THE SPECIES OFHAEMOPROTEUS. LEVCOCYTOZOONAND TRYPANOSOMA OFTHE AUSTRALIAN HONEYEATER FAMILY MEUPHAGIDAE(AVES: PASSERIFORMES) GORDONF BENNETT,DEBORAH SQUIRES-PARSONSANDTARMOPOLDMAA Bennett,G. F, Squires-Parsons, D.&Poldmaa, T 1994 1201: ThespeciesofHaemoproteus, Leucocyiozoon and Trypanosoma of the Australian honeyeater family Meliphagidae (Aves: Passerifarmes).MemoirsoftheQueenslandMuseum37(1): 13-18.Brisbane. ISSN0079-8835 TheavianhaematozoanspeciesofHaemoproteus, LeucocyiozoonandTrypanosomaoccur- ringintrieAustralianHoneyeaterfamilyMeliphagidae.firstdescribedin 1909and 1910,are re-described using modern criteria. The confusion surrouQnding the systematic position of these parasiteswhenthey werefirstdescribedisresolved. Meliphagidae,Haemoproteus, Leucocyiozoon, Trypanosoma, Queensland, avian haematozoa. G.F Bennett<fc D.Squires-Parsons, InternationalReference CentreforAvianHaematozoa and Department of Biology* Memorial University of Newfoundland, St, John\s, New- foundland, Canada, AJB3X9; T. Poldmaa, Deportment ofBiology, Queen's University, Kingston. Ontario, Canada. K7L3N6; 28July 1994. Clcland & Johnston (1909) described andthusgavetheopportunitytore-describethese Haemoproteus ptilotis, H. philemon and parasitesusingmodemcriteriaandevaluatetheir H. meliornis from the meliphagids Ptilotis systematicposition. 1= Meliphaga) chrvsops, Philemon cornhuUitus andMeliornis(=Phylidonyris)novaehollandiae, MATERIALS AND METHODS whichtheycollectedbyshootingatMilsonIsland inthe Hawkesbury Riverandin Sydney. In 1910 they described Trypanosoma anelloinae from Blood samples from 173 Noisy Miners Anellabia (= Anthochaera) chrysoptera which {Manorina melanocephala) in three locations in Queensland (Laidley, Wivenhoe Dam and was collected near Brisbane, Queensland. They Toohey forest) were collected via jugular obtained further samples ofa numberofspecies venipuncture during the period 1990-1993. A of meliphagids from the environs of Eidsvold, Queensland and in 191] they identified blood smear from each sample was prepared in Trypanosoma anellobiae from Myzomela san~ thefield, air-dnedand fixed inethanolwithin 12 hours. Smears were then sent tothe International guiniolenta, Ptilotis (= Melipkaga) fusca, En- Reference Cenlre for Avian Haematozoa tomyzon cyanoris and Myzaniha garrula (now (TRCAH) where they were re-fixed in 100% Manorina melanocephala). In 1911, they methanolandstained withGiemsa'sstainatapH described and illustrated what they called the 7.2 and examined for parasites. Forty-five hirafl "intracorpuscular' or '"Leucocyiozoon'" stage of were infected with species of Haemoproteus, Trypanosomaanellobiaeandpresentedadiscus- Leucotyiozoon and Trypanosoma and an addi- sionofhow thisstagewaspartofthe lifecycleof tional seven bird* were infected with Plas- the trypanosome However, the illustrations modium voMghtoi, which constitutes the first clearly indicate a species of Leucocyiozoon Australian recordofthis parasite. Johnston (J912)referredtoLeucotytozoonunci- Thebloodparasiteswere drawn with theaidof tobiae in a table and inadvertently established a a camera lucida and rhe morphomctric specificdesignation. parameters were determined with the aid of a Clearly, there is considerable confusion sur Zeiss MOP-3 Digital Analyser. The parameters rounding the identity of the avian haematozoa for the haemoproteids were measured by the described by Clcland & Johnston from the protocols established by Bennett & Campbell Meliphagidae. In 1990-93, a large sample of (1972)asmodifiedbyForresteretal.(1977).The Noisy Miners (Manorina melanocephala) from parameters used for the icucocytozoids werees- Laidlcy, Wivcnhoc Dam and the Toohey Forest tablished by Bennett et al. (1991). The mor- ofQueenslandwereexaminedforbloodparasites phometricparametersandderivedindicesforthe during the course ofa study of Iheirmating and trypanosomes follow the generally accepted social systems. These birds were infected with measurements for this group (Woo & Barileu, HaetnoproJeas. Leucocyiozoon and Trypanosoma 1982). All measurements are presented as the MEMOIRSOFTHEQUEENSLANDMUSEUM 14 mean with thestandarddeviation in parentheses. mentofthecell throughtheactionoftheparasite AJ1 photomicrographs were taken with a Zeiss (Bennett et al., 1990:194), vacuoles not Photoscopc III. In the re-descriptions of the prominent and volutin granules notseen. haemoproteids and leucocytozoids,themeasure- MterogameiocyrefFig, IB).N= 10.Microgarnelo- ments for the males arc not presented in the cytesclosely similar to macrogametocytes in all interests of brevity However, if the dimensions dimensionsexcept forthelargerparasitenucleus are markedly different from those ofthe macro- typical of the microgametocytes of all the gameiocyte, these arc mentioned in text- apicoraplexan parasites: parasite nucleus central Through the courtesy ofDr Penny Bcrcnts of with volutin granules concentrated at the poles the Australian Museum in Sydney, the original and notoccupyingtheareaoccupied by the large material used by Cleland & Johnston was made parasitenucleus. available forstudy. BasisofRedescript; TAXONOMIC REVIEW Blood films 115027 and 124757 from Noisy Miners Mannrina meianocephala collected by Poldtuaa in Haeiuoproteosptilotis (Cleland & Johnston, Qtoubeeerns1l9a9n0d,anAdusWtiravlcinahforeoDmaTmooohney6 SFoerpetsetmboenr71O9c9-2 1909)emend. Coatney, $36 respectively, TypeHost Comments Ptilotis ihn.ujps (Latham), now AMiphaga Haemoprotei4s ptilotis is a small, haltchdial chrysops[Lnihdm) hacmoproteid that occupies less than 60% ofthe host cell-parasite complex. It has lew and rather TypeLocality small pigment granules. It is considered to he a Milson island. Hawkcsbury River, New South distinct species on the basis of its occurrence in Wales. the family Meliphagidae, following the u&sump- tion that hacmoprotcids arc host family or sub- Uninfected erythrocyte*. N = 25 Erythrocyte family specific (Bennett 8c Peirce, 1988), 12.1 (0.8)p.min length,6.1 (0.6)\im in widthand Hacmoproteus ptilotis fits the description 58.1 (7,41pm2 in area; erythrocyte rhUcteDS 5.2 presented byCleland & Johnston (1909)as far tt (0-5)Mm in length. I 9 i,0.2>Mm in width and 7.7 can be followed. The illustrations presented by il-2)jim2 inarea. these authors are essentially the same as those Immature gametocytes. Youngest forms seen figuredincludingthefew,smallpigmentgranules were Usually lateral to Ihe erythrocyte nucleus, per parasite, The measurements presented by but sometimes inapolarposition; margin entire. Cleland & Johnston lie well within the range of Macrogamttocyte (Fig. IA). N =35. Infected thosepresentedabove, Unfortunately,the hapan- erythrocyte 12.8 r l.0)u;m m length (6% hyper- totypefcotypeofCleland&Johnston, 1909)slide trophy),7.1 (0.6)fiminwidth(\6% hypertrophy; ofH.ptilotishad degraded beyond use. Not only and 72.0 (8.6);im2 in area (24% hypertrophy); had the stain faded but the eiythrocytes themsel- infected erythrocyte nucleus 5.1 (0.6)u.m in ves weredisintegrating and noparasitescould be length (2% atrophy), 2.1 (0.3)ttm in width (10% distinguished at any place on the blood film. In hypertrophy) and 8.5 (L5)|im in area (10% hy- essence, the existing hapantotype slide is worth- pertrophy). Parasite ha'teridial, entire in outline lessandonly theoriginal desciiplion and illusita- and occupying 58% ofthe area of the host (.ell- tions ofthe species remains todefine it. parasite complex. Parasite somewhat sausage- Cleland & Johnston (1909), using the generic shaped, 12.1 (l.2)|im in length, &5 (0fV)|jm in designation of Halicrithu/ri, subsequently width at the middle of the parasite and 41.8 emended by Coatncy in 1936 to Haemoprotvus, (6.4)jinT* in area, parasite nucleus ovoid to round also described H&emoproteus philemon from in outline, median in position, 2.2 (O.l)Lim in Philemoncorniculatusand their illustrationsand length, 1.4(0.1)lJm in width and 2.4 (0,7)jinr in dimensions of the parasite in this bird are essen- area; pigmentgranules average 10 (1.7) granules tially the same as the description for H. f>lttOtU y per parasite, small and scattered randomly including the small parasite with tew pigment throughout parasite cytoplasm; erythrocyte granules.Theymentionthatalthougha fewofthe nucleus only slightly displaced laterally, NDR parasites of//, philemon were larger than (hose t(hNeucNlDeaRrrDeipsrpelseanctesmtehnetdReagtrieoe)o=fl0a.t6er(a0l.d2i)spwlhaecree- doefteHc.tepdtialnotdist,he*i\de.ntliittytleordoitfhfeerrweinsceeocfotuhledtwboe , HAEMATOZOA OFAUSTRALIANHONEYEATERS IS must await the investigation of other stages in broadly ovoid and sometimes elliptical. 4.0 their life histories" (Cleland & Johnston, (0.5)|lm \n length, 2.8 (0.5)p,m in width and 82 1909:R4). They also described Haemoprttfeus (|.9)p;nr in area, without a marled karyov.-n. meliornis from Meliornis (= Phylidonyris) occupying 9,7% of the area of the parasite; novaeholtandiae. This bird hadan intense infec- vacuoles small and not prominent; volutin tion with many erythrocyteshaving multiple in- granules not seen; nucleus of hosl cell-pardsik* vasion of parasites. Their illustrations of this complex usually as a ribbon but sometimes as a parasite indicate many ofthe parasites were im- cap, 23 1 (8.7)pjrC in area and covering 14,9 mature, but thematureformsare unquestionably f4.8)jim of the periphery of the parasite (44%) the same as H. ptilotisand the dimensions ofthe and occupying 21% ofthe area of the ru«t cell- cells arc within the range of those cited in the parasite complex; host cell-parasite complex redeseription above. Regrettably, the hapan- 108,5 (22.6)nnr in area. totypc slide of H. meliornis is in equally poor Micmgamesocytt {Fig. ID). N = 14. Microgameto- shape as thatofH. ptiiotis and nothing could be cyte similar to the macrogametocyte in most seenon thesmearexceptdisintegratingcells that respects except for the usual larger nucleus and had lost their stain and the slide is essentially pale staining that occurs in Ihe apicomplex.in worthless The blood film of H. philemon was parasites. The microgametocyte on average is fortunatetohavebeencovcr-slippodwithCanada 5-10% largerinrnosi dimensionslhan ihemacro balsam and the cells on the smear were intact gametocyte and the host cell-parasite nucleus is although badly faded. As described originally, larger and covers a greater amount of ihe this smearcontained cells with uptofourimma- periphery ofthe parasite (66% compared to4Z% ture parasites. However, only two mature forthe macrogametocyte), parasites were seen and these, as far as could be determined given the lack ofstaining, appeared to be similar to their illustrations in 1909 and to Basisofdescription those used in the re-description above. Although Harwtotypl: Blood film no. 1 15021 fromManama the hapantotypc slidesofthese parasites are use- melunovephuki collected by PoldmaaatToohey Fotcst, less for laxonomic purposes, on the basis of the QPuaekeanshlaaknadnotnot7yOpchtso.beBrl1o9o9d0.film no. 8872 from the bd01eysi.cCtriliienablleaddnedsfc&rroipmJtoithohnnesstmaoennldi(lp1i9hn0ae9gd)i,rdasawlilbnytghsrCelpeerlesaspneendctiee&ds NbBloeoninnsedytftMiliamtnneKocrnMm12ua4in7eo,1nQnfunaemeimnesilhhramnsodacmeeenphs1pueSkceiipetsceocmlobllleeecrctteiedd%&bby,v Johnston arc the same species. Bv page priority PoldmaaatWivciirHjcDanuQuccnslandon 15July 1992 (1CZN, Section 69B (II)), therefore*. llaemoproteus ptilotis is the name of the Comments haemoprotenl in the Meliphugidae and Haemoproteus phitemon and Haemoprotewt This isasmall round leucocytozoid. one ofthe meliornis fall as synonyms smallestofthespeciesdescribed. It isconsidered to be a distinct species on the basis of the Leucocytozoon andlobiae (Cleland & presumed familial/subfamilial specificity Johnston, 1911)emend. Johnston, 1912 demonstrated for a numher of species of Leucocytozoon (Bennett eta)., 1991). Bennett & de Swardt (1989) believed that Leucucytozmm TypeHost ancilohiac also occurred in the South African Thelittlewattlebird.Anthochaeraehrysoptera Gurncys sugarbird {Hrornerops gurneyi) which (Latham). was al thai lime classified as a meliphagid. How- ever, this genus is now believed to have little or TypeLocality norelationshipwith ihe Australian Meliphagid.tr Brisbane, Queensland. Australia and has been placed in its own family, the Promeropidae (although some authorities con- Macrogametocyte (Fig. 1C). N = 51. Parasite sider them to be in the subfamily Promeropinae with round rnorphs only. Parasite broadly ovoid oftheMeliphagidac). Oncomparisonofthesugar 10 round, with a maximum diameter of 11.3 bird material with that from the Australian noisy (1.6'tyim, minimum diameter of 9.5 (0.9)jim. a miner, it was evident that the South African periphery of 33.1 (3,5)|im and an area or 85.4 species was much larger and that Bennett and de (I5.6)(im*,occupying80%oftheareaofthehost Swardt( 1989)wereinerror.Therefore,theSouth cell-parasite complex; parasite nucleus round to African leucocytozoid was described as MEMOIRS OFTHEQUEENSLANDMUSEUM 16 Leucocytozoon deswardti by Bennettetal. (1992). & Cleland Johnston(1910) described Trypanosoma anellobiae from Anellobia (—Anthochaera)chrysoptera and in 191 1, elaborated on this parasite with remarks based on finding this trypanosome in several % other species of the Meliphagidae. They were also convinced that the "Leucocytozoon" stage was theintracorpuscularstageof the trypanosome life cycle, a commonly held view at thetime.Thisviewmayhave been prompted by observa- tion of the highly fusiform FIG. I.A,Haemoproteusptitotis,twomacrogametocytes;B,Haemoproteusptiiotis, microgamclocytc;C,Leucocytozaonanellobiae,macrogamelncytc;D,Leucocytozoon (almost trypanosomc-like) anellobiae,microgamclocytc;E,Trypanosomaanellobiae. appearance ofLeucocytozoon ziemanni of owls, birds "Leucocytozoon* stage was described and are which arc frequently concurrently infected with birds from the type locality. bothparasites.Johnston(1912)referredinatable toLeucocytozoonanellobiae.Thefootnotetothis Trypanosomaanellobiae specific name reads 'The name Leucocytozoon & Cleland Johnston, 1910. anellobiaeisheregiventoabloodparasitefound by Dr. Cleland and myselfin several species of birds.Webelieveittobeaphaseinthelifehistory TypeHost of Trypanosoma anellobiae (Cleland & Thelittle wattlebird,Anthochaerachrysoptera Johnston).Ihaveusedtheabovenameaspossess- (Latham). ing specific value. Should our opinion as to the specificidentity ofthetwoformsbecorrect,then TypeLocality the name L anellobiae becomes a synonym, or, Brisbane. Queensland,Australia. tobemoreexact, itrefers toaparticular phaseof T anellobiae" Thus Johnston inadvertently Trypomastigote (Fig. IE). N = 6. Trypomas- created Leucocytozoon anellobiae as a valid tigote small andslender, averaging 25.6(2.3)^m species. Whether inadvertent or not, the name inlengthand5.7(0.9)(j.m in width at theposition stands as the valid designation of the of the nucleus. Kinetoplast 2 7 (0.8)jtm from leucocytozoidofthe Australian meli&phagids and posteriorend and 9.7 (0.6)|xm from the nucleus. is herein so recognised. Cleland Johnston Nucleus 12.3 (0.8)fim from the anterior end (1910) did not indicate the disposition of the which has a long free flagellum averaging material used to define the "Leucocytozoon* 10.8(im (only two free flagellae measured). stage of Trypanosoma anellobiae. However, Trypomastigote 82.0 (12.7)|im* in area, nucleus when Johnston (1912) created Leucocytozoon 15.6 (3.5)|im2 in area, the nucleus representing anellobiae, he was in the Department ofBiology 19%oftheareaoftheparasite.Thedistancefrom oftheUniversityofQueensland.Thereisnotrace the posterior end to the kinetoplast represents ofthis material atthe Queensland Museumoron 10% ofthe length ofthe trypanosome, while the record at other Australian institutions as faras is distance of the centre of the nucleus from the known(LesterCannon,pers.comm.). Inasmuch posteriorendis48%ofthe lengthoftheparasite, as that no "type" material was designated for L thenucleusapproximately atthemid-pointofthe anellobiae, we are designating hapantotype and trypomastigote. The width ofthetrypanosome at parahapantotype slides from Manorina the centre ofthenucleus is 22%- ofthe length of melanocephala, one ofthe hosts from which the the organism. , HAEMATOZOA OFAUSTRALIANHONEYEATERS n BasisofDescription T. anellobiae is remarkably similar to T. on- Blood film Nu. 115082 from Manorina tarioensis Woo and Barllett, 1982. Both rnelanocepkala collected by Poldmaa al Toohey trypanosomes are small, slender and with the Fores*.Queenslandoo 18October 1990. kinetoplast located close 10 the posterior end; COMMENTS measurements cited herein lie within the ranges quotedby Woo& Bartlett fortheirspecies.Both Cleland & Johnston (1910) described species have a long free flagellum that is about Trypanosoma anellobiae from Anellobia one-half the body length and the derived ratios chrysoplcra (now Anthochaera ckrysoptera) are essentially the same. It would be essentially from a bird shot at Brisbane. Queensland. The impossible W separate the two species on the infectionwaslightandtheirdescriptionindicates basis of their morphometries and appearance. that the trypomasrigote was about 0.035mm in Trypanosoma ontarioensis was originally lengthwithamaximumbreadthof0.002mm.The described from a corvid in Ontario, Canada but "kinetonucleus*" was situated0.003mrn from Ibe its appearance is similar to the numerous small posteriorend. They couldnot see the nucleus of trypanosomes that have been inadequately rtieorganism andthey didnoldejectafreeflagel- described from South American birds and many lum. They concluded thai the undulating of these South American trypanosomes can un- membranewas very narrow and believed it to be doubtedly beassigned10thisspecies.Inadditu% short. Their illustrations (Plate xxxiv, figs 6, 1 1) T ontarioensis has been recorded from Sweden arcclearly thoseofthetrypanosomeillustrated in and appears to have a broad distribution. Fig. IE of this study. The measurements they Trypanosoma ontarioensis is a readily cultured presented are closely similar to those presented trypanosome,doingpartkularly wellondiphasic herein, especially whh respect 10 the position of blood-agarmedium,producing infcctivcculturcd thekinetoplast. Itisclearthat the trypanosomein forms in two weeks. While the isolation of theNoisy Miner is the same as thatdescribed by Cleland & Johnston. The hapantoiype slide of Australia would suggest that T. anellobiae is a Trypanosoma anellobiae was examined and distinct species and no attempt will be made to fouudtobeinthesameconditionasdescribed for synonymizethetwospeciesalthis lime, theclose the hapantoiype slides ofHaemoprateus/>/ similarityofthetwospeciestoeachotherrequires and H. metiornis. Only a few oftheerythrocytes experimental confirmation oftheir identity. were intact and the stain had faded to the extent This study has also highlighted what will be- that the blood smear was a nsottOCQlOuX The come .» major problem for museums and blood smear was reported to also contain two repositories of hapantoiype material of the species of microfilariae However, no trace of Protozoa. The hapantoiype material of the these parasites could he found. The hinod smear Cleland &Johnston species were 84-85 years of »s unacceptable as the basis for definition nf a age and had deteriorated to the extent they were taxon. of no value as the basis for the definition ofthe On the basis of the original description, taxons they were supposed to represent. It is Trypanosomaanellobiae is asmall trypanosome almost 90 years since the first edition of the that lacks the striated appearance and largersize International Code forZoological Nomenclature ofthe 7. avium group; it is alsoeasily separated was published and the practice of establishing from T. paddae* T. corvi and T. hannai on the type material became mandatory although \\\k basis of its much smaller size and distinctive material had frequently been designated decades derived ratios. It is smallerthan T. bouffardi but before. Stained protozoal and similar material shares the same slender appearance of this trypanosome and also differs in that the doesage with time andas indicated in this studj kinetoplast is much closer to the posterior end. in 85 years had deteriorated beyond use. While The length of T. anellobiae is within the same the use oi covers!ips and mounting media docs range as T. vvereltt, and the placement of the aid in thepreservationof(hecells,theproblemof kinetoplast is similar in both of these species stain fading over a long period still occurs. The However, T, everetti is a broader trypanosome preservationofhapantoiypematerial willbecome (which gives the organism a "stumpy" ap- 8 senous problem that will have to be addressed jn*arance)with4nucleusthat occupies atxiui26% hycurators ofthis typeofmaterial and shouldbe of ll>e area of the trypomastigotc and cannot be addressedas a priority bythe International Com- confused with T anellobiae. On the other hand. mission forZoological Nomenclature. MEMOIRS OFTHEQUEENSLANDMUSEUM 18 ACKNOWLEDGEMENTS CLELAND,J. B.&JOHNSTON,T.H. 1909. Descrip- tions ofnew haemoprotozoa from birds in New South Wales, with a note on the resemblance The financial support of the Natural Sciences between Lhe spermatazoa ofcertain honeyeaters and Engineering Research Council ofCanada to (Fam. Meliphagidae) and spirochaete- both the first and last authors is gratefully ac- trypanosomes. Journal oflhe Proceedings ofthe knowledged. RoyalSocietyofNewSouthWales43: 75-96. CLELAND. J. B. & JOHNSTON, T. H. 1910. The LITERATURECITED haematozoaofAustralianbirds. - No. I.Transac- tions ofthe Royal Society ofAustralia 34: 100- BENNETT, G. F. &CAMPBELL, A. G. 1972. Avian 114. Haemoproteidae.1. DescriptionofHaemoproteus CLELAND. J. B & JOHNSTON, T. H. 1911. The fallisin. sp. andareviewofthehaemoproleidsof haematozoaofAustralianbirds, No. II.Journalof thefamilyTurdidae.CanadianJournalofZoology the Proceedings of the Royal Society of New 50: 1269-1275. SouthWales45: 415-444. BENNETT, G. E, EARLE, R. A. & PE1RCE, M. A. COATNEY,G.R. 1936.Acheck-listandhost-indexof 1992. The leucocytozoidac of South African thegenusHaemoproteus.Journal ofParasitology birds: the Passeriforms. OnderstepoortJournal of 22:88-105. BENNHVEeUTteCTr.HinZaGEr.yRRMR,eEsYEeaAErRRcLh,E5,9F:.R2W.3.5A-.&2,47PS.EQIURICREE,S-MP.AAR.-, FORR&7E.SKAT1EGrReA,vYiDEe.,wJ.Mo,f.GtRMh.EeT1hN9aE7e7Rm..oApEvr,ioalCen.iHdBasEemNoofNpEtrhToetTef,iadmGai,el.Fy SONS, D. 1991. Avian Leucocytozoidae: the Ciconiidae (storks) and descriptions of leucocytozoids of the Phasianidae sensu lato. Haemoproteusbrodkorbi sp. nov. and H.peircei BENNJEoTurTn,alG.oFf.Na&tuPrEalIRHCiEst,oMry.2A5.:11948087.-M1o4r2p8.hologi- s1p2.74n.ov. Canadian Journal ofZoology 55: 1268- cal form in the avian Haemoproteidae and an INTERNATIONAL CODE OF ZOOLOGICAL annotated checklist of the genus Haemoproteus NOMENCLATURE. 1985. (International Trust Kruse, 1890.JournalofNaturalHistory22: 1683- 16%. forZoological Nomenclature in association with BENNETT, G.F., PEIRCE, M. A. & EARLE, R. A. British Museum (Natural History) London). 1990.Thehaemoproleidsoftheshrikesof(hethe JOHNSTON, T. H. 1912. Internal parasites recorded avian family Laniidae (Passeriformcs). South fromAustralian birds. Emu 12: 105-112. AfricanJournal ofZoology 25: 194-198. WOO, P. T. K. & BARTLETT, C. M. 1982. BENNETT, G.F. & DE SWARDT, D. H. 1989. First Trypanosoma ontarioensis n. sp. and 7". paddae African record of Leucocytozoon anelhbiae from Corvus brachyrhynchos in Ontario.Canada (Apicomplcxa: Leucocytozoidae) in Gurney's with notesonthebiologyofT. ontarioensisn.sp. sugarbird, Promeropsgurneyi. Ostrich60: 171. CanadianJournal ofZoology 60: 2107-2115.