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,
Collegeof VeterinaryMedicine,
Universityof Florida, Gainesville,FL 32677 U.S.A.
GORDON F. BENNETT
InternationalReferenceCentrefor Arian tiaematozoa,Memorial Universityof Newfoundland,
St. John's,Newfoundland,A 7B 3X9, Canada
ABSTRACT.--Fifteenspeciesof bloodprotozoansand an unidentifiedmicrofilariawere foundin thin blood
films from 55 strigiformsand 138 falconiformsexaminedin Florida. All four of the speciesof strigiforms
sampledwere infected,with an overall hemoparasiteprevalenceof 63%, excludingnestlings.Sevenof 11
speciesof falconiformssampledwere parasitized,with a prevalenceof 33%, excludingnestlings.Mixed
infectionsof two or more speciesoccurredin 28 birds, 22 had two speciesof hemoparasites,three had
three species,and three had four species.Among the infectionsof hemoparasites,
Haemoproteus
species
were mostcommon(67%), followedby Plasmodium
(22%), Leucocytozoon
(9%), Trypanosoma
(1%), and
microfilariae(1%). A Plasmodium
(Novyella)sp., previouslyknown only from a barred owl (Strix varia)
in Georgia,was presentin the greathornedowl (Bubovirginianus),
baldeagle(Haliaeetus
leucocephalus),
and broad-wingedhawk (Buteoplatypterus)in Florida. The identificationof Leucocytozoon
ziemanniis
the first recordof this speciesin barn owls (Tyto alba) from North America and Trypanosoma
confusum
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 protozoos
sanguineos
y una "microfilaria"fueronencontrados
en delgados
frotis de sangreobtenidosen 55 Strigiformesy 138 Falconiformesde Florida. Las cuatro especiesde
Strigiformesmuestreadasestabaninfectadasconuna prevalenciadel 63% de hemopar/tsitos,
excluidoslos
polluelos.Sietede 11 especies
de Falconiformesmuestreados
estabanparasitadosconuna prevalenciadel
33%, excluidoslos pollos.Infeccionesmezcladasde doso m/rsespeciesafectarona 28 aves,tres tenlan
cuatro especiesde par•isitos.Entre las infecciones
por hemoparSsitos,
Haemoproteus
fue la especiem•is
comfin(67%), seguidode Plasmodium
(22%), Leucocytozoon
(9%), Trypanosoma
(1%) y micofilariae(1%).
Plasmodium(Novyella)sp., previamenteconocidos61opara Strix varia en Georgia, estabapresenteen
Bubovirginianus,
tialiaeetus
leucocephalus
yen Buteoplatypterus
enFlorida.La identificaciGn
deLeucocytozoon
ziemanni,es el primer registrode estaespecieen Tytoalba presenteen America del Norte. Trypanosoma
confusumes reportadopor primera vez en Strix varia.
[TraducciGn de Ivan Lazo]
Strigiformsand falconiformsare prominentcomponentsof the avifauna of Florida, yet their blood
parasitesare poorly known. We are aware of only
three publicationsdealingwith this topicin Florida.
Greiner et al. (1981) reporteda parasiteresembling
Plasmodiumpolare in a bald eagle (Haliaeetusleucocephalus);
Sykesand Forrester (1983) examined
data with informationon parasiteinfectionsof raptors from other geographicareas.Somehostrecords
in the presentpaper have been includedalso in a
brief and limited format in a host-parasitecatalogue
(Bishopand Bennett 1992) and in a taxonomicreview of the haemoproteids
of falconiforms(Peirceet
al. 1990).
bloodfilms from 19 snail kites (Rostrhamussociabilis)
without finding hemoparasites;and Dooris et al.
(1981) found no blood parasitesin 30 burrowing
owls (Speotytocunicularia).
The objectives
of the presentstudywere to determine the speciesand prevalenceof bloodparasites
presentin raptorsin Florida, and to comparethese
226
METHODS
We obtainedbloodfilmsfrom 55 strigiforms(four species)and 138 falconiforms(11 species)from 1973-91. All
birds sampledwere fledgedjuveniles or adults with the
exceptionof 44 bald eaglesand one eastern screech-owl
(Otusasio) which were nestlings(<8 wk of age). Exact
ageswere not known.Of the 147 fledgedraptorsfor which
DECEMBER
1994
RAPTOR
BLOOD
PARASITES
227
we have preciselocality information(the localitywas unknown for one eagle), 121 were from northern Florida
(localities north of Manatee, Polk, Osceola, and Brevard
counties) and 26 were from southern Florida (localities
south of the above listed counties).
Thin blood smearswere prepared from cardiac or peripheral blood,fixed in absolutemethanol,and stainedby
standardGiemsa techniquefor 1 hr at pH 7.0, or in the
22 had two species,three had threespecies,and three
had four species.
An apparentlyundescribedPlasmodium(Novyella) specieswas seenin three birds: a great horned
owl (Bubovirginianus),a bald eagle,and a broad-
buffer at pH 6.4 for 1.5-2 hr (Kimsey 1992). Material
obtainedfrom the Collegeof Veterinary Medicine, Universityof Florida, was comprisedof coverslipsmearsthat
had been stained by the Wright-Giemsa method. Slides
were examinedat 400 x to determineprevalencesof parasites.Measurementsof parasiteswere done with a cal-
cruciform, measured 3.5-4.5 x 2-4 •tm and were
winged hawk (Buteoplatypterus).Gametocytesof
this parasitehad notably crenulatemargins. Schizcase of fixed but unstained slides which had been stored
for severalmonths,by Giemsa in an acidicacetone-based ontswere tiny with four nuclei,were fan-shapedor
ibrated ocular micrometer under oil immersion (1000 x ).
The taxonomiccharactersused for identificationof par-
asiteswerethoseutilizedby Telford (1988) for Plasmodium
species,by Forrester et al. (1977), Bennett and Peirce
(1988), Peirceet al. (1990), andBishopandBennett(1989)
for Haemoproteus
species,by Greiner and Kocan (1977)
and Bennett et al. (1991) for Leucocytozoon
species,and
by Baker (1976) and Telford et al. (1991) for trypanosomes.Statisticalcomparisonsof samplemeanswere made
by Student'st-test, and of sample proportionsby chisquare (a = 0.05).
Representativeblood films have been depositedin the
found in mature erythrocytes.
DISCUSSION
The samePlasmodiurn
(Novyella)speciesreported
from a barred owl (Strix varia) from southern Geor-
gia by Telford and Forrester(1992) is reportedhere
from three additional
hosts. The characteristic
schiz-
ontswere commonin the greathornedowl, very rare
in the bald eagle, and absentin the broad-winged
hawk.
Identification
of the infection
in the latter host
was basedupon a high proportionof gametocytes
which had irregular or crenulatemargins.
Greiner et al. (1981) reported the presenceof
distinctivegametocytes
with crenulatemarginsin a
collection of the International
Reference Centre for Avian
bald eagleinfectedby parasitesresemblingP. polare,
Haematozoa, Memorial University, St. John's, Newbut were uncertainwhether they representeda sepfoundland (AccessionNos. 68665, 116415-116441, and
arate taxon or were possiblysenescent.We were
125553-125556).
able to study blood films from the bald eagle exRESULTS
amined by Greiner et al. (1981). The gametocytes
Hemoparasiteswerefoundin all species
of raptors with crenulatemarginswere the mostcommonform
examinedexceptthe black vulture (Coragypsatra- presentin a ratio to thoseof P. polare that exceeded
tus),turkeyvulture( Cathartes
aura),osprey(Pandion 50:1, which would argue against senescence.Dishaliaetus),and merlin (Falcocolumbarius)(Table 1). coveryof a few tiny schizontssimilar to thosefound
The 44 nestling bald eaglesand the one nestling in the barredowl from Georgia(Telford and Forreseasternscreech-owlwere negativeand were not in- ter 1992) and the great horned owl (this paper)
eludedin statisticalanalysesor comparisons
because providedadditional evidenceof their conspecificity
of their young age and becausenestlingswere not with this undescribedspecies.These probably are
•ncludedin the samplesof other species.Overall, not immature schizontsof P. polare becausein this
strigiformsshoweda significantlygreaterprevalence species,nuclear division does not begin until the
of hemoparasites
than did falconiforms(63 vs. 33ø70, trophozoitesare nearly twice the size of the Plaschi-square,P < 0.01).
rnodiurn(Novyella)sp. schizonts.The identification
Haemoproteus
specieswere most common(67%), of P. polare-likeparasitesin the bald eagleby Greifollowedby Plasmodium
(22%), Leucocytozoon
(9%), ner et al. (1981) is appropriate,giventhe paucity of
Trypanosoma
(1%), and microfilariae (1%). Fifty- data available for this speciesof Plasrnodiurn.
We haveidentifiedthe haemoproteidfrom eastern
eight infectionswere found in strigiforms:44 Haetooproteus(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-owls
were 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 trypanosomes
or microfilariae.Mixed infec- have been due to strain differences or host effects,
tions of two or more speciesoccurredin 28 birds: but further studiesare needed.Both H. syrnii and
228
FORRESTER
ETAL.
VOL.28, NO. 4
DECEMBER 1994
RAPTOR BLOOD PARASITES
229
Table 2. Prevalences
of the commongeneraof bloodparasitesin raptorsfrom North Americaand the Neotropical
region.
PERNUMBER
CENT
OF BIRDS
POSI-
EXAMINED
TIVE
pa
Hb
Lc
Td
SOURCE
51
7
4
17
0
9
21
7
56
73
18
37
7
2
12
+e
3
4
2
0
+e
Greiner et al. (1975)
Williams and Bennett (1978)
This study
Olsen and Gaunt (1985)
White et al. (1978)
3
0
23
33
21
9
1
11
0
8
22
26
14
19
43
8
9
3
0
1
0
0
2
Greiner et al. (1975)
Williams and Bennett (1978)
Kirkpatrick and Lauer (1985)
This study
Olsen and Gaunt (1985)
White et al. (1978)
PERCENT
POSITIVE
FOR
Strigiformes
North
America
Maryland-New Jersey
118
28
18
Florida
54
63
Louisiana
34
68
Neotropics
44
25
Falconiformes
North
America
Maryland-New Jersey
New Jerseyareaf
309
33
40
33
249
59
93
33
Louisiana
21
24
Neotropics
119
30
Florida
1
Plasmodium.
Haemoproteus.
Leucocytozoon.
Trypanosoma.
Prevalencesnot givenby author.
New Jersey,Pennsylvania,
Delaware,andVirginia.
H. noctuae
havebeenreportedpreviouslyfrom east- muliid vectors by falconiformsbecauseof their
ern screech-owls(Bishopand Bennett 1989).
broaderranges,in comparisonto the moresedentary
Trypanosoma
confusum
is known from severalstri- strigiforms.It is possiblealsothat strigiformbehavgiforms (Bennett et al. 1982, Bishop and Bennett ior patterns(foragingat night and using secluded,
1992), but has not been reportedpreviouslyfrom shadyperchesduring day) exposethem more frethe barredowl. An unidentifiedtrypanosomefound quently to a variety of vectorspecies(and hencea
by Wetmore(1941) in thebarredowl wasprobably larger variety of hemoparasites)than do those of
T. confusum.
Although Baker (1976) hasdefinedthe falconiforms(daytime activity period and elevated
trypanosome from the New World as T. confusum, perchesat night).
theparasiteismorphologically
indistinguishable
from
The overall prevalenceof Plasmodiumspeciesin
Trypanosoma
avium of Old World strigids.Bennett
both strigiforms and falconiforms in Florida was
(1961, 1970) showedthat the trypanosomeorigi- greaterthan that recordedin other comparablesurnating from the northern saw-whet owl (Aegolius veys(Table 2). These prevalencesprobablywould
acadicus)
couldbetransmittedvia themosquitoAedes have been even higher if isodiagnostictechniques
aegypti to a number of different avian speciesof
severalordersand families, thus indicating a total
lack of hostspecificity.Measurementsand derived
•ndicesfromtrypanosomes
fromOld andNew World
borealowls (Aegoliusfunereus)
are identicalto those
from the northern saw-whetowl and the two species
of trypanosomes
are likely to be synonymous(G.
Bennett unpubl. data).
Falconiforms
wereparasitizedmorecommonlyby
Leucocytozoon
than were strigiforms.This may reflect a greater opportunity for contactwith the si-
had been used since Plasmodium
infections
in birds
are knownto virtually disappearfrom the circulating
blood when infections become chronic (Herman et
al. 1966). Haemoproteus
specieswere alsomore common in strigiformsin Florida than in other areas
exceptLouisiana(Olsen and Gaunt 1985), but in
falconiformstheir prevalencein Florida was similar
to the overall estimate for North America (Greiner
et al. 1975) and the Neotropics(White et al. 1978).
Leucocytozoon
species,however, had a lower prevalencein strigiformsfrom Florida than generallyin
230
FORRESTERET AL.
North America (Greiner et al. 1975) or on the eastern seaboard (Williams and Bennett 1978). In fal-
VOL. 28, NO. 4
list of the genusHaemoproteus
Kruse, 1890. J. Nat
Hist.
22:1683-1696.
, M. WHITEWAY AND C. WOODWORTH-LYNAS
coniforms,Leucocytozoon
specieshad a lower prev1982. A host-parasitecatalogueof the avian haemaalencein Florida than reportedin the North Amertozoa.Mere. Univ. NewfoundlandOcc.Pap. Biol. 5, St.
xcansurvey (Greiner et al. 1975) and the 1985
John's, Newfoundland, Canada.
New Jerseysurvey(Kirkpatrick and Lauer 1985), --,
R.A. EARLE,M.A. PEIRCE,F.W. HUCHZERMEYER
but was comparableto that foundin the 1978 MaryANDD. SQUIRES-PARSONS.
1991. Avian Leucocytoland-New Jersey survey (Williams and Bennett
zoidae:the leucocytozoids
of the Phasianidaesensulato
1978) and the Louisianasurvey(Olsenand Gaunt
J. Nat. Hist. 25:1407-1428.
1985). Leucocytozoon
speciesare presentin the Neo- BISHOP, M.A. AND G.F. BENNETT. 1989. The haemoproteidsof the avian order Strigiformes.Can. f. Zool
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mation on prevalences.The data on Trypanosoma
AND-1992. Host-parasitecatalogueof
from all areassurveyedmay be misleadingbecause -the avianhaematozoa,
Supplement1 andbibliography
of the inefficiencyin detectinginfectionsby using
of the avianblood-inhabiting
haematozoa,
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and if culture
methods
had been examined
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ACKNOWLEDGMENTS
FORRESTER,
D.J., E.C. GREINER,G.F. BENNETtaND M.K.
KIGAYE. 1977. Avian Haemoproteidae.7. A review
We thankNoha Abou-Madi andRamiroIsazafor providing accessto raptors in the Wildlife Clinic of the Vetof the haemoproteids
of the family Ciconiidae(storks)
erinary Medical TeachingHospitalat the Universityof
anddescriptions
of Haemoproteus
brodkorbi
sp.nov.and
Florida. Vicki L. Clydepreparedsomeof 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. ANDA.A. KOCAN. 1977. Leucocytozoon
ClinicalPathologyfiles.We appreciate
their cooperation.
(Haemosporidia;Leucocytozoidae)
of the FalconiDyanneD. Singlergaveus access
to raptorsat The Conformes. Can. f. Zool. 55:761-770.
servancyin Naples,Florida. Petra B. Wood suppliedus
D.J. BLACKAND W.O. IVERSON. 1981. Plaswith slidesfrom nestlingbald eagles.Ellis C. Greiner --,
modiumin a bald eagle (Haliaeetusleucocephalus)
in
generouslypermitted us to include someof his material
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from bald eaglesin our sample,and both he and Martin
D. Youngreviewed
themanuscript.
Marilyn G. Spalding --,
G.F. BENNETT, E.M. WHITE AND R.F. COOMBS
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an earlydraftof themanuscript
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Received10 March 1994; accepted2 July 1994