The Auk 114(2):179-191, 1997
AN
ALTERNATIVE
OF BRIGHTLY
HYPOTHESIS
COLORED
FOR HEAVIER
BIRDS:
PARASITE
EXPOSURE
AT THE
LOADS
NEST
MARYC. GARVIN
1 ANDJ.V. REMSEN,
JR.
Museumof NaturalScience
andDepartment
of ZoologyandPhysiology,
Louisiana
StateUniversity,
BatonRouge,Louisiana70803,USA
ABSTRACT.--Hamilton
and Zuk (1982)proposedthat bright plumagein birdsevolvedas an
advertisement
of parasiteresistance
in responseto heavyparasiteloads,and they predicted
that sexualdichromatism
shouldbe stronglycorrelatedwith parasiteloadsacrossspecies.
To
testtheir hypothesis,we sampled935 individualsof 19 speciesof passerinebirdsin Louisiana
for the presenceof bloodparasites.Nest height,a variablegenerallynot considered
in most
recentliteratureon the Hamilton-Zuk hypothesis,was as good or bettera predictorof parasiteprevalenceas was sexualdichromatism
or plumagebrightness.
Because
certainornithophilic vectorsare mostcommonin the canopy,the relationshipbetweennestheightand parasiteprevalencemay follow from the naturalhistoryof parasitism.Ecological
conditionsmay
influenceblood-parasite
loadsin the speciesstudied,suggesting
that geneticallybasedresistanceis lessimportant.If parasitevectorsaremorecommonin the canopy,thenmorecolorful
bird specieswill be more heavily parasitized,on average,than lesscolorfulspecies,because
bird speciesthat live high in the treestend to be morecolorfulthanthosethat live closerto
the ground.Received
18 July1994,accepted
14 August1995.
The
data
available
to
Hamilton
and
Zuk
HAMILTON
ANDZUK (1982)predictedthat bird
specieswith strongplumagedichromatismalso
will havethe highestprevalenceof parasiticinfection.They indicatedthat specieswith heavy
parasiteburdenshave undergonestrongselection for ways to advertiserelative healthiness,
suchas by evolutionof bright plumage.They
proposedthat males of suchspecieswould experience strong sexual selection, generating
strongsexualdimorphismin plumage.Hamilton and Zuk's specificprediction was that
"those[species]with mostevidentsexualselection are most subjectto attack by debilitating
parasites."Their review of data on blood parasitesin 109 speciesof North American passerines revealedthat bright plumage was positively associated
with prevalenceof bloodparasites,a finding consistentwith predictionsof
their hypothesis.They concludedthat although
"alternativeexplanations
for their resultscould
be offered,"their resultssuggestedthat genetic
complication is that sexual dimorphism in
plumageis not evenlydistributedbetweenmigratory and sedentarybird groups,or among
phylogeneticgroups.
We tested the Hamilton-Zuk hypothesisby
comparinglevels of blood-parasiteprevalence
in 19 speciesof North American birds, while
controllingfor seasonaland geographicvariation in parasiteburden.We also examinedanother variable, nesting stratum, that has not
variation
been used in most other tests of the Hamilton-
for
disease
resistance
contributes
to
(1982) did not allow them to assessseveral vari-
ablesthat could affectthe prevalenceof parasites,suchas geographicand seasonal
variation
in parasitedensityand diversity(Bennettand
Cameron 1974, Weatherhead et al. 1991). Fur-
thermore,Hamilton and Zuk did not analyze
migratoryand sedentaryspeciesseparately;certainly,thosespeciesthat winter in the tropicsare
exposedto a differentarray of arthropodvectors (Manwell
and Herman
1935). A further
sexualselectionand evolutionof bright plum-
Zuk hypothesis,althoughits potentialsignificanceto parasiteburdensof birds was suggestedand testedmore than 30 years ago by
Bennettand Fallis (1960).Specifically,birds are
thoughtto acquireinfectionsof bloodparasites
• Presentaddress:
VectorBiological
Laboratories,primarily on their breeding grounds from
Departmentof BiologicalSciences,
Universityof Notre blood-feedinginsects(Janovy1966). Nestlings
age.
of altricialbirds, nearly defenseless
due to their
incomplete feathering and poorly developed
Dame, Notre Dame, Indiana 46556, USA.
E-mail:[email protected]
179
] 80
GARVINANDREMSEN
[Auk, Vol. 114
motor control,are especiallyvulnerableto such pairs of congenersand, in the two caseswith a third
insects (Scott and Edman 1991, and references
species
in a familyor subfamilywith a pair of conge-
therein).Consequently,Bennettand Fallis (1960)
ners (i.e. Turdinae, Icteridae). Our treatment of fami-
proposedthat the prevalenceof bloodparasites liesandsubfamiliesreflectsnomenclaturethat will ap-
pear in the forthcoming7th editionof the AOU Check-
in birds was influencedstronglyby nest height. lisL
Becauseornithophilic biting flies, including
FromMarch throughJune1988,thin bloodsmears
ceratopogonids,culicids,and simuliids, show were collected in Louisiana from 935 individuals of 19
verticalfeedingstratification,with mostvectors passerinespeciesrepresenting
eightfamiliesand suboccurringin mid-canopy(Snow 1955, Bennett families(Appendix1; seealsoGarvin1989).The spe1960, Anderson and DeFoliart 1961, Bennett and
Coombs1975,Henry and Adkins 1975),Bennett
and Fallis (1960) reasonedthat canopy-nesting
bird speciesmay be exposedto higher concentrationsof potentialvectors.Bennettand Fallis'
data supportedthis hypothesis,with the high-
est incidenceof infectionfound in speciesthat
nestin the canopy.
Theoutcomeof theanalysisof prevalence
levels of blood parasitesprompted us to expand
our interspecificcomparisonsto two other
groupsof birdsto explorethepotentialrelationship betweennesting and foraging strata and
plumagebrightness.
ciessampledwerechosento spanthe rangein plumage brightness,sexualdimorphism,and nest height
availableamonglocal speciesfor which reasonably
large samplesizescouldbe obtained.By restricting
analysesto thosespeciesfor which we couldobtain
relatively large sample sizes, we avoided the bias
causedby small samplesizes,as found by Read and
Harvey(1989),pruett-Jones
etal. (1991),andChandler
and Cabana(1991).The rangein samplingdateswas
lessthan30 daysfor all excepttwo species,
Carolina
Wren (Thryothorus
ludovicianus)
and Northern Cardinal (Cardinalis cardinalis), whose blood smears were
collectedover a period of 70 days.Therefore,potential problemswith within-yeartemporalvariationin
parasiteprevalence(Kirkpatricket al. 1991;Weatherhead and Bennett1991, 1992) were minimized. Approximatelyequalnumbersof malesand femaleswere
analyzedfor all targetspecies,and no hatching-year
METItODS
individualswere sampled.Therefore,we also miniWe evaluatedfour potentialcorrelatesof parasite mizedheterogeneity
in parasiteprevalence
associated
prevalenceto testthe Hamilton-Zukhypothesis:
mi- with differences
amongage-sexcohorts(Kirkpatrick
gration,plumagebrightness,
sexualplumagedimor- et al. 1991; Weatherhead and Bennett 1991, 1992).
Birdswere nettedor shot,and a dropof bloodtaken
phisre,and nestingstratum.Becausemonogamyis the
primary mating systemin 17 of the 19 bird speciesin from the brachial vein or from blood around the
our sample,we could not evaluatemating systemas wounds. Blood films were air-dried and fixed in 100%
a correlateof parasiteload (Read 1991).
methanolupon return to the laboratory.Slideswere
The relativelysmallnumberof bird speciesexam- stained in Giemsa stain (Bennett 1970) and examined
ined limited quantitativeanalysesof otherpotentially for parasitesby scanningunder high dry (40x) and
confoundingvariables,suchas phylogeny.Although oil (100x) objectives.A minimum of 100,000blood
elaboratemethodshave been developedfor control- cellswasexaminedper smearfor thepresence
of paraling forphylogenyin comparative
analyses
(Pageland sites.To minimizepotentialproblemsof relyingon
Harvey 1988,Harvey and Pagel 1991),many system- only one kind of parasite(Weatherhead
et al. 1991),
atistshavelittle confidence
in the underlyingphylog- we scoredeachsmearfor the presenceof five types
(2) Haemoproteus,
and (3)
eniesused.For example,useof the phylogenetic
hy- of parasites:(1) Plas•nodium,
potheses
producedby Sibleyand Ahlquist(1990),the Leucocytozoon
(generaof sporozoansthat parasitize
onesmostfrequentlyused iu comparativeanalyses, blood cells, reticulo-endothelial cells, and other tismay posea seriousproblem(Gill and Sheldon1992, sues); (4) Trypanosotna
(flagellatesfound in blood
Lanyon 1992,Mindell 1992,Peterson1992,Harshman plasma);and (5) microfilaria(larval filarioid nema1994)for suchanalyses.Many ecologists
who attempt todes,adultsof whichparasitizebodycavityand tisto control for phylogeneticeffectsin comparative suesof host).Speciesidentificationwasdeterminedby
analysesevidentlydo not realizethat thebifurcating host-familyspecificityand morphological
characterisbranchingpatternsin any phylogenetichypothesis ticsof the gametocyte(seeGarvin et al. 1993).Species
may not representthe true phylogeny.No well- were identified at the International Reference Center
corroboratedphylogenyexiststhat would allow the of Avian Haematozoa,MemorialUniversityof Newamong-subfamily/familycomparisonsmade by a foundland,Canada(whereall positiveslidesare denumberof authors(e.g.Read1991);thisappliesto the posited).
interfamilial relationshipsof the bird taxa in our
A weaknessof our study is that we assume,withsampleas well. Therefore,our only meansof control- out corroborating
data,that thesebloodparasitesreling for phylogenetic
effectswas to comparethe six duce the fitness of their hosts. Until such data become
April 1997]
NestHeightandParasite
Loads
available, we have no alternative but to state the as-
sumption,a reasonableone given that theseparasites
arevectorborne(Ewald1983,1993).Studiessofar (e.g.
Bennett et al. 1988; Kirkpatrick et a1.1991;Weatherhead and Bennett1991,1992)have not revealedany
consistent association
between
haematozoan
TABLE1. Migratory tendencyand plumage dimorphismfor 19 speciesstudiedfor bloodparasites.
Mean
Species
infection
and body mass,usedas an index of fitness.Nevertheless,laboratorystudiesof domesticated
birds and anecdotalinformationon wild birds suggestthat most
haematozoain our study are potentiallypathogenic
(Atkinsonand van Riper 1991).
Bird specieswere grouped into four categories
basedon sexualplumagedimorphismand migratory
tendency(Table1). Bird specieswere ranked according to a subjectivecombinationof brightnessand
showiness(Pruett-Jones
et al. 1991)of male breeding
plumageby six ornithologists
who had no knowledge
of the parasitedataor of the rankingsof oneanother;
the mean rank was used for eachspecies(Appendix
2). Rankingswere restrictedto plumage;noneof the
bird speciesin our samplehas bright or contrasting
irides,bills, facialskin,or legsthat would affectoverall scores.The mean range of the individual ranksfor
the 19 specieswas4, with a maximumof 8 (for Thryo-
Monomorphic nonmigratory
Carolina Chickadee (Parus
carolinensis)
Tufted Titmouse (P. bicolor)
brightnessscoresproducedby humansreflectthe perceptionsby animalsof other animalsin their natural
backgroundis unknown. We used such plumage
scoresto make our analysescomparableto mostother
studies.
Each of the 19 bird specieswas assignedto a nest
stratumbasedon its mean nestheight (Appendix2).
Height categories
follow Greineret al. (1975)and conform
to those used to describe
vector
distribution
10.0
3.2
2
3
CarolinaWren (Thryothorus
carolinensis)
7.0
2
Monomorphic migratory
Veery(Catharus
fuscescens)
6.8
I
Swainson's Thrush (C.
ustulatus)
4.2
2
10.0
2
Wood Thrush (Hylocichla
mustelina)
Gray Catbird (Dumetella
1.8
2
Red-eyedVireo (Vireoolivaceus)
Ovenbird (Seiurusaurocapillus)
carolinensis)
3.0
5.3
3
I
Northern Waterthrush (S.
noveboracensJs)
5.1
1
Dimorphic migratory
thorusludovicianus;
some ornithologists
ranked this
Summer Tanager (Pirau,•a
specieshigh becauseof its reddish brown back,
ru bra)
orange-buffunderparts,and conspicuous
superciliary, ScarletTanager(P. Nivacea)
whereasothersregardedit as just a "brownish"bird) Rose-breasted Grosbeak
and a minimum of 1 (for ScarletTanager[Pirangaoli(Pheucticusludovicianus)
vacea]).Use of suchplumagescoresis an important Indigo Bunting (Passerina
cyanea)
issue.As emphasizedby Endler and Lyles (1989),
Endler (1990), and Weatherhead et al. (1991), whether
brightness Nest
score
stratum
PaintedBunting (P. ciris)
OrchardOriole (lcterusspurius)
1(7.0
3
18.3
3
• 4.8
3
15.2
18.3
10.3
2
2
3
Dimorphic nonmigratory
Northern Cardinal (Cardinalis
cardinalis)
16.3
2
Boat-tailed Grackle (Quiscalus
major)
12.2
2
Cominon Grackle (Q. q•iscula)
11.2
3
colors or strong, contrastingpatterns, and general
color dull shadesof brown or greenish;(2) iutermedi
ate no bright spectralcolors,but substantialportion
To determine
whether a correlation exists between
of plumagedominatedby strikingpatternsof stripes
nest height and plumage brightnesswithin a single or spots;and (3) bright at least some portion of
clade of birds, we analyzedthe wood-warblers(Pa- plumage containsat least one bright spectral color
rulidae) of easternNorth America (unfortunately, (Appendix 3).
parasitedata were not availablefor mostspecies).This
In addition,we performeda similaranalysison a
family is the onlyonein North Americathat hasa suf- complextropicalavifauna in AmazonianPeru (Terficient number of speciesand a sufficientrange of borgh et al. 1984). The 280 tropical speciesincluded
brightnessand nestheightsfor suchan analysis.Only only thosespeciesfound in "high ground forest"or
thosespeciesthatbreedin forests(i.e.vs.earlysecond- "transitionalforest"(i.e. "Fh" and "Ft" in Terborghet
growth or bogs)were included.Eachspecieswas as- al. 1984), but did not include members of the Falconisignedto oneof the threestratausedby Greineret al. formes,nocturnalspecies,and borealand australmi(1975)basedon its mean nestheight,or if not avail- grants. We also made trvo changesin the analysis.
able, the midpointof the rangeof nestheightsgiven First,we addeda fourthcategoryof brightness,
gaudy,
by Harrison(1975).Eachspeciesalsowas assignedto for those specieswith a substantialportion of the
oneof threebrightnesscategories
basedon thebreed- plumage coveredby two or more bright spectralcoling plumageof the male:(1) dull - no bright spectral ors (e.g, trogons [Trogonidae],certain macaws I/Ira
(Snow 1955, Anderson and DeFoliart 1961): I (0 to 0.3
m), 2 (>0.3 to 3.0 m), and 3 (>3.0 in).
182
GARVIN
ANDREMSEN
[Auk, Vol. 114
spp.],andcertaintanagers[e.g.Tangara
spp.]).Second,
becausethe nestsare unknownfor mostspecies,we
usedthefirstforagingstratumgivenfor eachspecies
by Terborghet al. (1984).We recognizethat somespeciesthat foragein one stratummay nestin another;
however,in the absenceof data on nest height,we
wereunableto devisean alternativeapproximationof
nestheight.Furthermore,it is not known for certain
that parasitesare acquiredonly or primarily at the
nestlingstage;we assme thatforagingadultsalsoare
vulnerableto someextent.Nevertheless,
our analysis
of the tropicalavifaunacannotbe consideredcomparableto thatof the Parulidaeabove.Additionally,we
cannotfind any analysesof verticaldistributionof
tween the mean (or midpoint)nestheightand
percent of infected individuals for all species
combined(Fig.2).
The correlationbetweennestingheight and
parasite prevalence (0.77) exceeded that be-
bird-biting vectorsin tropicalforests.
examine the relative
tweenplumagebrightness
and parasiteprevalence(rs = 0.45,P = 0.06,n = 19).Bothnesting
heightandplumagebrightness
had a significant
effect on parasite prevalence (ANOVA; nest
height,F = 29.7,P < 0.001;brightness,
F = 30.4,
P • 0.001;nestheightx brightnessinteraction,
F = 28.2,P -• 0.001).Consequently,
we usedpartial correlationanalysis(SAS Institute 1985) to
contribution
of these two
variablesto variationsin parasiteload. When
the effectof plumagebrightnesswas removed,
thecorrelation
betweennestheightandparasite
Migration.-•Of the 13 migrant speciessam- load was significant(Kendall'sTau = 0.58,P -•
pled, the meanprevalenceof infection,34%,was 0.001);in contrast,whenthe effectof nestheight
virtually identicalto the 33% found in the six was removed,the correlationbetweenplumage
residentspecies(seeAppendix 1). For the six brightnessand parasiteload was positivebut
pairsof congeners,
nonecontainedspeciesthat not significant(Kendall'sTau = 0.30,P -• 0.08).
differedin migratorytendency,
thusprohibiting Thisindicatesthatnestheightis a betterprediccomparisonsof within-family differencesin tor of variationin parasiteload than is brightprevalencewith respectto migratorytendency, ness.However,giventhe uncertaintyof the apas doneby Zuk (1991).
plicability of parametrictests to these data, a
Sexualdimorphism
andplumage
brightness.--Wemorecautiousconclusion
is thatnestheightprefounda positiverelationship
betweenplumage dictsparasiteload "as well as" any othervaribrightness
and parasiteprevalence(Fig. 1); the able.
Of particular interestwere two species,the
nine sexuallydimorphicspecieshad significantly higher levels of infection than the 10 Tufted Titmouse (Parus bicolor) and the Redmonomorphicspecies(51 vs. 24%,respectively; eyed Vireo (Vireoolivaceus),
that are unique in
Kruskal-Wallischi-squareapproximation,P = our samplein that both are dull-colored,mono0.016,n = 413and 522individuals,respectively). morphic speciesthat nest in the mid-canopy.
In three of the six pairs of congeners,
the spe- Bothspecieswere heavilyinfected(Fig. 1), concieswith the highestprevalencealsohad the trary to the predictionof the Hamilton-Zukhyhighestbrightnessscoreand, in the otherthree, pothesis,but consistentwith that of the Bennettthe conversewas true (binomial test, P = 0.50); Fallishypothesis.
An alternativeinterpretation,
therefore,the hypothesisthat the trend cotfidbe however, is that the red iris of the vireo and the
the resultof phylogenetic
biasescannotbe re- short crest of the titmouse are not considered in
jected.Because
thebrightness
scoresof thethird rankings such as ours that are restrictedto
speciesin the two taxa (Turdinae,Icteridae)with plumagebrightness
(M. Zuk pers.comm.).
a pair of congeners
was intermediateand close
For five of the six pairs of congeners,the
to valuesof thetwo speciesof congeners,
we be- specieswith the highest parasite prevalence
lievedthat an analysiswouldbe questionable. alsohad the highernestheight(binomialtest,
Nestingstratum.--A highly significantrela- P = 0.031);in the only genus(Seiurus)
in which
tionshipwas alsofoundbetweenmeanparasite the relationshipdid not hold, nestheightswere
prevalenceand mean nest height (Spearman virtually identical.Therefore,in contrastto the
rank correlation,rs = 0.77, P < 0.001, n = 19). relationshipbetweenparasiteloads and plumThe highestmean percentageof infectedindi- agebrightness,
the hypothesisthat the relationviduals,63%,was foundin speciesin theupper ship between parasite prevalenceand nest
stratum,wherevectorpotentiallikelyis highest height reflectsphylogeneticeffectscan be re(Snow 1955, Anderson and DeFoliart 1961). In
jected,at least at the within-genuslevel. At a
addition,we found a positiverelationshipbe- higherlevel,if we averagethe data for congeRESULTS
April 1997]
NestHeightandParasite
Loads
183
2O
Passarlna
Plranga
cIrls
ollvacea
18
CardinalIs
Passarlna
16
cardinalIs
ß
cyal•oa
Plranga rubra
14 ÷
Quiscalus
ludøvi••
"•*/
ß
major
P12
o
o
Hyloclchla
mustallna
ß • I...•US
spurlus
Parus
•
8'
Qulscalus
qulscula
carollnensls
Catharus
J
fuscesc•ns
J•
ß Thryothorus
iudoviclanus
ß ß Salurus
aurocaplllus
4'
ß
Selurus
noveboracenals
Vlrao
Catharus
ustulatus
•)
(•)
Parus
2'
ollvacaus
blcolor
ß
Dumetella
carolinesis
0
0
,
2O
40
60
60
lOO
Parasite prevalence (%)
FIC.1. Relationship
(r2 = 0.18,rs = 0.45)between
blood-parasite
prevalence
andbrightness
of maleplumagein 19 passerine
species.
Pointsfor two dull-plumaged
species
with relativelyhighparasiteprevalence
values are circled.
ners and consubfamilials,
then the relationship
betweenparasiteprevalenceand nestheightis
statisticallysignificant(genera,rs = 0.70, P =
0.015;subfamilies,
rs = 0.90,P = 0.01).Similarly,
the relationshipbetweenplumagebrightness
and percentageof individualsinfected(genera,
rs = 0.53, P = 0.065; subfamilies,rs = 0.60,
plumagebrightness,or nestingstratum.Therefore, phylogeneticeffectsmay have influenced
the outcomesof our analyses,but proper measurementof this influencerequires a larger
sampleof speciesand a well-corroborated
phylogeny.
Our analysis of nest height and plumage
brightnessin the wood-warblersremovesone
P = 0.09)suggests
that phylogeneticeffectsare
present,even though the probabilitylevels are level of phylogeneticeffectsby restrictingthe
slightlyhigherthan conventionalcriteriafor sta-
analysis to confamilials,or consubfamilialsif
tisticalsignificance(i.e. P = 0.05). In general, wood-warblersare considereda subfamily (Pacongeners
and confamilialsin our samplewere rulinae)of the Emberizidae(e.g.AOU 1983).For
more similar
to one another than to most other
wood-warblers
from eastern North America,
speciesin combinationsof parasiteprevalence, nestheightand brightnessof male plumageare
184
G^RVINAN][)REMSEN
[Auk, Vol. 114
10
Piranga
Icterus
ollvacea
spurius
Pheucticus
Plrang•
rub•
ludoviclanus
Hylocichla
•/• ©Vireo
ollvace
mustel/ha Oulscalus
major
,•..Parus bicolor
Dumetella
ß
ß,•"'carolinensis
ß Cardinalis
cardinalis
ß '(--
Thryothorus
Seiurus
Passerina
clrls
ludovicianus
•
noveboracensis
/ •
quiscula
a
carollnensis
ß
ß•
•
ß '(
Catharus fuscescens
Passerina
cyanea
20
40
Se•ur•, o•.... p.•,
60
Parasite prevalence (%)
80
100
FIG.2. Relalionship
(? = 0.50,r, • 0.77)betweenparasiteprevalence
andnestheightin 19passerine
species.Pointsfor two thdl-plumagedspecieswith relativelyhigh parasiteprevalencevaluesare circled.
highlysignificantly
associated
(X2 - 18.7,P <
0.001; Table 2). Switching the dullest speciesin
not affectthe outcomeof the analysis.Evaluationsof colorvariation (Bailey1978,Bakerand
the "brighi" category(e.g. Pine Warbler [Dend- Parker 1979, Burtt 1986) have not considered forin/capiuns])to the "intermediate"categorydoes agingor neststratumamongthe factorspotentially affectingplumage brightness,although
TAmF2. Numberof wood-warblerspecieswith various combinationsof male plumage brightnessand
nesting sh'ahm•.
Nesting stratum"
I'lumage brightness
I
2
3
Dull
In termediate
3
4
1
0
0
0
Bright
I
6
11
"Nest height:I d) to 0.3 nO,2 ( -(•.• to 3.(I m), 3 (-I.0 m).
Shutlet and Weatherhead (1990) showed that
ground-nestingwood-warblerswere lesssexu-
ally dichromaticthan thosenestingabovethe
ground.
Similarly,for the tropicalforestavifauna,foraging stratumand brightnessof male plumage
are highlysignificantly
associated
(X2 = 66.8,
P < 0.00l; Table3). This relationshipalsoholds
when Passeriformes
(X2 = 42.6,n = 184,P <
0.001)andnon-Passeriformes
(X2 = 44.0,n = 96,
April1997]
NestHeight
andParasite
Loads
] 8,5
TABLE
3. Number of bird speciesin a Peruviantropicalforestwith variouscombinationsof male plumage
brightnessand foragingstratum.Data takenin part from (Terborghet al. (1984).
Foraging stratum
Plumagebrightness
Dull
Intermediate
Bright
Gaudy
Terrestrial
Undergrowth
Subcanopy
Canopy
12
20
26
31
20
31)
II
28
2
0
7
2
14
9
41
27
P < 0.001) are analyzed separately.However, residentsand migrantsin our study,then no difonly onestatisticallysignificantrelationshipwas ferencein prevalencelevelswould be predicted
found (for hummingbirds,
Trochilidae;
X2 = betweenthe two groups,assumingrelatively
13.8, n = 17, P = 0.03) within seven smaller
similar vector and parasite communitiesover
taxonomicunits for which the numberof spe- the extensiverange of temperatelatitudes.
cieswas large enoughand the heterogeneityin
Sexualdimorphismand phuna,•,ebri,•,ht•ws>.
color or foragingstratumsufficientto permit Our finding of a positiverelationshipbetween
analysis(Piciformes;
Formicariidae;
Tyrannidae; bothplumagebrightness
and degreeof sexhal
Thraupidae;Dendrocolaptidae+ Furnariidae; dimorphism•vith parasiteprevalenceis conMsand Cotingidae+ PipridaeexcludingSchiffornis, tent with the interspecificanalysesof birds by
Pachyramphus,
and Tityra).Even within the Tro- Hamilton and Zuk (1982), Read (1987), I'ruettchilidae,however,the relationship
hasa strong Joneset al. (1990), anti Zuk (1991; brightness
phylogeneticcomponent,with all but oneof the only). However,asexplainedbelow,we propose
dull-coloredand intermediate-colored
speciesof that the cause of this relationshipinvolves an
the undergrowthbelongingto one subfamily, underlying verticalstratificationof parasitevec
Phaethorninae. Therefore, the overall relationtots and brightly coloredbirds,and not with an
ship betweenbrightnessand foragingstratum evolutionaryinteractionbetween parasitesand
is one that has a strongphylogeneticcompo- bird coloration,as proposedby Hamilton and
nent: The brightest taxa tend to occur in the Zuk (1982).
higher strata. However, all analysesfor the
Nestingstratum.--Aspredictedby Bennett
smallertaxonomicgroupsshowa positiveasso- and Fallis(1960),parasiteloadswere positively
ciation, albeit statisticallynonsignificant,be- correlatedwith nestheight.Our prevalence
data
tween brightnessand foraging stratum, with are consistentwith a hypothesisof greatestexprobability values ranging from 0.06 (Pici- posureto parasitevectorsin the upper stratum,
formes)to 0.46 (Formicariidae).The probability intermediate expostirein the middle stratum,
that all sevensubunitswould showa positive and the least exposurenear the ground. This
relationshipby chancealoneis lessthan 0.012 hypothesishas a simple rationale based in
(signtest).Therefore,
largersamplesizesof spe- the naturalhistoryof birdsand theirbloodparaciesfor eachtaxonwould potentiallyrevealsta- sites;i.e. the bird speciesmost heavily exposed
tistically significant associationswithin each to vectors that transmit blood parasites are
clade.
thosemost heavily infected.In contrastto the
Hamilton-Zukhypothesis,
theBennett-Fallis
hypothesisrequiresno complex,cyclic,coadaptaDISCUSSION
tiehal interactionsamongeffectsof parasiteson
Migration.--Althoughmigratory speciesare hosts,geneticallybasedresistanceto parasites,
exposedto a differentarrayof insectvectorsand and feedback from sexual selection. We think
otherecologicalfactorsthan are sedentaryspe- that the Bennett-Fallishypothesisdeservesatcies,we found no differencein parasitepreva- tention from a researchfield that has ignored it
lence between the two groups. The similar almostcompletely.Read(1991) statedit is "wellprevalences
foundin our studyperhapscanbe known that the densityof bitingflies,the main
explainedin the phenologyof the vectortrans- vectors of avian hematozoa, is higher above
mission.If infectionsare acquiredprimarilyon groundlevel." However,Garyin (1989)was the
the breeding grounds (Beaudoin et al. 1971), first to integratethis into testsof the 1lamiltonwhicharelargelyat temperatelatitudesfor both Zuk hypothesis,
and Read'sown previousinter-
186
GARVINANDREMSEN
specificanalyses(e.g.Read1987,Readand Harvey 1989)neitherincludednestheightas a vari-
[Auk, Vol. 114
atedwith upperor middlevegetationstrata(e.g.
Capitoninae,Cotingidae,Irenidae,Musophagi-
able nor cited Bennett and Fallis (1960).
dae, Nectariniidae,
The Bennett-Fallis
hypothesisappliesexclusivelyto bird speciesthat differ in nestheight.
Perhapsthe positivecorrelations
betweenparasiteload and brightnessin othertaxafor which
nestheightis of little or no relevance(e.g.fishes,
Ramphastinae,Thraupidae, Trochilidae,Trogonidae).For bird speciesin a tropicalforestin
Oriolidae,
Psittaciformes,
plague suchinterspecific
analyses(Pageland
Harvey 1988,Readand Harvey 1989).Additionally, our perceptionof brightnessmay not be
comparableto that of the bird speciesinvolved
(Endler and Lyles 1989, Weatherheadet al.
1991).We predict,however,that more sophisticated analyseswith a much larger number of
species
would showthat,throughouttheworld,
brightlycoloredbird speciesform a higherproportionof thecanopyavifaunathanof the neargroundavifauna.With someexceptions
(e.g.Pittidae, Momotidae, and many membersof the
Phasianinae),taxa renowned for specieswith
brilliant colorationare thosegenerallyassoci-
limitationsprobablyreducethenumberof arboreal predatorsrelative to terrestrialones.Perhaps terrestrialand near-groundbird species,
therefore,are exposedto a greatervarietyof visually oriented, diurnal predators,thereby selectingagainstbright coloration.(However,do
mostsuchnear-groundpredatorshavethecolor
visionthat would make bright birds conspicuous to them?)Alternatively,bright coloration
might be obscuredin the more evenly lit but
darkerundergrowthrelativeto the more complex backgroundbut brightlight of the canopy.
Forthisreason,it alsois unclearwhetherthesignal value of brightcolorationis greaterin the
New Guinea, Pruett-Joneset al. (1991) found a
stronglysignificantcorrelationbetweenforag-
ing strata and male plumage showiness.
Ward 1988; waterfowl, Scott and Clutton-Brock
Whether the distributionof ornithophilicvec1990) might also be explainedby similar hy- torsin tropicalforestsis similarto that known
pothesesbased on parasiteexposure;in other for temperateforestsis criticalto interpretations
words,perhapsthe parasite-brightness
correla- of thesedata.Currently,the degreeof similarity
tion might explainedby a brightness-exposureis unknown.
relationship.The potentialimportanceof expoWhy would bird taxathat nestin the canopy
sure was also shownby Bennettet al. (1992), tendtobemorebrightlycoloredthanthosenestwho found that individuals of the same bird
ing near the ground? Proponentsof the
speciesdifferedin levelsof parasiteprevalence Hamilton-Zukhypothesismight arguethat high
nestersare more brightly coloredbecausethey
dependingon nestinghabitat.
Only two other analysesof the interspecific are more heavily parasitized.However,factors
predictionsof the Hamilton-Zukhypothesisfor other than parasiteloads that might influence
birdsincludeda variablethat might be related verticaldistributionof brightcolorationinclude
to parasiteexposure.Pruett-Joneset al. (1991) predatoravoidance,unevenverticaldistribution
found a strong correlationbetween foraging of avianmatingsystems,
and constraints
on sigstrata and parasite prevalence.Read (1991) nal visibili•. Shutlerand Weatherhead
(1990),
found that monogamousspecieshave higher for example,proposedthat few wood-warbler
prevalence
levelsthan polygynousspeciesand specieswith brightlycoloredmalesneston the
that monogamousspecieshave higher nests; groundbecause
conspicuous
malesmightsignal
however,when restrictingcomparisons
to sister the presenceof the nestto predators.The resoproblem awaits
taxa, he found no tendencyfor monogamous lution of this cause-and-effect
specieswith the higherneststo havethe higher more detailed,comparativestudies.
prevalence.
In general,resultsfromtheinterspeWe foundthat few gaudyor brightspeciesof
cificapproachhavenot providedmuchsupport tropical forest birds are found in the underfor the Hamilton-Zuk hypothesis(e.g. Moller growth or on the ground,whereasmany dull
1990, Chandler and Cabana 1991, Lefcort and
speciesare found in the canopy.This suggests
Blaustein1991),and predictionsof the hypoth- that, if thereis an adaptiveexplanationfor the
esisare controversial(Claytonet al. 1992).
trend observed,it is most likely to be a conAlthoughwe found strongpositiverelation- straint on bright colorationnear the ground.
shipsbetweenbrightnessand nestingor forag- Predatoravoidancemight serveas sucha coning strata, we recognizethat many problems straint in the following way. Morphological
April 1997]
NestHeightandParasite
Loads
undergrowthor the canopy(Endler1990).Following the reasoningof Endlerand Lyles(1989),
Endler (1990), and Weatherhead et al. (1991),
how do we know whethera stronglymarked
specieswithoutbrightcolorsis lessconspicuous
in the undergrowthto other birds or predators
thanis a brilliantlycoloredspeciesin its canopy
environment? Therefore, conclusions that de-
pend on human judgmentof plumagebrightnessmust be regarded as tentative (Bennettet
al. 1994).Our analysesdependon the assump-
tion that evenif bird and humanperceptions
of
colorationare not equivalent,at least they are
correlated.
187
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We thank:J.M. Bates,R. T. Chesser,
D. H. Clayton,
R. T. Damian, J. A. Endlet, P. W. Ewald, S. J. Hackett,
M. S. Hafner, A. W. Kratter, C. A. Marantz, S. A. Na-
dler, A. T. Peterson, S. G. Pruett-Jones,A. E Read,
G. D. Schnell, T. S. Sillett, E. J. Temeles,B. Walther,
R. M. Zink, M. Zuk, and severalanonymous
reviewers for many perceptivecommentson variousdrafts
of this paper;G. E Bennett,M. A. Bishop,and J. R.
Caines
at the International
Reference
Center
of Avian
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GARVINANDgEMSEN
[Auk, Vol. 114
April1997]
NestHeight
andParasite
Loads
191
APPENDIX
2. Nestheights(fromCornellLaboratory
of Ornithology
nestrecords)
andbrightness
rankings
for
19birdspecies
usedin analysis.
"Original
rankings"
arethosegivenindependently
to eachspecies
by six
ornithologists
unawareof resultsof analysis
of bloodparasite
loads.
Species
Meannestheight
(m)
GrayCatbird
Red-eyed
Vireo
1.63
3.60
Veery
Tufted Titmouse
Swainson's Thrush
Northern Waterthrush
Ovenbird
Carolina Wren
Wood Thrush
Meanbrightness
(range)
Original
rankings
2.57
2.24
0.21
0.004
1.8(1-4)
3.0(1-5)
3.2 (1-7)
4.2 (2-7)
5.1 (4-6)
5.3 (4-6)
4, 1, 1, 1, 1,3
5, 2, 3, 3, 4, 1
0.52
6.8(3-9)
3, 7, 8, 6, 9, 8
1, 3, 7,
2, 4, 2,
6, 5, 5,
6, 5, 5,
2, 2, 4
7, 3, 7
4, 6, 5
4, 6, 6
1.57
2.51
7.0 (2-10)
10.0 (9-12)
10, 8, 4, 10, 8, 2
9, 12, 11, 9, 10, 9
Carolina Chickadee
1.62
10.0 (5-13)
8, 11, 12, 13, 5, 11
Orchard Oriole
Common Grackle
Boat-tailed Grackle
Rose-breastedGrosbeak
5.97
2.98
2.13
3.83
10.3 (8-13)
11.2 (9-13)
12.2 (10-13)
14.8 (14-17)
11, 9, 13, 8, 11, 10
12, 10, 9, 11, 13, 12
13, 13, 10, 12, 12, 13
17, 14, 14, 15, 14, 17
IndigoBunting
Summer
Tanager
0.91
5.82
15.2(14-16)
16.0(15-17)
16,15,15,14,15,14
15,16,17,16,17,15
PaintedBunting
Scarlet
Tanager
1.38
8.85
18.3(18-19)
18.3(18-19)
18,19,16,19,19,19
19,18,19,18,18,18
Northern Cardinal
1.70
16.3 (14-18)
14, 17, 18, 17, 16, 16
APPENDIX
3. Wood-warbler
species
of someeastern
NorthAmerican
forests,
withvaluesfor nesting
strata(1
to 3) and plumagescoresin parentheses.
Bachman's
Warbler(Vermivora
bachmanii,
2, bright);Tennessee
Warbler(V.peregrina,
1, dull);Orange-crowned
Warbler(V. celata,1, dull);NashvilleWarbler(V. ruficapilla,
1, bright);NorthernParula(Parulaamericana,
3,
bright);Magnolia
Warbler(Dendroica
magnolia,
2, bright);CapeMay Warbler(D. tigrina3, bright);BlackthroatedBlueWarbler(D. caerulescens,
2, bright);Yellow-rumped
Warbler(D. coronata,
3, bright);BlackthroatedGreenWarbler(D. virens,3, bright);Blackburnian
Warbler(D. fusca,3, bright);Yellow-throated
Warbler(D. dominica,
3, bright);PineWarbler(D. pinus,3, bright);Bay-breasted
Warbler(D. castanea,
3,
bright);Cerulean
Warbler(D. cerulea,
3, bright);Black-and-white
Warbler(Mniotilta
varia,1, intermediate);
American
Redstart
(Setophaga
ruticilla,
3, bright);Prothonotary
Warbler(Protonotaria
citrea,
2, bright);WormeatingWarbler(Helmitheros
vermivorus,
1, dull); Swainson's
Warbler(Limnothlypis
swainsonii,
1, dull);
Ovenbird(Seiurus
aurocapillus,
1, intermediate);
NorthernWaterthrush
(S. noveboracensis,
1, intermediate);
LouisianaWaterthrush(S. motacilla,
1, intermediate);
KentuckyWarbler(Oporornis
formosus,
1, bright);
HoodedWarbler(Wilsonia
citrina,2, bright);CanadaWarbler(W.canadensis,
2, bright).