Blackfly-Induced Mortality of Nestling Red-Tailed Hawks

The Auk 115(2):368-375, 1998

BLACKFLY-INDUCED MORTALITY OF NESTLING RED-TAILED HAWKS

ROGER N. SMITH, TMSTEVEN L. CAIN, 1 STANLEYH. ANDERSON,2 JEFFREYg. DUNK, L5AND ELIZABETHS. WILLIAMS3 •GrandTeton National Park, Officeof Scienceand ResourceManagement, P.O. Drawer 170, Moose,Wyoming 83012, USA; 2WyomingCooperative Wildlife Research Unit, P.O.Box 3166, Universityof Wyoming, Laramie,Wyoming 82071, USA; and 3WyomingState Veterinary Laboratory, University of Wyoming,1174 SnowyRange Road, Laramie,Wyoming 82070, USA

ABSTRACT.--Wedocumented blackfly infestations(Simulium canonicolum) at 42 Red-tailed Hawk (Buteojamaicensis) nests in Wyoming. Blackfliescaused mortality at 6 of 42 (14%)nests where young hatched(13 of 87 nestlings)and were the only known causeof nestling mortality. The onsetof infestationsoccurred when nestlings were 3 to 20 daysold and usually lasted until nestlingsdied or fledged. Age of nestlingsat mortality ranged from 9 to 43 days. Levelsof blackflyinfestation were highly variableamong nests and wereaffected by weather The cumulativeeffects of infestationson nestlings,including physical harassment, Leuco- cytozoon(a blood protozoantransmitted by blackflies)infection, and direct lossof blood and body fluids from biting flies,apparently resulted in mortalitiesthrough sustained physio- logicaldamage, trauma associated with early nestdeparture, or both. Becauseblackfly in- festationscan be detectedonly at closerange, are ephemeral at nests,and cancause mortality of nestlingsover a wide rangeof ages,the presenceof blackfliesand their influenceon re- production probably are undetected during most raptor productivity surveys. Received23 January1997, accepted26 August1997.

A VARIETY OF PARASITES has been found in ifornia.However, they did not suggestpossible raptors (Trainer 1969, Keymer 1972, Green- mechanismsof mortality and gaveno source wood 1977, Guti6rrez 1989,Philips 1990,For- for the information.Stabler and Holt (1965) re- resteret al. 1994).Although the literaturede- ported a prevalence of blood protozoa in a scribingparasites in raptors is fairly extensive, number of different hawks, and Forrester et al. few researchers have described the effects of (1994) documentedthe relative occurrenceof theseparasites on their raptorhosts. Blackflies blood parasitesin raptors in Florida but made (Simuliumspp.) and the parasitesthey transmit no mentionof the potentialeffects of thesepar- havebeen associated with at leastfour species asites on raptor productivity. Hunter et al. of raptors (Greiner and Kocan1977, Jolly 1982, (1997) attributed mortality of Great Horned Hunter et al. 1997),but their effecton the health Owls (Bubovirginianus) to feeding blackflies of thesespecies is largelyunknown. (Simulidae), anemia, and blood parasite (Leu- Fitch et al. (1946)reported that 7 of 11 mor- cocytozoonspp.) infection.However, all of the talities of nestlingRed-tailed Hawk (Buteoja- mortalitythey observedoccurred in owlsteth- maicensis)were due to blackflies (Eusimulium ered to platformsfor experimentalpurposes. clarum).Similarly, Brown and Amadon (1968) In a portion of our study area in Grand Teton reported that during wet years, biting flies National Park (GTNP), northwesternWyo- (Prosimuliumspp.) were a principal cause of ming, the numberof youngRed-tailed Hawks mortality of nestlingRed-tailed Hawks in Cal- fledged per nest declined from 1.4 to 0.7 be- tween 1947 and 1975 (Craigheadand Mindell 1981). More recent monitoring of productivity 4 Present address: Teton Science School, P.O. Box 68, Kelly, Wyoming 83011, USA. E-mail: (1990 to 1991)indicated a high proportionof [email protected] nestingfailures, and dead youngwere found in s Present address: Department of Wildlife, Hum- and beneathsome nests (S. Cain unpubl.data). boldt State University, Arcata, California 95521, In all caseswhere dead nestlingswere found, USA. prey itemswere in the nests,and adultswere 368 April1998] Red-tailedHawk Mortality 369 present and defendedthe nests, suggesting ability,the sameindividual (RNS)made all estimates that parasitismor diseasecaused the mortali- of blackflies. Blackflieswere collected by passing a ties (versus parental abandonmentor starva- smallhand-held net overthe nestand by pickingflies tion).These findings provided the impetusfor off of the nestlingsby hand. Protocalliphoralarvae (blowflymaggots) were removed from theear cavity a broad-basedecological study of Red-tailed of severalnestlings. Both blackfliesand blowflies Hawks. Here,we describethe effectsof blackfly were preservedin 10%formalin. infestations,and associatedtransmission of the Weused nonparametric analyses because our data blood protozoanLeucocytozoon, on Red-tailed were categorical.Comparisons of levelsof ectopar- Hawk nestlings.Our primary objectiveswere asitism were by Kruskall-Wallis one-way ANOVA. to: (1) categorizeboth the levelsand duration Statisticaltreatment of nestlingmortality with G- of blackfly infestationat individual nests,and testsfollowed Sokal and Rohlf (1995). (2) investigatethe effectsof blackfly infesta- To assessblood parasitemia,a 0.5-ccblood sample tions on the survival of Red-tailed Hawk nest- was collectedfrom one nestlingin eachnest (1993 lings. and 1994only) when youngwere approximately30 to 35 daysold. Samplesalso were collectedfrom two adults. Fresh blood smears were air-dried, fixed, and STUDY AREA AND METHODS stainedwith Hema3 modifiedWright's stain. Smears were scannedusing dry and oil magnification.Leu- We studied Red-tailed Hawks in northwestern cocytozooninfection was diagnosed by the presence Wyomingwithin GTNP (43ø67'N,110ø72'W). GTNP of elongategametocytes. Smears were considered encompassesa high mountainvalley surrounded by negativeif no Leucocytozoonwere detected after scan- the Teton Mountains to the west, the Gros Ventre ning the entiresmear. Mountainsto the east,and the Yellowstoneplateau Laboratoryanalyses were performed at the Wyo- to the north.All studynests were on the valleyfloor ming StateVeterinary Laboratory. Nestling carcasses within a 226-km 2 core area in southern GTNP. The wereexamined grossly and selected tissues were col- study area extendedapproximately 29 km north lected, fixed in 10% buffered formalin, and pro- from the park'ssouthern boundary and was approx- cessedfor embeddingin paraffin.Sections for light imately10 km wide. The valleyfloor is dominatedby microscopywere sectionedat 5 to 6 I• and stained numerous river terraces with minor elevational re- with hematoxylinand eosin(Luna 1992).Some sec- lief, glacial moraines,and severaltimbered buttes tionsof skinwere stained by the periodic-acidSchiff risingfrom 150 to 300 m abovethe valleyfloor. The method. Cloacal swabs and portions of liver, lung, study area contained large areas of previously or and small intestine were collected from most car- currentlyirrigated and grazedhay lands.Elevations cassesfor bacterialculture by routinemethods (Car- rangefrom 1,890m in the valleyfloor to 4,197m atop ter and Cole 1990).Sections of skin from the neckof the surroundingmountain peaks. The climate is affectedbirds were cultured for fungi and examined characterizedby long, coldwinters and short,cool by low-power microscopyfor ectoparasites.Flota- summers.The 30-year mean maximum and mini- tions were conducted on feces collected from the co- mum monthly temperaturesduring the breeding lon or cloaca.Neck skin from two nestlingswas ex- season(March to July) were 9.5øC (range 1.5 to aminedby negative-stainelectron microscopy for vi- 16.1øC) and -4.7øC (range -12.4 to 0.5øC), respec- ruses (Nunamaker and Williams 1986). The livers tively (National Climatic Data Center 1992-1994). from four birds were examined for lead, cadmium, Approximately67% of the annualprecipitation oc- phosphorus,barium, manganese,magnesium, cal- curs in the form of snow.Human developmentsin- cium,copper, molybdenum, zinc, iron, cobalt,chro- cludedcampgrounds, houses and guest ranches, and mium, vanadium, tin, nickel, arsenic, selenium, and roads. mercuryby inductivelycoupled plasma atomic emis- We estimated blackfly abundance414 times at 42 sion spectroscopy.Brain tissuesfrom two nestlings nests from 1992 to 1994. The number of estimates at were analyzedfor cholinesteraseactivity by a mod- nests varied from 2 to 22. Of the 42 nests, 35 were ification of the Ellman method (Ellman 1961). Liver monitored from incubation to fledging, and 7 were tissuesof two nestlingswere tested for the presence monitoredfrom the early nestlingperiod to either of barbituratesby a commercialspot test (Toxi-lab, nest failure or fledging. Nest contents and blackfly Inc., Irvine, California). abundancewere monitoredusing a modifiedmirror- Minimum and maximum daily temperaturesdur- and-pole device (Parker1972) or by climbing nest ing the nestling stage were recorded at nearby trees. Blackfly infestation levels were placed into Moose, Wyoming. Temperatureswere examined four categoriesbased on estimatednumbers of black- with respectto their potentialinfluence on blackfly fliesfound aroundthe nestlingsor nest:(1) low (<50 activityat all nestsmonitored. Comparisons of max- flies),(2) moderate(50 to 200), (3) high (200to 500), imum daily temperaturesamong years were by one- and (4) severe (>500). To minimize observer vari- way ANOVA followed by Tukey's multiple compar- 370 SMITHET AL. [Auk, Vol. 115

TABLE1. Overall mortalityof Red-tailedHawks and mortalityattributed to blackfliesin northwesternWy- oming, 1992 to 1994.

Overall mortality Mortality from blackflies Year No. nests Nestlingsa Nestlings(%) Nests (%) Nestlings(%) Nests (%) 1992 14 37 19 (51.3) 8 (57.1) 10 (27.0) 5 (35.7) 1993 14 29 3 (10.3) 2 (14.2) 1 (14.2) 1 (7.1) 1994 14 28 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) Total 42 94 22 (23.4) 10 (23.8) 11 (11.7) 6 (14.3) No. nestlingsthat hatched. ison tests.Differences were consideredsignificant at known infestationduring a 10-day period be- P < 0.05. All statisticalprocedures were done using tweennest visits, and four disappearedfrom a SYSTAT for Windows (SYSTAT Inc. 1992). nestwith a low blackflyinfestation over a 4-day periodwhen young were 14 to 17 daysold. The RESULTS timing and pattern of these disappearances suggestedthat blackfliescaused the mortali- Elevenof 94 (12%)nestlings monitored died ties. However,we cannotrule out other possi- of the effectsof blackfly infestations(Table 1). Mortalities occurred in birds that were 9 to 43 ble causesof mortality,such as predation. All blackflies collected at nests were identi- daysof age,and rangedfrom 0 to 10 nestlings fied as Simuliumcanonicolum, although another annually. The onset of infestationsoccurred when nestlingswere 3 to 20 daysold andlasted speciesof Simuliumalso may havebeen present until nestlingsdied or fledged.The duration of (P. Adler pers. comm.).For the three yearsof infestationprior to nestlingmortality ranged study,mean Julian hatching date was 145 + SD from 7 to 30 days.The levelof nestlingmortal- of 6.25days (range 137 to 161days), and mean ity and thenumber of nestswith mortalityvar- fledgingage was 45.5 - 3.49 days(range 36 to ied during the three yearsof study (Table1). 50 days). Levels of ectoparasitism(Kruskall-Wallis test, Dermatitis,characterized by lossof feathers, H = 14.36,P < 0.0001)and nestlingmortality thick crusting, and folding of skin, occurred due to blackflies (G = 17.37, P < 0.0001) were with varying degreesof severityon the head, higherin 1992than in otheryears (Fig. 1). Mor- and from the intermandibular skin to the skin talities attributed to blackflies included nine overthe upper thoraxof eight nestlings(three nestlingsfound on the groundand two found males, five females) examined postmortem. in nests. In addition, nine nestlings disap- Multiple fracturesof bones(skull, long bones, peared and died of unknown causes.Of these ribs) with associatedhemorrhaging occurred nine nestlings,two were siblingsof birds found in six nestlings.Splenomegaly was prominent dead, three disappearedfrom a nest with un- in six nestlings.Tissues were pale, and the

10' 8' • []Nestling mortalities:'F[]Numberofnest• 4-

0 LowMod Highs .... LowMod Hi•gh Se'•ere L•wM•od Hi'gh S..... 1992 1993 1994 FIG. 1. Maximum level of blackfly infestationand associatednestling mortality documentedat 42 Red- tailed Hawk nestsfrom 1992to 1994in northwesternWyoming. Low = 1 to 50 flies,moderate = 50 to 200, high = 200 to 500, severe= >500. April 1998] Red-tailedHawk Mortality 371

FIe;.2. Photomicrographdepicting inflammation FIG.3. Photomicrographdepicting round micro- of skinfrom the neck of a Red-tailedHawk nestling. gamontsor microgametesof Leucocytozoon(arrows) Note the largefocus of necroticdermis (margins de- with dilatedcapillaries of the skinof the neckof an lineatedby arrowheads)and hyperkeratosis (arrow). affectedRed-tailed Hawk nestling. bloodappeared watery in sevenof eightbirds. No viruses were identified in skin by electron Microscopically,the dermatitiswas character- microscop•and no pathogenicfungi werecul- ized by dermal edema, vascularcongestion, tured. One fecal sample containedlow num- multipleareas of necrosis,dense superficial in- bersof Eimeriasp. oocysts,and sporulatedoo- filtrationof macrophagesand heterophils,and cystsof Sarcocystissp. were found in the sub- markedhyperkeratosis (Fig. 2). Roundmicro- epitheliumof the villi in the small intestinesof gamontsor macrogametesof Leucocytozoonsp. two birds. Cholinesterase levels were normal were foundin dilateddermal capillaries of af- for raptors.No abnormalitieswere detectedin fectedneck skin (Fig. 3). Megaloschizontswere the livers. Twenty-one of 28 (75%) blood presentin the spleenand kidneyof four birds. smearstaken from live nestlingsand blood Multiple areasof acutehepatic necrosis with- samplesfrom sixadditional dead nestlings that out inflammatory reaction were found in one were necropsiedtested positive for the blood bird. Severalbirds had small aggregatesof protozoanLeucocytozoon. The spleensand kid- mononuclear cells in the renal interstitium. neyswere greatly enlarged in five of the seven Therewas no microscopicevidence of signifi- (71%) nestlingsnecropsied, and megaloschiz- cantbacterial or viral infection,or of toxicolog- onts were found in four of these individuals. ical disease. Blood-suckingblowfly larvae(Protocalliphora Bacteria isolated from tissues and intestines avium)were observed in the auricularopenings of nestlingsincluded Escherichia coli, Streptococ- of 32 of 33 nestlingsbetween 4 and 11June 1992 cus,and coagulasenegative Staphylococcus sp.; and were present in some nestlings until at theseisolates were not consideredsignificant. least22 June(• = 6.7 days). In 1993 and 1994, 372 SMITHET AL. [Auk, Vol. 115 larval blowflies were detected in auricular

openingsof 21 of 21 and 29 of 29 nestlings,re- •1992 spectively. In all, larval blowflies were ob- servedin 82 of 83 nestlingsexamined. In most 993 cases,larvae completelyfilled the auricular openings.Nine larvaeoccurred in theauricular openingsof one live nestling found on the groundbeneath a nest.This nestling, estimated to be 14 daysold, alsohad larvaeon openand penetratingwounds on the neckregion and be- neathboth wings. Blackfliesburrowed through the nestlings' downy plumageto bite the skin on the neck, underwings,or aroundthe auricularopenings, and alightedto bite thehead, eye margins, and cere. Small dots and flakes of dried blood often

occurred where the blackflies had fed. Nest- PERIOD lings frequently,if not incessantly,exhibited F•O.4. Numberof daysdurinõ the nest]inõstaõe annoyancebehavior during infestations,con- when maximumdaily temperaturewas <]4øC and tinuously flapping their wings, vigorously blackflyinfestations were interrupted. shaking their heads, moving around in the nest,and pecking at exposedareas of theirbod- ies. Based on our field observations,these nestling behaviorsdid not occurwhen blackflies et al. 1975,P. Adler pers. comm.).During the were absent. blackfly life cycle,Leucocytozoon may be trans- mitted among individual birds by feeding Maximum daily temperaturesduring the blackflies.The cycle starts when blackflies nestlingperiod varied significantly(F = 19.28, emergein thespring and are infected while ob- df = 2 and 213, P < 0.0001)among the three tainingblood mealsfrom adult birds that are years of study. Blackflyabundance at nestsde- chronicallyinfected with Leucocytozoon.Spo- creasedsubstantially or ceasedwhen ambient rozoitesare thenformed, which migrate to the temperatureswere below 14øC.Ambient tem- salivary glands of infected blackfliesand are peratureswere below 14øCfor 21 days during injectedinto otherbirds, particularly nestlings, thenestling period for all yearscombined, with during subsequentfeeding (Wobeser 1981, At- annualtotals ranging from 2 to 15 days(Fig. 4). kinson and van Riper 1991,Cupp et al. 1993). Blackflyabundance at nestsdecreased as wind Under most natural conditions,up to 60% of velocityincreased, but we collectedno system- adult birdsretain their infectionfrom oneyear atic data on wind velocity. to the next (Bennet1987). A relapseof parasitemia in chronicallyinfected adult raptorsdur- DISCUSSION ing spring(P. Redig pers.comm.) may coincide with the emergenceof blackflies.Spring re- Blackfliesin the genusSimulium are nearly lapses of parasitemia in breeding ducks and cosmopolitan (Crosskey 1990). To complete geeseare well documented(Desser et al. 1968, theirlife cycle,they require moving water with 1978, Herman et al. 1975). During spring re- trailing vegetationand a bloodmeal for the fe- lapses,Leucocytozoon may be foundin sub-epi- males (James and Harwood 1979, Crosskey dermalcapillaries of the skin wherethey are 1990).Blackflies are vectorsfor a variety of par- accessibleto biting flies. asites,including nematodes and severalspecies Differences among years in blackfly abun- of bloodprotozoans (e.g. Leucocytozoon; Stabler danceat hawk nestswere at leastpartially re- and Holt 1965, Bennett 1987). Leucocytozoonlated to differencesin ambient temperatures spp.have been documented in morethan 1,000 (Fig. 4). All fly activity ceasedduring a 4-day speciesof birds in 98 families (Bennett1987) periodin June1992 when the meandaily tem- and have been found in Canada, California, perature dropped from 22.5 to 12.8øC.During and throughoutthe RockyMountains (Greiner 1993, temperaturesdropped below 14øCdur- April 1998] Red-tailedHawk Mortality 373

ing six separateperiods lasting approximately tributed to an overall weakened condition. two dayseach. We estimatedthat nestlings re- Mortality due to Protocalliphoralarvae is rare ceiveda breakfrom fly harassmentfor 15 days (Sabroskyet al. 1989).They can,however, dis- (roughly35% of the nestlingstage) during the figurethe outerear, destroy the eardrums, and 1993nestling period. This temperaturepattern contributeto anemiain nestingbirds (Borto- may help explain why infestationsdid not Iotti 1985,Sabrosky et al. 1989).Although the progressto more severelevels in 1993. In 1994, life historyof Protocalliphorain North America temperaturesdropped below 14øC for onlyfour is not well known, Sabroskyet al. (1989) re- days.However, the 1994breeding season was ported that they overwinteras adult flies,and unusuallywindy, which may haveresulted in that only dead,empty, or parasitizedpuparia a lower effective infestation level and the sub- were foundin nestsduring the fall and winter. sequentabsence of nestlingmortality that we It is notknown whether female flies lay eggsin observed(Table 1). Crosskey(1990) reported nests where larvae crawl onto the birds, or that blackfliesceased all flight activitywhen whethereggs are laid directly on the birds. temperaturesdropped to 8 to 10øCand that However,Tirrell (1978)reported fairly conclu- flight resumedwhen temperaturesrose above sive evidence that the latter occurred on Red- 13 to 15øC. tailed Hawks in North Dakota. Thus,it would appearthat breaksin infes- The causeof deathof six of the nestlingsin tationwould have the highestpotential to pre- our studywas severetrauma accompanied by vent nestingfailure from blackfliesby remov- fracturedbones and hemorrhaging. We believe ing the associatedharassment, excessive ener- that birds founddead beneath nests probably gy expenditure,dehydration, and anemia when fell or jumpeddue to harassmentby blackflies. nestlingsare young. At earlystages of nestling Blackflybites causedsevere dermatitis on the development,the effectof a reprievefrom in- head,neck, and thoracicskin of nestlings.This festationmay be similarto the effectof greater severe inflammation in the neck would have nestlingage at the onsetof infestation.More- caused considerable irritation to the birds. We over, featherdevelopment and maturationof foundno evidenceof othersignificant bacterial, theimmune system that normally occur during viral, mycotic, or toxicologicdiseases to ac- an infestationreprieve also may contributeto a count for the deaths of these birds. lower "effective" infestation level when it re- Young hawks appearedto be particularly sumes(Davidar and Morton 1993). susceptibleto blackfly bites, and thereforeto Blackflieshave been documented on raptors the transmissionof Leucocytozoonspp., when elsewherein Wyoming. R. Oakleaf and W. theywere in the nataldown stage(<25 days). Heinrich(pers. comm.) indicated that blackflies After youngwere about30 to 35 daysold, their causedconsiderable stress to PeregrineFalcons bodieswere approximately90% feathered. This (Falcoperegrinus) in the Greater Yellowstone mayhave provided some protection from flies, Area (GYA).Harmata and Oakleaf (1993)found althoughagitated behavior due to feedingby a dead Bald Eagle (Haliaeetusleucocephalus) flies was observed in nestlings until they nestlingbeneath a nestin the GYA with severe fledged or died. Chronic infectionby blood dermatitison its neckand breast. A live sibling protozoansmay have little effecton adultbirds testedpositive for Leucocytozoon,indicating ex- that survivethe initial infection(Herman et al. posureto blackflies,as did 7.3% of 96 nestling 1975, Davidar and Morton 1993). In 1993 and Bald Eaglesin the GYA (Harmataand Oakleaf 1994,more than 75% of the nestlingswe sam- 1993). Blackflies also have been observed in pledtested positive for Leucocytozooninfection, nestsof Bald Eaglesand Ospreys(Pandion hal- yet only one mortality was attributedto black- iaetus)in the GYA(G. Montopolipers. comm.). fly infestation. Parasitismof nestlingraptors by blowfliesis Althoughwe found no evidencethat Leuco- well known (Burtch 1922, Sargent1938, Hill cytozooninfection led directly to disease,the and Work 1947, Hamerstrom and Hamerstrom cumulativeeffects associated with blackflyin- 1954, Tirrell 1978, Crocall and Parker 1981, Bor- festationcould causeillness and mortality in tolotti1985). Although none of thesestudies at- nestlingsin the followingscenario: (1) harass- tributedsevere injury of nestlingsto larval in- ment by flies leadsto energyexpenditure and festations,most suggestedthat blowfliescon- prematurenest departure; (2) infectionby Leu- 374 SMITHET AL. [Auk, Vol. 115

son),researchers should design their studiesso thatthe presence and effects of blackfliescan be documentedproperly. Blood Protozoan

Harassment (Leucocytozoon) ,.• ACKNOWLEDGMENTS

Premature Nest / • DehydrationWe thank Peter Adler (ClemsonUniversity), James Departure Philips (BabsonCollege), and Erik Stauber(Wash- Damage ington StateUniversity) for identificationof blackfly specimens.We are gratefulto M. Baptiste,T. Cain,L. Carlman, M. Creel, A. Harvey,T. McFetters,M. Reid, OrganA•m••and Y. Wolfers for assistancein the field and JoelBer- ger for thought-provokingdiscussions. FIG. 5. Proposedcumulative effects of blackflies on nestlingRed-tailed Hawks. LITERATURE CITED

ATKINSON,C. m.,AND C. VAN RIPERIII. 1991. Patho- genicityand epizootiologyof avianHematozoa: cocytozoonleads to anemiaand organdamage; Plasrnodiurn,Leucocytozoon, and Haernoproteus. and (3) lossof blood from infestationsof blood- Pages19-48 in Bird-parasiteinteractions: Ecol- suckingflies leads to anemiaand dehydration ogy,evolution and behavior(J. E. Loye and M. (Fig. 5). Zuk, Eds.). Oxford University Press,Oxford. Herman et al. (1975) discussedthe impor- BENNETT,G. E 1987. Hematozoa.Pages 120-128 in tance of looking at several cumulative factors Companionbird medicine(E. W. Burr, Ed.). Iowa relatedto waterfowlreproductive success and StateUniversity Press,Ames. blackfly (S. innocens)infestation. Hunter et al. BORTOLOTTI,G. e. 1985. Frequencyof Protocalliphora (1997)speculated that owl nestlingscan recov- aviurn(Diptera: Calliphoridae)infestations on Bald Eagles (Haliaeetusleucocephalus). Canadian er from the effectsof Leucocytozooninfection Journalof Zoology 63:165-168. during years of high food supply. However, BROWN,L. H., ANDD. AMADON.1968. Eagles, hawks they did not mentionthe potential effectsof and falconsof the world. Country Life Books, weatheron blackfly infestationand associated London. owletsurvivorship. We foundno evidencethat BURTCH,V. 1922. Maggots in the ears of nestling food supplies were limited, and we propose Cooper'sHawks (Accipitercooperii). Auk 37:293. that the age of nestlingsat the time of the in- CARTER,G. R., AND J. R. COLE,JR. 1991. Diagnostic festation,the levelof infestation,and the timing proceduresin veterinary bacteriologyand my- of infestationreprieves due to coldor inclement cology,5th ed. AcademicPress, New York. weather act synergisticallyto affect nestling CRAIGHEAD,E C., ANDD. P. MINDELL. 1981. Nesting raptors in western Wyoming, 1947 and 1975. survivorship. Journalof Wildlife Management 45:865-872. The influenceof parasiteson host popula- CROCALL,S., AND J. W. PARKER.1981. Protocalliphora tions is poorly known (Toft 1991). During one infestationin Broad-wingedHawks. WilsonBul- yearof our study,blackflies reduced the repro- letin 93:110. ductive successof Red-tailed Hawks by 27%. CROSSKEY,g. W. 1990. The naturalhistory of black- Prestonand Beane(1993) reportedthat Red- flies.John Wiley and Sons,London. tailed Hawk populationsare regulatedprimar- CuPP, M. S., E. W. CuPP, AND E B. RAMBERG. 1993. ily by nest-siteavailability, food supply, and Salivary gland apyrasein blackflies(Sirnuliurn predation.Our datademonstrate that parasites vittaturn).Journal of Insect Physiology39:817- canhave a significantinfluence on the repro- 821. ductivesuccess of Red-tailedHawks and sug- DAVIDAR,P., ANDE. S. MORTON.1993. Living with gest that they contributeto the regulationof parasites:Prevalence of a blood parasite and its effecton survivorshipin the Purple Martin. Auk populations.Moreover, because the cumulative 110:109-116. effectsof blackflyinfestations can be important DESSER,S.S., A.M. FALLIS, AND P. C. C. GARNHAM. sources of nestling mortality, and because 1968. Relapsesin ducks chronicallyinfected blackfly infestationsand associatednestling with Leucocytozoonsimondi and Parahaemoproteus mortality may go undetectedin standardrap- nettionis.Canadian Journalof Zoology 46:281- tor surveys(i.e. two to threenest visits per sea- 285. April 1998] Red-tailedHawk Mortality 375

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