The Auk 117(3):731-738, 2000

EFFECTS OF MALARIA ON ACTIVITY BUDGETS OF EXPERIMENTALLY INFECTED JUVENILE APAPANE (HIMATIONE SANGUINEA )

NANCY YORINKS 1'3AND CARTER t. ATKINSON TM •Departmentof Zoology,University of Wisconsin,Madison, Wisconsin 53706, USA; and 2UnitedStates Geological Survey, Pacific Island Ecosystems Research Center, P.O. Box 218, HawaiiNational Park, Hawaii 96718, USA

ABSTRACT.--Weused behavioral, physiological, and parasitological measures to document effectsof acute malarial infectionson activity budgetsof experimentallyinfected juvenile Apapane(Himatione sanguinea). Five of eightbirds died within 20 to 32 daysafter exposure to a singleinfective mosquito bite. InfectedApapane devoted less time to locomotoryactiv- itiesinvolving flight, walking or hopping, and stationary activities such as singing, preening, feeding,and probing. The amountof timespent sitting was positively correlated with par- asitemia and increaseddramatically after infection and between treatment and control groups. that succumbedto infectionexperienced a significantloss of body massand subcutaneousfat, whereassurviving Apapane were better able to maintainbody condition and fat levels.When rechallenged with the parasitefive monthsafter initial infection,sur- viving birds experiencedno increasein parasitemia,indicating that they had becomeim- muneto reinfection.Regardless of theoutcome, infected birds experienced acute illness that would have left them unableto forageor to escapefrom predatorsin the wild. Received8 March 1999, accepted11 January2000.

NATIVE HAWAIIAN forest birds were first ex- and abundanceof highly susceptiblenative for- posedto vector-borneparasitic diseases after estbirds (Scottet al. 1986,van Riper et al. 1986, the accidentalintroduction of mosquitoesin Atkinson et al. 1995). Most extant populations 1827 and the subsequentimportation of avian of Hawaiian honeycreepersare confined to pox virus and malaria (Plasmodiumrelictum) in shrinkingtracts of native forest at elevations cage birds and domestic fowl (Zimmerman above1,200 m, where coolertemperatures be- 1948,Warner 1968). Warner (1968) provided the gin to limit populationsof the primaryvector first detailed evidence that diseases from vec- of pox and malaria,Culex quinquefasciatus (Goff tor-bornepathogens were influencingnative and van Riper 1980,van Riper et al. 1986). forestbirds by exposingLaysan (Teles- Recent surveys of native Hawaiian birds pizacantans) from a disease-freepopulation on have shownthat populationsof a few LaysanIsland to mosquitoesat low elevations are able to survive in mid- and low-elevation on the island of Kauai. All cagedindividuals habitatsbelow 1,200m, where mosquitoesare died from fulminatingpox and malarial infec- seasonallycommon and malaria and pox trans- tions within 21 days of initial exposure,sug- missionhave become endemic, suggesting that gestingthat high vectorpopulations and a res- thebirds have developed resistance to lethalef- ervoir of disease in non-native birds main- fectsof the diseases(Scott et al. 1986,van Riper tained active cyclesof diseasetransmission at et al. 1986, Jarvi et al. 2000). On the island of these elevations. Studies conducted since then have shown Hawaii, Apapane (Himationesanguinea) and Hawaii Amakihi (Hemignathusvirens) are the thatpox and malaria,in conjunctionwith hab- itat destruction and the introduction of mam- only honeycreepersstill commonlyfound in malianpredators and aviancompetitors, have mid- and low-elevationhabitats. These species, causeddramatic changesin the distribution as well as Omao (Myadestesobscurus) and Ele- paio (Chasiempissandwichensis), have become 3 Present address: 1208 Tamarack Drive, Moscow, primaryreservoirs for malariabecause of their Idaho 83843, USA. high susceptibilityto infection(van Riper et al. 4Address correspondence to this author.E-mail: 1986, Atkinson et al. 2000). Based on blood [email protected] smears,the prevalenceof infectionin thesena-

731 732 YORINKSAND ATKINSON [Auk, Vol. 117 tive speciesranges as high as40% at elevations ular vein with a 27.5-gaugesyringe within two to between 900 and 1,500 m, with most infected three days of being moved to captivity. A blood individualscarrying chronic, low-intensity in- smear was prepared, fixed in absolutemethanol, fections characteristic of birds that have recov- stainedwith 2% bufferedGiemsa (pH 7.0), for 1 h, and examinedfor 10 min with a 400x objectiveto eredfrom acutemalaria and havesome degree diagnose patent malarial infections.Heparinized of resistance to reinfection. whole blood was centrifuged in microhematocrit The effectof diseaseon juvenilebirds is of tubesand plasmawas collectedand screenedfor an- particularinterest because a changein theirbe- tibodiesto P.relictum with an immunoblottechnique havior potentially could translate into de- (Atkinson et al. 1995) to confirm that the birds had creased fitness as adults. Parasitemias in hatch- no prior historyof exposureto malaria. ing-yearHawaiian honeycreepers are up to six The behavioralexperiment was conductedin a timeshigher than thosein adults,suggesting mosquito-proofflight cage(5.5 x 2.4 x 3.6 m) that the youngerbirds have less resistance to infec- contained various types of local vegetation.Birds tion and are the age classthat is hardesthit were fed Nector Plus in eight 40-mL feeders,and eight otherfeeders containing water were placed in during malarial epidemics (van Riper et al. the room.Locations of the 16 feederswere changed 1986).Findings from other studieshave been eachmorning to mimic the transitoryconditions of similar For example,infections of Haernoproteusnatural food sources.A fine mist of water vapor was progneiin Purple Martins (Prognesubis) are be- spayedinto the flight cage for 15 to 30 min each lievedto be morevirulent in youngbirds (Dav- morning to simulaterain forest conditions.Feeding idar and Morton 1993). Sublethal infections and mistingended at least2 h beforebehavioral ob- with Trichinellapseudospiralis in American Kes- servations. trels (Falcosparverius) influenced juvenile fit- Eight Apapanewere assignedrandomly to the ex- nessthrough altered incubation behavior and perimentalgroup and eight to the controlgroup. Ex- parentalcare by infectedadults, and through perimentalbirds were infected by thebite from a sin- gle Plasmodiumrelictum-infected mosquito using col- altered careof infectednestlings by uninfected onized Cidex quinquefasciatus(see Atkinson et al. parents(Saumier et al. 1991).In this study,we 1995). Control birds were bitten by a single unin- used behavioral,physiological, and parasito- fected mosquito.Morphological measurements and logicalmeasures to quantifythe effects of acute behavioral observations were taken before and after malarial infectionson morbidity and mortality infection. in juvenile Apapane under controlledexperi- No morethan eightbirds were presentin the flight mental conditions. cageat one time, and equalnumbers of infectedand controlbirds were presentat the beginningof each METHODS of two successivetrials. Becausedensities of Apa- pane in the wild exceed3,000 birds/km 2 (Ralph and We caught16 hatching~yearApapane in mistnets Fancy 1995), densityin the flight cagewas compa- in ohia(Metrosideros polymorpha) /koa (Acaciakoa) for- rable to natural conditions. Behavioral observations estsat 1,800m in the Upper WaiakeaForest Reserve were not takenfor the first three to four daysafter on the easternslopes of Mauna Loa in March and birds were movedto the flight cageto allow themto April 1993.Birds were capturedat three sitesthat habituateto their surroundings.This wassufficient were approximately3 km apart. This area is rela- time for the birdsto locatefood sourcesin the aviary tively free of Culexmosquitoes, and the prevalence and exhibit behaviorscomparable to what we have of malarial infection in forest birds is less than 5% observedin the wild. After this acclimationperiod, (C. Atkinson unpubl. data). All 16 birds were in ju- observationswere takenfor four to eightdays (pre- venal plumageand had not startedtheir first pre- infectionperiod). Birds were then infectedand sub- basicmolt (Fancyet al. 1993). sequentlyobserved for the next 24 days. The first Birdswere transferredto a mosquito-proofaviary four dayswere the "pre-patent"period of infection at Hawaii Volcanoes National Park (elevation 1,200 where the parasitewas undergoingdevelopment in m) and allowed to acclimate under conditions of am- fixed tissues in the host and had not reached detect- bienttemperature and light for oneto four weeksbe- able concentrationsin blood.The next 20 dayswere fore use in experiments.This was sufficienttime for takenduring the "patent" periodwhen intraeryth- massand food consumptionto stabilize.During the rocyticparasites could be found on bloodfilms of pe- acclimatizationperiod, birds were housedindivid- ripheral blood. ually in cagesmeasuring 1 x 0.5 x 0.5 m and fed a Behaviorwas quantifiedwith a laptop computer diet of artificial nectar (Nector Plus, Necton USA, througha programthat assigneddifferent keys on TarponSprings, Florida) and freshoranges and pa- thekeyboard to specificbehaviors. The program kept paya.Birds were color banded and bled from thejug- trackof the timebetween keystrokes so that the total July2000] BehavioralEffects of Malaria 733 timespent on each behavior could be determined at ments. Thus, we did not include time and weather as the end of an observationperiod. Observationstook independentvariables in testsof treatmenteffects. placethrough a one-waymirror at one end of the Differencesin mortality betweeninfection groups flight cage.Observed behaviors were definedas ei- were examined with a Fisher's exact test. We ana- therlocomotory (flying, flapping, hopping, walking) lyzed behavioraland morphologicaldata by repeat- or stationary(preening, probing, singing, feeding, ed-measuresANOVA (PROC GLM; SAS 1985) using scratching,sitting, miscellaneous). Each wasob- time blockas the repeatedunit and individual birds servedfor 10 to 20 min per day for an average7.7 h as the experimentalunits. The repeated-measures per bird. All birds were observedfor approximately designallows detection of a differencein behavior the sameamount of time per day, and the order of betweeninfection groups over time. We then useda observationwas determinedrandomly. Observations contrastanalysis to examineeffects within groups were conducted between 0900 and 1700 Hawaii Stan- morecarefully. Characteristics before infection were dard Time. comparedwith thoseafter infectionwithin and be- Every four days,Apapane were capturedin the tweeninfection groups. Pre- and postinfectionchar- flight cagewith a smallmist net. We weighedcap- acteristics also were compared between infection tured birds to the nearest0.1 g and estimatedthe groups. amountof furcular fat on a four-pointscale (1 = no All birds that died during the experimentwere visiblefat, 4 = fat bulgingbeyond the plane of the necropsiedto determinecause of death. Represen- chest).In addition, smearswere made from a drop tative piecesof major organswere fixed in 10%buff- of blood collected from the brachial vein to follow ered formalin, embeddedin paraffin, sectioned,and the progressof malarialinfection in infectedbirds stainedwith hematoxylinand eosin.Birds that re- and to confirm absence of infection in control birds. covered from acute malarial infection were rechal- We alsomeasured tarsus, wing, and culmenlength lenged with the same isolate of P. relictumfive everyeight days.Morphological measurements and monthspostinfection to assessimmunity to reinfec- bloodsamples were takeneither after observations tion. Threeuninfected Apapane also were exposed were finished,or at least2 h prior to the beginning to singleinfective mosquito bites at the sametime to of observationsin the morning. Parasitemiawas act as positive controls. quantifiedas the number of infectederythrocytes per 1,000 erythrocyteson Giemsa-stainedblood RESULTS smears(see Godfrey et al. 1987). We averagedthe proportionof time spenton each All eightinfected Apapane developed patent behaviorover all observationperiods for eachbird erythrocyticinfections within eight dayspost- within four-dayblocks. Results from the two trials infection, whereas all control birds remained were similar, so data from all 16 birds were com- uninfectedthroughout the durationof the ex- bined for analysis.Each block had corresponding periment.Mean parasitemiain three of the in- measurementsof growth and parasitemiabecause fectedindividuals peaked at 10% 12 dayspost- theseparameters were obtained every four days. The infection and subsequentlydeclined (Fig. 1). postinfectionperiod consistedof five time blocksin the20 daysafter the pre-patent period. Because path- The remaining five infectedbirds succumbed ogeniceffects of P.relicturn are associatedwith eryth- to acuteanemia during the courseof the ex- rocyticstages of infection(Atkinson et al. 1995),the periment,with mean parasitemiasas high as four daysbefore infection and the pre-patentblock 28%before death (Fig. 1). Threeof thesebirds were combinedas the preinfectionperiod. survived the duration of the five time blocks of Becausewe were concernedprimarily with effects postinfectionbehavioral observations, whereas of malarial infection on behavior of these birds, the two (25%)died duringthe fourthpostinfection eight infected birds were consideredthe infected block (Fig. 1). None of the uninfectedcontrol group,regardless of their later survivalstatus, and birds died duringthe experiment(Fisher's ex- were comparedwith the eight uninfected control act test, P = 0.026). birds. We also divided the infectedgroup into two Grossand microscopiclesions in the five fa- subgroups:(1) birds that survivedto be experimen- talities were characteristic of severe malaria. tally reinfectedfive monthslater, and (2) birdsthat All five individuals were emaciatedat necropsy died towardthe end of the experiment. Behavioral and morphological measurements and had enlarged and blackened livers, were analyzedfor the effectsof time and infection spleens,and kidneysfrom extensivedeposition group.Because time of day and weatherwere dis- of malarialpigment. Microscopic changes were tributedsimilarly among observation periods, we as- characteristic of severe acute anemia described sumedthat any effectsthey may have had on behav- in otherspecies of h0neycreepers with malarial ior also were uniform across experimental treat- infections,including diffuse extramedullary 734 YORINKSAND ATKINSON [Auk, Vol. 117

40

eE 30 Survivors Fatalities ...... • 2o

lO

• 20 40

60

lOO I i i i I I I I I I I 0 4 8 12 16 20 24 28 32 36 Days Post-Infection

FIG. 1. Mortality and meanparasitemia for surviving(n = 3) and dying (n = 5) Apapaneafter exposure to a singleinfective mosquito bite.

erythropoiesisin the hepaticsinusoids and oc- groups,and locomotionalso was significantly casionalareas of extramedullaryerythropoie- different over time (Table 1, Figs. 2B,C). sis in the hepaticparenchyma (Atkinson et al. We then analyzedbehavioral data by con- 1995). trasts. We found no differences in behavior be- Beforeexposure to mosquitoes,probing, sit- tween infected and control groupsbefore in- ting, and preeningwere the predominantbe- fection, but after infection all behaviors dif- haviorsamong birds in the controland infec- fered significantly between treatment groups tiongroups. Locomotory behaviors were infre- (P < 0.05).Among infected birds, all behaviors quent,so they were analyzedtogether as the changedsignificantly after infection (P < 0.05). category"locomotion." The behaviorsscratch- Among control birds, probing and preening ing, stretching,and "miscellaneous"also were declined after exposureto uninfectedmosqui- infrequentand were droppedfrom the analy- toesand werethe onlybehaviors to changesig- sis. nificantly (P < 0.05). Because two birds died before the fifth time When infected birds were subdivided into block,we usedtype III sumsof squaresso that survivors and mortalities, a significanttreat- thesebirds couldbe includedin the repeated- ment x time interaction occurred for mass (P measuresANOVA despitethe missingcells. A < 0.01), sitting (P < 0.01), and preening (P < significantinteraction (P < 0.05) occurredbe- 0.05). When the three surviving birds were tween time and experimentalgroup for sitting, comparedwith the eight controlbirds by con- preening, probing, and singing (Table 1). trast analysis,no characteristicswere signifi- Preening activity increasedfor control birds cantly different between groupsbefore infec- and decreasedfor infected birds. Probing and tion, whereasall variablesexcept preening and singing activity decreasedfor infectedbirds, mass differed after infection (P < 0.05). Al- and the amountof time spentsitting increased though the size of the surviving group was (Fig. 2A). None of these three behaviors small, the results concur with those obtained changed significantlyfor control birds. Al- when all eight infectedbirds were considered thoughneither locomotion nor feeding showed together(Table 1). A positiverelationship oc- significanttreatment x time interactions,they curred between parasitemia and sitting, and were significantlydifferent between treatment negativerelationships occurred between para- July2000] BehavioralEffects of Malaria 735

TABLE1. Resultsof repeated-measuresANOVA for differencesin behaviorand massof Apapaneby time and experimentalgroup.

Treatment" Time b Treatment X time c

Characteristic F P F P F P Sitting 49.03 0.0001 16.04 0.0001 11.03 0.0001 Locomotion 21.52 0.0004 6.42 0.0001 1.24 0.294 Preening 0.36 0.558 0.67 0.672 4.28 0.001 Probing 14.25 0.002 9.35 0.0001 2.65 0.021 Singing 2.71 0.122 2.91 0.013 2.79 0.016 Feeding 4.94 0.043 1.91 0.088 1.40 0.224 Mass 1.39 0.258 8.92 0.0001 13.27 0.0001

a df = 1 and 14. b df = 6 and 84. c df = 6 and 84. sitemiaand all otherbehaviors (Table 2). All of Eachfour-day time blockhad corresponding the behavioralcorrelations with parasitemia measurementsof body mass,tarsus, wing, cul- (exceptfeeding) were significant(P < 0.05;Ta- men,and fat. Noneof thebirds grew during the ble 2). experiment, so tarsus, wing, and culmen lengthswere not included in theanalysis. Mass

0.8 was analyzedby the samerepeated-measures method used for the behavioral data and showeda significantinteraction between time and infection group (Table 1, Fig. 3A). Follow- 0.5- ing contrast analysis, mass differed signifi- cantly between treatment groups after infec- tionand within the infected group' before and 0.2- after infection (P < 0.05). Fat scores declined E significantly in infected birds relative to con- trols (Mann-WhitneyU = 57.5, n• = 8, n2= 8, o P < 0.05; Fig. 3B). Of the three birds that recovered from acute malarial infection,one died at day 155 postin- o o.o5- fectionfrom an impactedgizzard that was not related to malarial infection. Parasitemias in

.mo o.o3- the two survivors remained below 2% when o theywere rechallenged with thesame isolate of Q,, 0.05 P. relicturnon days 142 and 171 postinfection. One of the two rechallengedbirds experienced 0.045- a relapse at day 200 postinfection and died 0.04' from acute anemia complicatedby a partially

0.035'

0.03- TABLE 2. Pearson correlation coefficients between parasitemia and proportion of time devoted to -4 0 4 8 12 16 2O eachbehavior by infectedApapane."

Time (Days) Characteristic Correlation Bonferroni P FIG. 2. Behavioral effects of malarial infection on Sitting 0.720 <0.001 eight controland eightexperimentally infected Apa- Locomotion -0.531 0.001 pane during five four-day time blocks between ex- Preening - 0.449 0.016 posureto mosquitoesat day 0 and terminationof ex- Probing -0.514 0.002 periment at day 20. (A) Proportion of time sitting Singing - 0.422 0.034 still; (B) proportionof time engagedin locomotory Feeding -0.139 1.000 activities;and (C) proportionof time spent feeding. Overall testof significance,Bartlett X 2 = 495.5,df = 21, P < 0.0001. 736 YORINKSAND ATKINSON [Auk, Vol. 117

16 15 14 13 12 11 Controls .... 10 - '"'"'" A I I I I I I I I I I

.

_.o

..

SurvivorsFatalities ...... '-...... Controls .... B 0 I I I I I I I I I I 0 4 8 12 16 20 24 28 32 36 Days Post-Infection F•c. 3. Effectof malarial infectionon (A) meanbody massand (B) meanfat scorefor eight uninfected controlApapane, three infected survivors, and five mortalities.Measurements were taken at four-dayinter- vals beginning at day 0.

impacted gizzard and poor body condition. lethal effectsof the diseaseare closelylinked to Parasitemia at death was 18%. The second re- level of resistancein a particular individual. challengedbird surviveduntil day 605 post- In general the behavioralchanges we de- infection, when it died from accidental causes tected suggestan overall decreasein activity duringblood sampling. All threepositive con- among infected birds. Particularly significant trol birds developedacute infections and suc- was the negativeinfluence of acuteinfections cumbedwithin 14 dayspostinfection with par- on surviving birds. All individuals passed asitemiasas high as 18%at death.Mean body througha periodof severephysiological stress mass of these three birds at death was 8.55 ___ where they were almosttotally inactive.In the SD of 0.49g, whichwas slightly lower than the wild, they would havebeen extremely vulner- mean massof the five original fatalities(Fig. able to predation. 3A). Apapane feed primarily on nectar of ohia flowers and may conduct elevationalmigra- DISCUSSION tions in searchof ohia blooms(MacMillen and Carpenter1980, Ralph and Fancy1995). Unin- We assessed the effects of acute malarial in- fectedbirds may follow periodic blooms of ohia fectionson juvenileApapane under controlled trees to lower elevations,become exposedto experimentalconditions with a combinationof malaria, and then migrateupslope during the behavioral,physiological and parasitological pre-patentperiod of the diseasebefore behav- measures.We observedsignificant declines in ioral effects of the infection have been mani- activity levelsof infectedbirds, with all birds fested.Once the infectionbecomes patent, de- becomingmoribund during the period when creasedmobility and feedingeffort (Figs.2A- parasitemiareached a peak.Infected birds un- C) would placeacutely ill individualsat a com- derwentan acuteillness with significantloss of petitive disadvantage with Iiwi (Vestiaria body mass and fat over its duration. Loss of coccinea)and other native nectarivoresthat still body mass and declinesin activity were cor- maintain densepopulations in high-elevation relatedwith parasitemia,indicating that sub- montane forests (Carpenter and MacMillan July2000] BehavioralEffects of Malaria 737

1976). Acute illness also would leave infected ACKNOWLEDGMENTS Apapanemore susceptibleto thermalstresses (Hayworthet al. 1987). We thankMichael Samuel and DongXiang for as- sistancewith the statisticalanalysis and Louis Sileo, Factors that determine whether a bird will Robert Dusek, William Iko, Julie Lease, Christine survive infectionare poorly understood.Such Gaasch,and BonnieLewis for help in capturingand factorsmay be relatedto geneticsof the host caringfor Apapaneused in the study.John Coleman, and parasiteand to overallphysiological con- Departmentof Wildlife Ecology,University of Wis- dition of the host (Gustafssonet al. 1994,Sorci consin-Madison,kindly providedthe computerpro- et al. 1997).It is interestingthat body massof gram to quantify behavioralobservations. Bethany survivingApapane did not differ significantly Woodworthand Donald Forresterprovided helpful from that of control birds, suggestingthat commentson earlier drafts of the manuscript. stored fat reservesand overall body condition are criticalfor survivingthe acute phases of the LITERATURE CITED infection when foraging behavior declines ALLANDER,K. 1997. Reproductiveinvestment and sharply.Atkinson et al. (1995)found a similar parasitesusceptibility in the GreatTit. Function- relationshipin experimentallyinfected Iiwi, al Ecology11:358-364. where preinfectionbody masswas a goodpre- ATKINSON, C. t., R. J. DUSEK, K. L. WOODS, AND W. dictor of survival time. M. I•co.2000. Pathogenicity of avian malaria in Recoveryfrom acute malarial infection may experimentallyinfected Hawaii Amakihi. Jour- benefitan individual by conferringacquired re- nal of Wildlife Diseases 36:197-204. sistanceto reinfectionwith homologousiso- ATKINSON, C. T., K. L. WOODS, R. J. DUSEK, L. S. SIL- EO, AND W. M. IKO. 1995. Wildlife disease and latesof the parasite.This phenomenon, termed conservationin Hawaii: Pathogenicityof avian concomitant immunity or premunition, was malaria (Plasmodiumrelictum) in experimentally first describedin avian host-parasitemodels infected Iiwi (Vestiariacoccinea). Parasitology more than 70 years ago (Taliaferroand Tali- 111 :S59-S69. aferro 1929) and is based on persistenceof a CARPENTER, E L., AND R. E. MACMILLEN. 1976. subclinicalinfection that stimulatesstrain-spe- Thresholdmodel of feeding territoriality and cifichumoral and cell-mediatedimmunity. It is test with a .Science 194: likely that thesechronically infected individu- 639-642. als form the corebreeding population in low- DAVIDAR,P., AND E. S. MORTON.1993. Living with and mid-elevation habitats where malaria parasites:Prevalence of a bloodparasite and its effecton survivorshipin the PurpleMartin. Auk transmission has become endemic. It is not 110:109-116. clear, however, whether chronic infections are FANCY, S. G., T. K. PRATT, G. D. LINDSEY, C. K. HAR- sufficientlyvirulent to influencehost fitness, al- IDA, g. H. PARENT, Jr., AND J. D. JACOBI.1993. thoughrecent studies suggest that a clearphys- Identifying sexand ageof Apapaneand Iiwi on iologicaltradeoff exists between host defense Hawaii. Journalof Field Ornithology 64:262- againstparasites and the stressesassociated 269. with reproduction(Norris et al. 1994,Oppliger GODFREY, R. D., Jr., A. M. FEDYNICH, AND D. B. PENCE. 1987. Quantification of hematozoa in et al. 1996, Allander 1997). blood smears. Journal of Wildlife Diseases 23: We provided additional experimental evi- 558-565. dencedocumenting the pathogenicityof avian GOFF, M., AND C. VAN RIPERIII. 1980. Distribution of malaria in Hawaiian honeycreepers.These mosquitoes(Diptera: Culicidae) on the east findingssupport the idea that this introduced flank of Mauna Loa Volcano, Hawaii. Pacific In- diseasecontinues to have profoundeffects on sects 22:178-188. native forest birds at lower elevations(Warner GUSTAFSSON,L., D. NORDLING, M. S. ANDERSSON,B. 1968, van Riper et al. 1986, Atkinson et al. C. SHELDON,AND A. QVARNSTR•M. 1994. Infec- 1995). Efforts to restore populationsof native tious diseases,reproductive effort and the cost forest birds in mid- and low-elevation habitats of reproductionin birds. PhilosophicalTrans- actionsof the Royal Societyof London SeriesB will continueto be hamperedunless effective 346:323-331. techniquesfor managingvector populations HAYWORTH, A. M., C. VAN RIPER III, AND W. W. and interrupting transmissionof this intro- WEATHERS. 1987. Effects of Plasmodium relictum duced diseasecan be developed. on the metabolicrate and body temperaturein 738 YORINKSAND ATKINSON [Auk,Vol. 117

Canaries (Serinuscanarius). Journal of Parasitol- SAUMIER, M.D., M. E. RAU, AND D. M. BIRD. 1991. ogy 73:850-853. Behavioralchanges in breedingAmerican Kes- JARVI, $. I., C. T. ATKINSON, AND R. C. FLEISCHER. trelsinfected with Trichinellapseudospiralis. Pag- 2000. Immunogenetics and resistance to avian es 290-313 in Bird-parasite interactions:Ecolo- malaria (Plasrnodiurnrelicturn) in Hawaiian hon- gy, evolution,and behaviour(J. E. Loyeand M. eycreepers(Drepanidinae). In press in Conser- Zuk, Eds.). Oxford University Press,Oxford. vation and ecology of Hawaiian birds (J. M. SCOTT,J. M., S. MOUNTAINSPRING,E L. RAMSY,AND C. B. KEPLER. 1986. Forest bird communities of Scott, S. Conant, and C. van Riper III, Eds.). Studiesin Avian Biology. the HawaiianIslands: Their dynamics,ecology MACMILLEN, R. E., AND E L. CARPENTER.1980. Even- and conservation.Studies in AvianBiology No. 9. SORCI, G., A. P. MOLLER, AND T. BOULINIER. 1997. Ge- ing roostingflights of the honeycreepersHima- netics of host-parasiteinteractions. Trends in tionesanguinea and Vestiariacoccinea on Hawaii. Ecologyand Evolution 12:196-200. Auk 97:28-37. TALIAFERRO,W. H., AND L. G. TALIAFERRO. 1929. Ac- NORRIS, K., M. ANWAR, AND A. E READ. 1994. Re- quired immunity in avian malaria I. Immunity productiveeffort influencesthe prevalenceof to superinfection. Journal of Preventive Medi- haematozoanparasites in Great Tits. Journalof cine 3:198-208. Ecology63:601-610. VAN RIPER III, C., S. G. VAN RIPER, M. L. GOFF, AND OPPLIGER, g., P. CHRISTE, AND H. RICHNER. 1996. M. LAIRD.1986. The epizootiologyand ecologi- Clutch size and malaria resistance. Nature 381: cal significance of malaria in Hawaiian land 565. birds. EcologicalMonographs 56:327-344. RALPH,C. J., ANDS. G. FANCY.1995. Demography WARNER, R. E. 1968. The role of introduced diseases and movementsof Apapaneand Iiwi in Hawaii. in the extinction of the endemic Hawaiian avi- Condor 97:729-742. fauna. Condor 70:101-120. $A$ INSTITUTE.1985. SAS user's guide: Statistics, ZIMMERMAN, E. C. 1948. Insects of Hawaii, vol. 1. version5. SASInstitute, Inc., Cary,North Caro- University of Hawaii Press,Honolulu. lina. Associate Editor: E. Danchin