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<I>HIMATIONE SANGUINEA</I 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.Birds 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 Finches (Teles- Recent surveys of native Hawaiian birds pizacantans) from a disease-freepopulation on have shownthat populationsof a few species 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
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