Cooper Ornithological Society
Scarcity of Haematozoa in Birds Breeding on the Arctic Tundra of North America
Author(s): Gordon F. Bennett, Robert Montgomerie, Gilles Seutin
Source: The Condor, Vol. 94, No. 1 (Feb., 1992), pp. 289-292
Published by: University of California Press on behalf of the Cooper Ornithological Society
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SHORT COMMUNICATIONS
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The Condor 94:289-292
? The Cooper Ornithological Society 1992
SCARCITY OF HAEMATOZOA IN BIRDS BREEDING ON THE
ARCTIC TUNDRA OF NORTH AMERICA'
F. BENNETT
GORDON
InternationalReferenceCentrefor AvianHaematozoa,Memorial Universityof Newfoundland,
St. John's, Newfoundland,AJB 3X9, Canada
ROBERT MONTGOMERIE
AND GILLES SEUTIN2
Departmentof Biology, Queen's University,Kingston,Ontario,K7L 3N6, Canada
Key words: Haematozoa;tundra;arctic;parasites; American arctic-nestingbirds. In a review of haematozoanprevalencein NorthAmericanbirds,Greiner
longspur;ptarmigan;redpoll;plumage color.
et al. (1975) indicatethat less than 3%of birdssampled
Despite widespreadinterestin documentingthe blood from the "arcticbarrens"(their region 6) were paraparasitesof birds (e.g. Loye and Zuk 1990), there is sitized, but they provideno furtherinformationon the
little informationavailableon the haematozoaof spe- sample of birds involved in this analysis.
In this paper, we reporton the haematozoafound
cies occurringin arctic regions.Laird(1961) reported
that none of the 149 individualsof 23 bird species he in 276 breedingbirds of 10 species sampled in the
sampled on Prince of Wales Island (72-740N, 96- courseof field studiesof theirbehaviorand ecologyat
1030W)duringone summerharboredhaematozoa,but four very differentarctic sites. While some of these
no other intensive surveys have been done of North species have been sampledfor haematozoabefore,our
samples allow us to comparehaematozoaprevalence
betweenhabitattypes, both within and betweensites.
' Received 24 June 1991. Accepted 27 September We also discuss the implications of our findingsfor
recent comparativeanalysesof parasiteprevalencein
1991.
2
Present address:Departmentof Biology, Univer- relation to plumage brightness in birds (see Moiller
1990).
sity of Pennsylvania,Philadelphia,PA 19104.
290
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TABLE 1. Prevalenceof Haemoproteus(H), Leucocytozoon(L) and Trypanosoma(T) in tundra-nestingbirds.
Site
Species
SarcpaLake
Lagopusmutus
Eremophilaalpestris
Calcariuslapponicus
Plectrophenaxnivalis
Churchill
Carduelisflammea
Carduelishornemanni
Carduelissp.
Calcariuspictus
Zonotrichialeucophrys
St. Paul Island
Aethiapusilla
Fort Simpson
Cygnusbuccinator
Total
Percent
Total individuals
Examined
Infected
39
3
29
8
0
0
0
0
97
19
6
19
4
63
12
1
3
4
14
0
38
276
25
108
39.1
METHODS
Birds were capturedopportunisticallyin a variety of
ways (mist nets, noose carpets,noose poles and potter
traps),oftenin conjunctionwith otherresearchon their
behaviorand ecology. All individualswere bandedto
facilitatelateridentification.Blood smearswere made
followingthe protocolsof Bennett(1970). All smears
were air-driedin the field and fixed in 100%ethanol
within 24 hr. At the InternationalReferenceCentrefor
Avian Haematozoa,smearswere stained with Giemsa's stain and examined for Leucocytozoon,Trypanosoma and microfilariaat 250 x and for Haemoproteus
and Plasmodium at 400 x magnification.Each slide
was examined until approximately100,000 erythrocytes had been scanned.In this paperwe mainlyreport
parasiteprevalence,i.e., whetheror not eachindividual
wasinfectedwith eachof thesetaxa.Parasiteintensities
(i.e., infestationlevels perindividualbird)tend to vary
seasonallyand among age and sex cohorts (Weatherhead and Bennett 1991) and are thus not very useful
in interspecificcomparisonsunlessthese factorscan be
statisticallyor experimentallycontrolled.
Most of our sampleswere collectedat SarcpaLake,
Melville Peninsula, Northwest Territories(68033'N,
83019'W) during June and July 1987-1989 and at
Churchill,Manitoba(58045'N,94005'W)duringJune
and July 1989. The habitat at SarcpaLake is upland
high arctic tundra (see Montgomerieet al. 1983 for
details), more than 1,000 km north of the northern
limit of treesat this longitude(Danks 1981).Churchill,
on the otherhand,is on the arctictreelineat the northern edge of the forest-tundra/openborealforest vegetation zone (see Fig. 3 in Danks 1981). All birds captured at Churchillwere breedingwithin 5 km of the
Hudson Bay coast, either on relatively open tundra
with scatteredclumps of black spruce(Picea mariana
(Mill.) BSP) or within the spruce stands themselves
(see Jehl and Smith 1970 for habitatdetails).
H
Individuals with
L
T
8
0
0
0
0
53
12
1
3
3
10
2
0
0
1
18
26
9.4
8
80
29.0
0
13
4.7
We also reporton blood samples collected in June
and July 1987 fromLeastAuklets(Aethiapusilla) nesting on St. PaulIsland,PribilofIslands,Alaska(57008'N,
170017'W)and in July and August 1989 from Trumpeter Swans (Cygnusbuccinator)nesting on the Mackenzie River nearFortSimpson,NWT (620N, 1220W).
These two samplespermitcomparisonwith those from
relatedspecies reportedelsewhere.St. Paul Islandis a
small oceanicislandin the BeringSea, well beyondthe
arcticlimit of treesand tall shrubs,whereasFortSimpson is at the southernedge of the forest-tundra/open
forestvegetationzone (see Danks 1981),about 500 km
southwestof the arctictreeline.
At SarcpaLake, Churchilland on St. Paul Island,
all blood smearsweretakenfromadultbreedingbirds;
at Fort Simpson,they weretakenfrom 25 adultbreeders and 13 goslings.Adults of both sexes were represented in all samples except Horned Larks(females
only).
RESULTSAND DISCUSSION
Sarcpa Lake, NorthwestTerritories.No haematozoa
were found in the 79 individualbirds of four species
sampled at SarcpaLake (Table 1). Both Rock Ptarmigan (Lagopusmutus)and LaplandLongspurs(Calcarius lapponicus)were sampled duringthe breeding
season in three differentyears; nine individual Rock
Ptarmiganandtwo individualLaplandLongspurswere
sampled in more than one year. Thus, the absence of
haematozoain breedingbirdsat this site appearsto be
a generalphenomenon.
Forty-threeindividualsof the same fourspeciesalso
were sampled by Laird (1961) in a single season on
Princeof WalesIslandand no haematozoawerefound
there either.HornedLarks(Eremophilaalpestris)and
Rock Ptarmiganalso nest south of the northernlimit
of trees where haematozoahave been found in their
of 50 Rock Ptarmiganfrom insularNewblood--36%
SHORT COMMUNICATIONS
foundland harboredhaematozoa (Bennett and Inder
1972) and 13%of 23 Homed Larksfrom St. Bride's,
Newfoundlandand False River, Ungava Bay, Quebec
had either Leucocytozoonor Haemoproteus(unpublished data, see Greineret al. 1975). Thus, the absence
ofhaematozoain thesespecieson the higharctictundra
is not a species-specificphenomenon,but ratherseems
to be site-related.
The complete absence of avian haematozoa from
birds nestingin high arcticregionsis almost certainly
due to the absence of suitable vectors (see also Laird
1961, Greineret al. 1975), especiallythe various species of ornithophilicblackflies (Simuliidae;see Danks
1981). The fact that haematozoahave been found in
both Homed Larksand Rock Ptarmigannestingsouth
of the arctictreelinesupportsthis argument.The four
birdspeciessampledat SarcpaLakealso wintermainly
in the northern half of North America where there
would be no active vectorsfor haematozoain the winter. Thus, the only potential vectors for haematozoa
that they might have encountered on the breeding
grounds are mosquitoes (Culicidae).Mosquitoes are
not particularlycommon at SarcpaLake,but it is also
possible that arctic species do not act as vectors for
avian haematozoa.
Churchill,Manitoba.Haematozoanswere found in
at least some individualsof all four passerinespecies
sampledat Churchill(Table 1). Leucocytozoonfringillinarumwas found in all four bird species, Trypanosoma aviumin all but the longspur,and Haemoproteus
macropigmentatusand H. chlorisonly in the two redpolls. Parasiteintensitieswere low 10 infectedcells
(_except seven inper 100,000 examined) in all birds
dividual redpollsthat had up to 500 infectedcells per
100,000 examined.
Parasite prevalencewas highest (63-100%) in the
three species that primarilyoccupy treed habitatsand
nest mainly within the treeline: the White-crowned
Sparrow(Zonotrichialeucophrys)and the two redpolls
(Carduelisflammeaand C. hornemanni;Table 1).The
prevalenceof haematozoain these speciesat Churchill
is similarto levels reportedforotherspeciesfromthree
localitieswithin the borealforestzone: Lac Kohlmeister, Quebec (60% of 129 birds of 29 species; Laird
1961);ChurchillFalls, Labrador(61%of 140 birds of
21 species;Bennett 1972);and insularNewfoundland
(48%of 209 birds of 3 tetraonidspecies;Bennettand
Inder 1972). Given the abundanceof potentialvectors
in treed habitatsat Churchill(pers.obser.),it is likely
that haematozoa were picked up on the breeding
grounds.
Smith's Longspurs(Calcariuspictus),which nest on
the ground in more open forest-tundrahabitats (Jehl
1968), had a significantlylower prevalenceof blood
parasites(16%)than each of the otherthreepasserines
sampledat Churchill(Table 1; G-tests with William's
correction,Gadj = 9.0-15.9, P < 0.01, df = 1 in each
case). Since the redpollsand White-crownedSparrows
mainly nest in or among black sprucetrees (Jehl and
Smith 1970),this differencein parasiteprevalencesuggests that even when vectorsfor a parasitesare present
in the generalvicinity,microhabitatcharacteristics
may
be importantin parasitetransmission.Thus, the constantlywindy conditionsin the more open tundrasites
inhabitedby Smith'sLongspursprobablyreducestheir
291
exposureto biting flies comparedto sympatricspecies
occupyingmoreshelteredhabitats.A similarargument
was madeby Laird(1961) to explainthe low prevalence
of parasites in several Charadriiformespecies when
compared to sympatricallybreedingspecies of other
avian ordersat Lac Kohlmeister,Quebec.However,it
should be noted that the Charadriidaein generalare
seldom infected with blood parasites-only 1.2%of
individualsin this family, sampledin North America,
had haematozoa (Greineret al. 1975) and it is not
known whether this is due to microhabitator some
parasiteresistancein this taxon.
Fort Simpson, Northwest Territories.Twenty-five
adultTrumpeterSwans(Cygnusbuccinator)weresampled near Fort Simpson, of which 19 (76%)were infected with haematozoa:L. simondi, H. nettionisand
H. greineri.At this boreal forest site, six (46%)of the
13 goslingssampledwerealso infectedwith L. simondi
and H. greineri, indicating that suitable vectors for
thesehaematozoawerepresenton the breedinggrounds
and that transmissionoccurredthere.
The prevalence(66%;Table 1) of blood parasitesin
swans from Fort Simpson is similar to that observed
in seven other anatid species at Goose Bay, Labrador
(where 48% of 56 individuals were infected;Bennett
1972),anothersite withinthe open forest/forest-tundra
zone in the borealforest(Danks 1981).This is in sharp
contrastto haematozoaprevalencerecordedfromSnow
(Chen caerulescens)and CanadaGeese (Brantacanadensis) in the delta of the McConnell River, NWT
(60050'N, 94025'W),where only 3% (21/736) of the
geese examinedwere infected (Bennettand MacInnes
1972). The McConnellRiver delta is on the open tundra about 200 km north of the treeline.This suggests
thatthe scarcityof haematozoaat the McConnellRiver
is attributableto the absenceof vectors there.
St. Paul Island,Alaska.None of the 14 LeastAuklets
(Aethia pusilla) sampled harbored any haematozoa
(Table 1).This is consistentwith the findingof Greiner
et al. (1975) who recordedno haematozoain fourother
species of alcids from the north temperatezone. We
can again attributethe absence of haematozoain the
Alcidae, in general,to the absence of vectors in their
nestinghabitaton windy, treelessoceanicislandsor at
sea.
CONCLUSIONS
We conclude from this study that blood parasitesare
virtually absent in bird species nesting on the open
tundra.Althoughthe evidencepresentedhereindicates
thatthis patternis due to the absenceof suitablevectors
on the treelesstundra,this hypothesiswill need to be
tested criticallyby actuallysamplingvectors(see Bennett 1960 for suitablemethods). It is possible, for example, that tundra-nestingbirds are eitheravoided by
suitable vectors or are more resistantto parasiteinfection than forest-dwellingspecies. This seems unlikely becausetwo speciesthat we studied(Rock Ptarmiganand HornedLark)havehaematozoain the boreal
forest zone but not on the arctictundra.Similarly,at
Churchill,there was a strikingdifferencein parasite
prevalenceacross species between habitatsoften separatedby only a few hundredmeters. Thus, neithera
species-specificdifferencein parasiteresistancenor a
differencein vector behaviordue to climate appearto
292
SHORT COMMUNICATIONS
be able to account for the scarcityof haematozoain
tundra-nestingbirds.
Combinedwith previouslypublishedwork, the resultsof our studysuggestthatbirdsnestingon the arctic
tundraand on small oceanicislandstypicallylackhaematozoa. Among passerinebird species, in particular,
only those populations nesting on the arctic tundra
have been found consistentlywithoutblood parasites.
Ourresultsalso have implicationsforanalysesof the
relationbetweenblood parasitesand plumagebrightness in birds. For the past decade, there has been intense interest in the hypothesis (Hamilton and Zuk
1982) that femalebirds might use male plumagecolor
as an honest signal of parasite resistance.Hamilton
and Zuk (1982) predicted,and found, a positive relation between blood parasiteprevalenceand plumage
brightnessacross North Americanpasserines.Subsequentworkershave foundevidenceboth forandagainst
this prediction(see Moller 1990 for review).Ourstudy
indicatesthattundra-nesting
speciesshouldnot be used
in any comparativetests of the Hamliton-Zukhypothesis becauseinter-and intraspecificvariationin plumagecolor in these speciescannotbe relatedto variation
in parasiteprevalenceor intensity.Thus, plumagedifferencesbetween male Horned Larks(dull), Lapland
Longspurs(brighter)and Snow Buntings(brightest)as
well as intraspecificvariation in the plumageof both
male and female Lapland Longspurs(Montgomerie,
unpublisheddata)cannotbe explainedby haematozoa
infestations.
Our analysesalso suggestthat not only the presence
of vectors,but also theirrelativeabundancein different
microhabitats(see Greineret al. 1975), may influence
parasite prevalenceboth within and among species.
Vector abundancehas so far not been taken into account explicitlyin tests of the Hamilton-Zukhypothesis and could potentiallyaccountfor some of the apparentcorrelationswith plumagebrightness.
WethankJimBriskie,KarenHolder,IanJones,Adele
Mullieand Len Shandruckfor providingblood smears
from theirstudyspecies.This studywas fundedby the
CanadianWildlifeService(to Len Shandruckworking
at FortSimpson)and grantsfrom the NaturalSciences
and EngineeringResearchCouncil(to GFB and RM),
the ScientificTrainingGrantsProgramof Indian and
NorthernAffairsCanada(to RM andGS),the National
GeographicSociety (to Ian Jones workingon St. Paul
Island),the FrankM. ChapmanFund and the A. B.
Kelly Fund of the Provinceof QuebecSociety for the
Protectionof Birds (both to GS).
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