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BLOOD PARASITES OF PRAIRIE ANATIDS AND THEIRIMPLICATION IN WATERFOWL MANAGEMENT INALBERTA AND SASKATCHEWAN

Authors: BENNETT, GORDON F., NIEMAN, DANIEL J., TURNER,BRUCE, KUYT, ERNIE, WHITEWAY, MADONNA, et. al.

Source: Journal of Wildlife Diseases, 18(3) : 287-296

Published By: Wildlife Disease Association

URL: https://doi.org/10.7589/0090-3558-18.3.287

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Journal of Wildlife Diseases Vol. 18, No. 3, July, 1982 287

a Present address: I)epartment of Preventive Medicine, University of Florida, Gainesville, Flonda 32610, USA.

BLOOD PARASITES OF PRAIRIE ANATIDS AND THEIR

IMPLICATION IN WATERFOWL MANAGEMENT IN ALBERTA

AND SASKATCHEWAN

GORI)ON I-’. BENNEVF,rn l)ANIEL J. NIEMAN,a HRU(’E ‘l’tTRNER,0 ERNIE KITYT,G MAI)ONNA

WHITE WAY,� and ELLIS C. GRELNER��

Abstract: Information on the blood parasites occurring in :3,866anatids of 14 species

collected from five locations in Alberta and Saskatchewan during 1976-80 is

summarized. An overall prevalence of 26% with avian hematozoa was recorded.

Leucocytozoon simondi was the most frequently encountered parasite, occurring in

17% of the ducks; Haemoproteus nettionis was observed in 11% of the birds while

Plasmodium circumfiexum and microfilariae (probably of Splendidofilaria

fallisensis) occurred in only 2% and <1% of the sample respectively. Overall

prevalence of infection in both imm�tures and adults was similar, although the

sample was heavily biased in favor of the immature age class. While the overallprevalence of L. simondi was similar in both age classes, H. nettionis occurred twiceas frequently in the adult birds. Infection prevalences of birds in the five geographicareas sampled were different and these differences are discussed. Prevalences alsodiffered from year to year in birds from the various areas and these differences areattributed, in part, to the water levels encountered each year. Leucocytozoon simondi

is considered a potentially limiting factor for waterfowl production in some areas ofnorthern Alberta and Saskatchewan.

INTRODUCTIONExtensive surveys of the blood

parasites of both breeding andoverwintering populations ofanseriforms have been made in variousparts of North America, especially alongthe Atlantic Flyway (Bennett, 1972;Bennett et al., 1974, 1975; Herman, 1968;Nelson and Gashwiler, 1941; Thul et a!.,1980). With the exception of a recentsurvey of the blood parasites of theanatids from central Alberta and theMackenzie delta (Williams et al., 1977)and a survey of the blood parasites inTrumpeter swans of Alberta (Bennett et

a!., 1981), few extensive surveys have

been carried out in Canada’s PrairieProvinces - a region noted for its water-fowl production. The lack of surveys inthis region is somewhat surprising as atleast one of the commonly occurringanseriform blood parasites, Leucocyto-

zoon simondi, can cause extensive mor-tality among flocks of domestic ducksand geese (Fallis and Bennett, 1966;Laird and Bennett, 1970; O’Roke, 19:34),

and has been cited as the major factorlimiting the success of Canada Geese inthe Seney National Wildlife Refuge innorthern Michigan (Herman eta!., 1975).It is thus strange that the possible role of

this particular parasite as a population

1)epartment of Biology and International Reference Centre for Avian Haematozoa, Memorial University of

Newfoundland, St. John’s, Newfoundland MB 3X9, Canada.

Prairie Migratory Bird Research Centre, 115 Perimeter Road, Saskatoon. Saskatchewan S7N llWl), Canada.

Canadian Wildlife Service, Western and Northern Region, #1000, 9942- 108 St., Edmonton, Alberta T5K 2,J5,

Canada.


288 Journal of Wildlife Diseases Vol. 18, No. 3, July, 1982

limiting factor in this area of high duckproductivity has not been previously in-vestigated as part of a waterfowlmanagement strategy.

The role of other blood parasites asfactors limiting anatid survival is lessclear, but experimentally, parasites suchas Plasmodium lophurae and P. cir-

cumflexum can cause mortality(Garnham, 1966). On the other hand,with the exception of a single report(Julian and Galt, 1980), Haemoproteusnettionis is not known to have lethaleffects (Bennett et al., 1976) and itspresence in an anseriform population,while doing it no conceivable benefit,may only serve to indicate the activityand/or density of the population of its

ceratopogonid vectors.

In 1976, cooperative projects were in-itiated with the Canadian Wildlife Ser-vice in both Saskatchewan and Alberta

to assess the prevalence of bloodparasites in the breeding anatid pop-ulations of the two provinces. This reportsummarizes the findings of the 5-yrstudy.

MATERIALS ANI) METHODS

Blood smears were obtained fromducks while they were being handledduring normal banding regimes, usuallyduring the month of August, andrepresented local breeding, moulting andpre-migration populations. The latterwere composed of either adults or im-

mature birds 8-10 wk of age. Waterfowlwere captured in clover-leaf wire trapswith funnel entrances baited with grain.Blood was obtained from the femoralvein along the tarso-metatarsus and thepreparation of blood smears in the fieldfollowed the protocols previously de-scribed (Bennett, 1970a). Followingcollection, the blood films were sent to theInternational Reference Centre forAvian Haematozoa (IRCAH) where theywere stained with Giemsa’s stain prior to

examination for blood parasites. TheIRCAH accession numbers for these

smears are as follows: 55377-56026;63146-63869; 63963-64140; 64206-64244;

66027-66109; 66292-69358; 70646-71188;73040-73481; 76768-77218; 77713-78030;80355-80377.

The ducks were obtained from twolocalities in Saskatchewan. The first was

the Corning-Heward region in theparkland of southern Saskatchewan, ap-proximately 100 km from the UnitedStates border. The area does not supporta large number of water bodies (lakes,rivers, streams) and is severely affectedby periodic drought. The second localitywas the Lake Lenore area (St. Brieux,Naicam), some 300 km north of the firstregion, in the east-central portion of theprovince. This area supports a muchlarger number of water bodies than theformer, with numerous tributaries of theSouth Saskatchewan and Carrot Rivers.The Lake Lenore region is one of the moststable in the province with respect toannual water conditions and is rarelyaffected by periodic drought. Anatidblood smears were obtained from threeareas in Alberta. The first was WoodBuffalo National Park in northeasternAlberta. The area is located on thenorthern edge of the mixed forest adja-cent to the Canadian Shield. Lakes,ponds and streams are abundant in thearea although the annual water regimecan be quite variable. Samples werecollected in Wood Buffalo National Parkin 1977, 1978 and 1979. The second areawas the Vermilion region, located some

160 km east of Edmonton. Vermilion issituated on the northern edge of thecentral Alberta parkland in an un-dulating to hilly moraine. The area isdotted with many potholes and lakes andis threaded by two permanent rivers andseveral seasonal streams. Blood sampleswere collected in the Vermilion area in

1976 and 1977. The third area sampledwas the Grande Prairie region located

some 380 km northwest of Edmonton.The region is somewhat unique in that itis an island of park!and isolated withinthe mixed forests of northern Alberta.



The area consists mainly of the rem-nants of a former till plain and is

characterized by an undulating to gentlyrolling terrain. Numerous lakes andseveral permanent rivers and seasonalstreams occur within the region. Bloodsamples were collected in this area in1979 and 1980. Chi square analyses weredone to determine the independence ofprevalence in relation to year, age and

location (Sokal and Rohlf, 1979).

RESULTS AND DISCUSSION

Approximately 3,870 anatids of 14species (Table 1) were examined for bloodparasites. The sample was primarily

composed of mallards (69%), pintails(13%), blue-winged teal (12%) and green.winged teal (3%), together totalling 97%of the sample. A total of 1,015(26%) ducksharbored one or more species of bloodparasites (Table 1). Leucocytozoon

simondi was the most frequently en-countered parasite, seen in 655 (17%)birds; H. nettionis was recorded in 442(11%) of the ducks while P. circumflexumwas seen in only 63 (2%) of the waterfowl.Microfilariae, probably those of

Splendidofilaria fallisensis (the onlyspecies recorded from Canadianansenforms [Anderson and Freeman,19691), occurred in 18 adult mallards, oneadult pintail and an adult green-wingedteal. Ten of the adult mallard infectionsoccurred in the Lake Lenore region ofSaskatchewan. Trypanosomes were notseen, but their absence was not con-sidered unusual as this parasite is rarelyencountered in anseriforms (Bennett,1970b; Herman et a!., 1971). A few

parasites were seen that could not beidentified. The combined total of the P.circumfiexum, microfilariae and uniden-tified parasites was less than 3% of thetotal infections; as these numbers were solow, these infections were not furtherconsidered. Prevalence of blood parasitesin the blue-winged teal was significantlylower than that observed in the green.winged teal (x2 = 72.1, df = 1, p<O.OO1)(Table 1). This observation is similar to

those made elsewhere (Bennett et al.,1975) and suggests that the blue-wingedtea! enjoys some sort of behavioral or

ecological immunity from blood protozoa(probably through some type ofreductioqin host-vector interaction) as the birdsthemselves are physiologically capableof sustaining infection.

The sample was weighted to immaturebirds (HY-Hatching Year) as this ageclass best illustrates transmission on thenatal areas and indicates the potential ofblood parasites as a mortality factor on a

susceptible waterfowl population.Among the 2,422 immature birdssampled, 557 (23%) were infected (Table

2); L. simondi was recorded from :386(16%) and H. nettionis from 211 (9%);mixed infections of both species wererecorded in 40 ducks. Among the 1,394adults examined, 414(305) were infected,with L. simondi occurring in 251 (18�i)

and H. nettionis in 209 (151�i); mixedinfections of both species occurred in 46ducks.

The immature ducks sampled wereunlikely to have travelled far from theirnatal areas, probably moving at bestfrom the small production ponds to thelarger “pre-staging” areas. In Sas-katchewan, the immature birds from

the Corning-Heward area showed anoverall prevalence of 7iXi, a prevalencesimilar to that of adults from the sameregion (9%). Immature birds from theLake Lenore region had an overallprevalence of 15%, about twice the levelin the Corning-Heward birds (x2 = :39.2,df= 1, p<O.OO1). However, the adultbirdsfrom the Lake Lenore area had a

significantly higher prevalence of 60%

(x2 = 309.5, df = 2, p <0.001), with all theadults examined in 1977 harboring oneor more species of blood parasites.Leucocytozoon simondi and H. nettioniswere present in approximately the sameproportions in both age classes of ducks,

although there was some variation fromyear to year (Table 2). Plasmodium cir-

cumfiexum was most commonly en-countered in waterfowl from the Lake


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TABLE 2. Haemoproteus nettionis and Leucocytozoon simondi infections in ana-tids from five regions of Saskatchewan and Alberta. (Table captions as in Table 1).

Total birds Infections with

no. no.examined infected infected H.n. L.s.

Corning-Heward, Saskatchewan

1977 HY* 99 11 11 2 9AHY* 253 11 4 7 4Total :352 22 6 9 1�3

1979 HY 244 14 6 10 5AHY 195 25 13 17 11

Total 439 :39 9 27 16

1980 HY 155 9 6 7 2AHY 186 19 10 13 6Total :341 28 8 20 8

Three-year total

HY 498 :34 7 19 16AHY 634 55 9 37 27

Total 11:32 89 8 56 4:3

Lake Lenore, Saskatchewan

1976 HY 151 27 18 11 19AHY 88 �35 40 17 29Total 239 62 26 28 48

1977 HY 11 11 100 1 10AHY 120 120 100 62 62Total 1�31 1:31 100 63 72

1978 HY 176 14 8 4 8AHY 165 69 42 :36 45

Total :341 8:3 24 40 53

Three-year total

HY :338 52 15 16 :37

AHY :37:3 224 60 115 136Total 711 276 :39 1:31 17:3

Wood Buffalo National Park, Alberta

1977 HY 60 22 :37 7 1:3AHY 5 5 100 1 5Total 65 27 42 8 iS

1978 HY 20 7 35 2 7

AHY 58 17 :30 3 15Total 78 24 31 5 22

1979 HY 58 29 50 7 27AHY S 4 50 2 2

Total 66 :3:3 50 9 29

Three-year total

HY 1:38 55 42 16 47AHY 71 26 :37 6 22

Total 209 84 40 22 69



TABLE 2. (continued)

Total birds Infectio

H.n.

ns with

L.s.no.

examinedno.

infected

�5

infected

Vermilion, Alberta

1976 HY

AHYTotal

303

67:370

81

:3211:3

27

4831

23

528

58

2684

1977 HYAHYTotal

43()47

477

11227

1:39

265729

268

34

762096

Two-year total

HYAHYTotal

7:3:3114847

19:359

252

265230

491362

1:3446180

Grande Prairie, Alberta

1979 HY

AHYTotal

389

79

468

152

26

178

39

3:3

38

8120

101

10:312

115

1980 BYAHYTotal

:32612:3449

682492

212021

:301848

498

57

Two-year total

HYAHYTotal

715

202917

220

50270

302529

1!!:38

149

15220

172

GRANI) TOTAL

HYAHY

24221:394

557414

23

:30211209(15)

386

251(18)

*HY : Hatching Year bird - i.e.- immature*AHY After Hatching Year bird - i.e. - adult

NOTE: Totals fur Saskatchewan regions consist of mallards, blue-winged teals andnorthern pintails only; totals for Alberta exclude Canada Geese.

Lenore area (21 of the 24 Saskatchewaninfections). The observations that theprevalence of blood parasites in the im-mature ducks of both regions was equalto or less than that in the adults wassurprising. In most other areas of NorthAmerica, the immature birds show thehighest prevalence of parasitism(Bennett et al., 1974, 1975; Herman, 1968;Herman et al., 1975; Laird and Bennett,1970; Nelson and Gashwiler, 1941; Thulet a!., 1980; Trainer et al., 1962).Presumably this situation arises from

the fact that the immature birds have notas yet developed immunity to parasiticinfections and thus are susceptible. Inthe Lake Lenore area, however, it ispossible that the simuliid vectors of L.

simondi and the ceratopogonid vectors ofH. nettionis are most active prior to thehatching of the birds of the year (thispoint should be established by co!!ec-tions of vectors in these areas) so that theducklings escape the majority of thetransmission season. That this may oc-cur in this region is highlighted by the



fact that the hatching peaks of mallardsand blue-winged tea! can be as much as 2wk later than their counterparts in the

Cormng-Heward area. This would implythat in the Lake Lenore area, transmis-sion is most active to 1-yr old and olderbirds. This situation would be of advan-

tage to the duck population as the olderbirds are presumably more able to resistthe effects of blood parasite infectionsthan newly hatched ones.

In Alberta, however, although L.

simondi occurred more frequently thanH. nettionis in all three areas, age classdifferences in prevalences were not con-

sistent among regions. Immature birdsshowed slightly higher prevalences in

the Grand Prairie and Wood BuffaloNational Park samples (x2 = 0.6, d.f. =1,p>O.O5; x2 = 2.74, d.f. = 1, p>O.O5 respec-

tively), whereas the adult componentwas more frequently infected in the Ver-

milion area (x2 = 30.5, d.f. = 1, p<O.OO1)(Table 2). The results from the Vermilionarea are similar to those observed fromthe Lake Lenore region and suggestagain that in these regions, the peakvector abundance precedes the peakduckling hatch. This could be a naturalphenomenon, but could also reflect ahigher re-nesting rate in zones of intense

agricultural activity, i.e. Vermilion andLake Lenore, than in the less disturbedhabitats to the north, i.e. Wood BuffaloNational Park and Grand Prairie.

In Saskatchewan, the overallprevalence of blood parasites in the

Cormng-Heward region during the years1977, 1979 and 1980 were remarkably

similar(x2 = 2.1, d.f. = 2, p> 0.05) (Table2). Variation from year to year wasstatistically insignificant(x2 = 2.1, d.f. =

2, p>O.O5). Prevalences in immature ver-sus adult birds during the same yearswere variable being signficantly

different in 1977(x2 = 6.4, d.f. = 1, p<O.O5)and in 1979 (x2 = 6.7, d.f. = 1, p<O.O5).Haemoproteus nettionis was the mostcommon parasite, occurring in 56 (63%)of the infected birds, while L. simondi

occurred in 43 (48%) (Table 2). The low

overall prevalence (8%) of bloodparasites, particularly L. simondi, might

be anticipated in this parkland regionwhere the absence of an abundance ofponds and streams, combined withsevere periodic drought, would con-tribute to a low vector population andhence reduced host-vector interaction

and transmission. Certainly, theprevalence of blood parasites in theducks of the extreme southeasterly por-tion of Saskatchewan is low in com-parison to other areas in Canada(Bennett, 1972; Bennettetal., 1975; Fallisand Bennett, 1966; Laird and Bennett,1970; Williams et a!., 1977), with theexception of those in the arctic tundra

(Bennett and Maclnnes, 1972). Hence

blood parasites may have little influenceon anatid populations in this part of

Saskatchewan, although a study of theblood parasites of 2 and 3 wk-old duckswould be necessary to confirm or refutethis hypothesis.

In contrast to the Corning-Heward

region, prevalence of blood parasites inanatids from the Lake Lenore region washigh (Table 2). In both 1976 and 1978, theoverall prevalence of parasitism in adultbirds was similar (x2 = 0.1, d.f. = 1,p>O.OS), but the infection in young birds

in 1976 was almost double that in 1978(x2= 7.4, d.f. = 1, p<O.Ol). In 1977, all birds

sampled were infected. No explanationfor these fluctuations is immediately ap-

parent. However, it is possible that either(i) a cold spring in 1976 synchronizedemergence of vectors with peak ducklinghatch or (ii) there was a greater success infirst nest hatching and a reduction in re-nesting, which would have operated tosynchronize duckling hatch and peakvector emergence. The high infection

rate in the Lake Lenore area is similar tothat observed in anatids in eastern NorthAmerica (Bennett et al., 1974, 1975; Her-man, 1968; Nelson and Gashwiler, 1941;Thul et al., 1980) and suggests a highhost-vector interaction, presumablythrough increased vector density. The

topography of the Lake Lenore area, with



numerous lakes, ponds and streams,together with a highly stable annualwater regime (similar to conditions seenin Vermilion, Alberta), favors the

breeding of vectors, especially simuliids.Higher prevalences of blood parasites,especially L. simondi, would be an-ticipated. The results indicate that L.simondi is the most frequently en-countered blood parasite in this region(Table 2) and it is in this region that one-half of the filarial infections (alsotransmitted by simuliids if they are S.fallisensis) and much of the mosquito-born P. circumflexum occurs. This alsosuggests that the Lake Lenore region has

a more diverse vector fauna than in theCorning-Heward region. Some of thehigh prevalence of infection in birds inthe Lake Lenore region is undoubtedlydue to birds which hatched in the “forestfringe” ecotone (a typically CanadianShield boreal forest area with a multitudeof fast-flowing streams) and stagedslightly further south in Lake Lenore.The immature birds in the Lake Lenoresample had a lower prevalence of bloodparasites than the adults from the same

region, but were nearly double the rate ofthe immatures from the Corning-Hewardarea. Nevertheless, the prevalence ofblood parasites in these immatures isstill low in comparison to similarbirds ineastern North America. Prevalence ofinfection in the adult ducks of the LakeLenore region is high in comparison tothose from the Corning-Heward area,and is fully comparable to the prevalencelevels recorded in this age class ofanatids elsewhere on the continent(Bennett, 1972; Bennett et al., 1974, 1975;

Herman et al., 1971; Laird and Bennett,

1970; Thul et al., 1950).

In Alberta, the prevalence ofhematozoa was highest in waterfowlfrom Wood Buffalo National Park (Table2), an area on the fringe of the CandianShield; 40% of the birds from this regionwere infected compared to 30% fromVermilion and 29% from Grande Prairie.Leucocytozoon simondi was the most

frequently encountered parasite, oc-curring in 33%, 21% and 19% of the birdsfrom Wood Buffalo National Park, Ver-milion and Grande Prairie respectively(Wood Buffalo vs. Vermilion x2 = 8.4, d.f.= 1, p<O.OO5; Wood Buffalo vs. GrandePrairie x2 = 9.1, d.f. = 1, p<O.OOS). Theprevalence of H. nettionis was one-thirdthat of L. simondi in both the Vermilionand Wood Buffalo National Park birds,but only marginally lower in the GrandePrairie sample. In all cases, theprevalence of H. nettionis was higher inAlberta waterfowl than in those fromSaskatchewan.

Annual infection rates were re-markably consistent in the Vermilion

area but varied widely in Grande Prairie.In fact, the prevalence of hematozoa inthe Vermilion sample varied marginallyfrom 31% in 1976 to 29% in 1977 (x2 = 0.2,d.f. = 1, p>O.O5), whereas in the Grande

Prairie birds the infection rate rangedfrom 38% in 1979to21%in 1980(x233.2,d.f. = 7, p<O.OOl). As water levels werecomparable in 1976 and 1977 but de-creased markedly between 1979 and1980, variations in the annual infectionrate may well reflect the amount of vectorbreeding habitat available. Hence the1980 drought conditions in GrandePrairie probably lowered the vector pop-ulation and reduced the potential for

parasite transmission. Though the smallsample sizes from Wood BuffaloNational Park renders comparisons of

annual infection rates somewhatspecious, it is noteworthy that fluc-tuations in prevalence of hematozoaadhere directionally to changes in waterlevels.

The elevated prevalence of hematozoain ducks from Wood Buffa!o NationalPark is largely attributable to the highprevalence of L. simondi in both ageclasses. That L. simondi occurs frequent-ly in birds from this area, as in the LakeLenore sample, is not surprising given itsproximity to the Canadian Shield en-vironment. In the Grande Prairie region

the prevalence of H. nettionis and L.


Journal of Wildlife Diseases Vol. 18, No. 3. July, 1982 295

simondi did not markedly differ,although in 1980 the infection rate ofeach species was reduced about 50% from

the previous year. As 1980 was ananomalous year of drought conditions,the 1979 results were likely more in-dicative of the hematozoan patterns inthis area. Nevertheless, the lowprevalence of L. simondi is enigmatic

considering the topography of the areaand the known occurrence of two provenvectors, Simulium (Byssodon) ruggelsi

and Simulium (Eusimulium) anatinumin watersheds only 100 km from GrandePrairie (Craig and Pledger, 1979). Thepattern of hematozoan occurrence in Ver-milion is similar to that observed in tfieLake Lenore area of Saskatchewan.

Leucocytozoon sirnondi was the mostfrequently encountered parasite and

both L. simondi and H. nettionisoccurred more frequently in adult thanimmature birds. As both areas arelocated in parkland and topographicallysimilar, the similarity of the results is notsurprising.

Though L. simondi occurs in a fairly

high percentage of the areas studied,with the exception of the Corning-

Acknowledgements

Heward region in Saskatchewan, it isnoteworthy that the prevalence of thisparasite in hatching-year birds increaseswith latitude north, as follows: 4i%i insouthern parkland (Corning-Heward);11% in central parkland (Lake Lenore);18% in northern parkland (Vermilion);21% in mixed forest (Grande Prairie); ;34i%i

in northern mixed forest (Wood BuffaloNational Park). Although this variableprevalence probably reflects the amountand suitability of vector habitat, it isfortunate that this situation exists as the

primary waterfowl breeding habitat islocated in the southern regions of theprairie provinces.

In general it would appear that ducks

in the Canadian Prairie provinces arenot subject to as high an attack rate byblood protozoans as their counterparts inthe northeastern portion of the conti-nent. Consequently, the impact of theseparasites on the waterfowl populations isprobably low. Nevertheless hematozoado occur in increasing numbers innorthern areas. In such areas bloodparasites, especially L. simondi, may be

an important but unrecognized cause ofmortality in duck populations.

We wish to acknowledge the technical and field assistance of R. Isbister, J. Smith,K. Godwin and S. Edmunds. The financial assistance of the Natural Sciences andEngineering Research Council of Canada, initially to E.C. Greiner and subsequentlyto the first author is gratefully acknowledged.

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ANDERSON, R.C. and R.S. FREEMAN. 1969. �ardiofilaria inornata (Anderson,1956) from woodcock with a review of the L�ardiofilaria and related genera(Nematoda: Filarioidea). Trans. Am. Microsc. Soc. 88: 68-79.

BENNETT, G.F. l970a. Simple techniques for making avian blood smears. Can. J.Zoo!. 48: 585-586.

1970b. Trypanosoma avium I)anilewsky in the avian host. Can. J. Zoo!. 48: 803-

807.

1972. Blood parasites of some birds from Labrador. Can. J. Zoo!. 50: 353-:356.

and CI). MACINNES. 1972. Blood parasites of geese of the McConnell River,N.W.T. Can. J. Zoo!. 50: 1-4.


296 Journal of Wildlife Diseases Vol. 18, No. 3. July, 1982

E.C. GREINER and W. THRELFALL. 1976. Impact of parasitic diseases onwildlife: Protozoans. In: Wildlife Diseases. L.A. Page (ed). Plenum Press, New

York, pp. 25-33.

B. TURNER and G. HOLTON. 1981. Blood parasites of Trumpeter Swans, Olorbuccinator (Richardson), from Alberta. 3. Wild!. Dis. 17: 213-215.

W.W. BLANI)IN, H.W. HEUSEMANN and A.G. CAMPBELL 1974.Hematozoa of the Anatidae of the Atlantic Flyway. I. Massachusetts. J. Wild!.Dis. 10: 442-451.

A.!). SMITH, W. WHITMAN and M.F. CAMERON. 1975. Hematozoa of theAnatidae of the Atlantic Flyway. II. The Maritime Provinces of Canada. J. Wildl.

Dis. 11: 280-289.

CRAIG, I).A. and D. PLEI)GER. 1979. A contribution to the population dynamics ofbiting flies in the Swan hills area of boreal forest. Report to the Minister of theEnvironment, Province of Alberta, April, 1979. 70 pp.

FALLIS, AM. and G.F. BENNETT. 1966. On the epizootio!ogy of infections causedby Leucocytozoon simondi in Algonquin Park, Canada. Can. 3. Zool. 44: 101-112.

GARNHAM, P.C.C. 1966. Malaria Parasites and Other Haemosporidia. B!ackwe!lScientific Publications, Oxford, England. 1,114 pp.

HERMAN, CM. 1968. Blood parasites of North American waterfowl. Trans. N. Am.Wild!. Nat. Resour. Conf. :3:3::348-:359.

J.H. BARROW and lB. TARSHIS. 1975. Leucocytozoonosis in Canada Geeseat the Seney National Wildlife Refuge. J. Wild!. Dis. 11: 404-411.

J. 0. KNISLEY JR. and GD. KNIPLING. 1971. Blood parasites of wood ducks.J. Wildl. Manage. :35: 119-122.

JULIAN, R.J. and I).E. GALT. 1980. Mortality in Muscovy I)ucks (C’airina moschata)caused by Haemoproteus infection. J. Wild!. Dis. 16: 39-44.

LAIRD, M. and G.F. BENNETT. 1970. The subarctic epizootiology of Leucocytozoonsimondi. J. Parasitol. 56 (sect. 2): 198.

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Received for publication 28 September 1981


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