesur- nating from the northern saw-whet owl (Aegolius veys(Table 2). These prevalencesprobably would acadicus)could be transmittedvia themosquito Aedes have been even higher if isodiagnostictechniques aegypti to a number of different avian speciesof had been used since Plasmodium infections in birds severalorders and families, thus indicating a total are known to virtually disappearfrom the circulating lack of host specificity.Measurements and derived blood when infections become chronic (Herman et •ndicesfrom trypanosomes from Old andNew World al. 1966). Haemoproteusspecies were alsomore com- borealowls (Aegoliusfunereus)are identicalto those mon in strigiformsin Florida than in other areas from the northern saw-whet owl and the two species exceptLouisiana (Olsen and Gaunt 1985), but in of trypanosomesare likely to be synonymous(G. falconiformstheir prevalencein Florida was similar Bennett unpubl. data). to the overall estimate for North America (Greiner Falconiformswere parasitized more commonly by et al. 1975) and the Neotropics(White et al. 1978). Leucocytozoonthan were strigiforms.This may re- Leucocytozoonspecies, however, had a lower prev- flect a greater opportunity for contactwith the si- alencein strigiformsfrom Florida than generallyin 230 FORRESTERET AL. VOL. 28, NO. 4

North America (Greiner et al. 1975) or on the east- list of the genusHaemoproteus Kruse, 1890. J. Nat ern seaboard (Williams and Bennett 1978). In fal- Hist. 22:1683-1696. coniforms,Leucocytozoon species had a lower prev- , M. WHITEWAY AND C. WOODWORTH-LYNAS alencein Florida than reportedin the North Amer- 1982. A host-parasitecatalogue of the avian haema- xcan survey (Greiner et al. 1975) and the 1985 tozoa. Mere. Univ. NewfoundlandOcc. Pap. Biol. 5, St. John's, Newfoundland, Canada. New Jersey survey(Kirkpatrick and Lauer 1985), --, R.A. EARLE,M.A. PEIRCE,F.W. HUCHZERMEYER but was comparableto that foundin the 1978 Mary- AND D. SQUIRES-PARSONS.1991. Avian Leucocyto- land-New Jersey survey (Williams and Bennett zoidae:the leucocytozoidsof the Phasianidaesensu lato 1978) and the Louisianasurvey (Olsen and Gaunt J. Nat. Hist. 25:1407-1428. 1985). Leucocytozoonspecies are presentin the Neo- BISHOP, M.A. AND G.F. BENNETT. 1989. The haemo- tropics(White et al. 1978), but there is little infor- proteidsof the avian order Strigiformes.Can. f. Zool mation on prevalences.The data on Trypanosoma 67:2676-2684. from all areassurveyed may be misleadingbecause -- AND-- 1992. Host-parasitecatalogue of of the inefficiencyin detectinginfections by using the avianhaematozoa, Supplement 1 andbibliography bloodfilms; more trypanosome infections would have of the avianblood-inhabiting haematozoa, Supplement been detected if bone marrow had been examined 2. Mern. Univ. NewfoundlandOcc. Pap. Biol. 15, St John's, Newfoundland, Canada. and if culture methods had been used. DOORIS,G.M., P.M. DOORISaND W.D. COURSER. 1981 The absenceof hematozoain burrowing owls of the Tampa Bay area, Florida. Fla. Field Nat. 9:9. ACKNOWLEDGMENTS FORRESTER,D.J., E.C. GREINER,G.F. BENNETtaND M.K. We thank Noha Abou-Madi and Ramiro Isazafor pro- KIGAYE. 1977. Avian .7. A review viding accessto raptors in the Wildlife Clinic of the Vet- of the haemoproteidsof the family Ciconiidae(storks) erinary Medical TeachingHospital at the Universityof anddescriptions of Haemoproteusbrodkorbi sp. nov. and Florida. Vicki L. Clyde preparedsome of the bloodfilms H. peircei sp. nov. Can. f. Zool. 55:1268-1274. and Edward B. Rabin furnished us with slides from the GREINER,E.C. AND A.A. KOCAN. 1977. Leucocytozoon ClinicalPathology files. We appreciatetheir cooperation. (Haemosporidia;Leucocytozoidae) of the Falconi- DyanneD. Singlergave us accessto raptorsat The Con- formes. Can. f. Zool. 55:761-770. servancyin Naples,Florida. Petra B. Wood suppliedus with slidesfrom nestlingbald eagles.Ellis C. Greiner --, D.J. BLACKAND W.O. IVERSON. 1981. Plas- generouslypermitted us to include some of his material modiumin a bald eagle (Haliaeetusleucocephalus) in from bald eaglesin our sample,and both he and Martin Florida. f. Wildl. Dis. 17:555-558. D. Youngreviewed the manuscript. Marilyn G. Spalding --, G.F. BENNETT, E.M. WHITE AND R.F. COOMBS alsoexamined an earlydraft of themanuscript and offered 1975. Distribution of the avian hematozoa of North somehelpful suggestions. This researchwas supported by America. Can. f. Zool. 53:1762-1787. contracts from the Florida Game and Fresh Water Fish Commission's Federal Aid to Wildlife Restoration Pro- HERMAN,C.M., J.O. KNISLEYAND E.L. SNYDER. 1966. gram, Florida Pittman-RobertsonProject W-41 to DJF Subinoculationas a techniquein the diagnosisof avian and by an operatinggrant from the Natural Sciencesand Plasmodium. Arian Dis. 10:541-547. EngineeringResearch Council of Canada to GFB. This KIMSEY,R.B. 1992. Host associationand the capacity •sFlorida Agricultural Experiment Station's Journal Series of sandflies as vectorsof lizard malaria. Int. f. Parasitol No. R-03155. 22:657-664. KIRKPATRICK,C.E. AND D.M. LAUER. 1985. Hematozoa of raptors from southernNew Jersey and adjacent LITERATURE CITED areas. J. Wildl. Dis. 21:1-6. OLSEN, G.H. AND S.D. GAUNT. 1985. Effect of hemo- BAKER,J.R. 1976. Biologyof the trypanosomesof birds. Pages 131-174 in W.H.R. Lumsden and D.A. Evans protozoal infectionson rehabilitation of wild raptors lEDS.],Biology of the Kinetoplastida.Vol. 1. Academic f. Am. Vet. Me& Assoc.187:1204-1205. Press, New York, NY U.S.A. PEIRCE, M.A., G.F. BENNETT AND M. BISHOP. 1990 BENNETT,G.F. 1961. On the specificityand transmis- The haemoproteidsof the avian order Falconiformes sion of someavian trypanosomes.Can. J. Zool. 39:17- f. Nat. Hist. 24:1091-1100. 33. SYKES,P.W., JR. ANDD.J. FORRESTER.1983. Parasites 1970. Trypanosomaavium Danilewsky in the of the snail kite in Florida and summaryof thosere- avian host. Can. J. Zool. 48:803-807. ported for the species.Fla. Field Nat. 11:111-116. -- AND M.A. PEIRCE. 1988. Morphological form TELFORD,S.R., JR. 1988. A contributionto the system- in the avian Haemoproteidaeand an annotatedcheck- atics of the reptilian malaria parasites,family Plas- DECEMBER 1994 RAPTOR BLOOD PARASITES 231

modiidae(: Haemospororina). Bull. Fla. District of Columbia and Patuxent ResearchRefuge State Mus. Biol. $ci. 34:65-96. vicinity. J. Parasitol.27:379-393. ^ND D.J. FORRESTER. 1992. Morphometric WHITE, E.M., E.G. GREINER, G.F. BENNETT AND C.M. comparisonsof the Plasmodium(Novyella) speciesre- HERMAN. 1978. Distribution of the hematozoa of portedfrom North American birds,with commentson neotropicalbirds. Rev. Biol. Trop. 26:43-102. a speciesfrom the barred owl ($trix varia Barton). WILLIAMS, N.A. aND G.F. BENNETT. 1978. Hematozoa System.Parasitol. 22:17-24. of somebirds of New Jersey and Maryland. Can. J --, M.G. S?ALDING•,ND D.J. FORP,ESTEP,. 1991. ZooL 56:596-603. Hemoparasites of wading birds (Ciconiiformes) in Florida. Can. J. Zool. 70:1397-1408. WETMORE,P.W. 1941. Blood parasitesof birds of the Received10 March 1994; accepted2 July 1994