The Condor98~322-327 Q The CooperOrnithological Society 1996

BROWN NODDY CHICK PREDATION BY GREAT FRIGATEBIRDS IN THE NORTHWESTERN HAWAIIAN ISLANDS

JENNIFER LYNN MEGYESI~ Department of Forestry and Wildltfe Management, Universityof Massachusetts, Amherst, MA 01003

CURTICE R. GRIFFIN Department of Forestry and Wildlife Management, Universityof Massachusetts, Amherst, MA 01003

Abstract. Adult female Great Frigatebirds (Fregata minor) were responsiblefor 64% of the predatory behaviors on Brown Noddy (Anousstolidus) chicks on Tern Island, French Frigate Shoals, Hawaii. Subadultswith red orbital rings (presumably females) also preyed on Brown Noddy chicks, although they were observed hunting less frequently than adult females. No adult male frigatebirds were observed hunting in 118.3 hours of observation. Frigatebird predation likely accountedfor 95% of mortality observedin Brown Noddy chicks lessthan 24 days of age.Chicks were as likely to survive to fledgingregardless of nest location or down coloration; however, more chicks survived to fledging if hatched between mid- February and mid-May. Unequal sex ratios, sexualsize dimorphism, resourcepartitioning, and breeding strategiesof fiigatebirds were evaluated to explain why sex differences in frigatebird predation behaviors were observed on Tern Island. Kev words: Freaata minor: Anous stolidus;predation; kleptoparasitism;seabirds; sex- spec$cbehavior.

INTRODUCTION (15.0 ha), located near the northwestern tip of Frigatebirds feed on fish and squid seized at the the atoll, is the largest of ten permanent islands ocean’s surface and commonly kleptoparasitize and is the only human-made island at French seabirds.Also, three of the five speciesare known Frigate Shoals. An active coralline rubble run- to prey on seabird chicks (Diamond 1975, Nel- way extends the length of the island, while ap- son 1976). Several authors have reported fiiga- proximately 4 ha of the island is vegetated.Thir- tebird predation of seabird chicks (Beard 1939, ty-seven vascular plant species have been de- Sprunt 1948, Shea and Mahoney 1983, Ashmole scribed (Amerson 197 l), though vegetation is 1963, Schreiberand Ashmole 1970), but whether dominated presentlyby ten species(Megyesi, pers. this behavior occursat all fiigatebird colonies is observ.). The north and southeasternends of the unknown. Descriptions of the age and sex of fri- island are densely covered with Tournefortia ar- gatebirds observed preying on seabird chicks are gentea and Scaevola taccada bushesthat are be- not discussedin most of these studies. Here we tween 1.0-5.0 m in height and 1.0-4.0 m in di- report age- and sex-specificpredation behaviors ameter, while the remainder of the island is dom- of Great Frigatebirds and the effect of frigatebird inated by coralline rubble and clumps of vascular predation on Brown Noddy reproductive success plants 5 1.O m in height, including Lepturus re- on Tern Island, French Frigate Shoals, Hawaii. pens, Chenopodium oahuense, Boerhavia repens, Ipomoea pes-caprae, and Portulaca spp. STUDY AREA AND METHODS Approximately 1,700-2,500 pairs of Brown French Frigate Shoals is a crescent-shapedatoll Noddies nest on Tern Island, with fewer pairs situated approximately midway in the Hawaiian on East and Whale-Skate islands (Megyesi, pers. Archipelago (23” 45’ N, 166” 17’ W). Tern Island observ.). Excluding the runway, noddies nest on the ground over the entire island in areas where vegetation is I 1.O m in height, though approx- I Received4 October 1995. Accepted 27 February imately 2% of the Brown Noddies nest I 1.O m 1996. above the ground in Chenopodium oahuense 2 Current Address:P.O. Box 741, Truro, MA 02666. shrubs.

~3221 GREAT FRIGATEBIRD PREDATION 323

Although Great Frigatebirds formerly nested characteristic to female Great Frigatebirds. Us- on East, Whaleskate and La Perouse islands, by ing plumage coloration and feather wear to iden- 1990 all 550 pairs had moved to Tern Island tify individuals, we could estimate the minimum (Megyesi 1995). Nesting frigatebirds are concen- number of individuals hunting on each obser- trated at the north- and southeasternends of Tern vation day. Hunting events within the study plot Island in Tournefortia argentea and Scaevola were recorded as failures when the frigatebird taccada. There are no ground-nesting frigate- actively swooped down on a nest without suc- birds on Tern Island. cessfully securing prey and as takes when prey Four areas on the island were observed during was obtained. 1980-1982 and 1988-1992. Individual nests in each of the study areas were observed to deter- RESULTS mine reproductive success.Seventy-two nests in Of 2,139 Brown Noddy chicks hatched in 1980- 1980-1981 and 101 nests in 1989-1991 con- 1981 and 1989-1991, 3% (n = 73) were found taining eggsor newly hatched chicks were indi- dead in the nest, 59% (n = 1,256) disappeared vidually numbered and checked daily to deter- before 24 days of age, and 36% (n = 8 10) fledged. mine the age at which nestlingswere found miss- Mean (&SD) age at disappearancefrom the nest ing. Brown Noddy chicksare either white or dark, was 9.0 f 5.6 d (n = 173, range = O-24 days). slate-colored. In 1980-1981 and 1989, the down Most chicks (86%) disappeared between 0 and color of each of the chicks at hatching was re- 15 days of age. corded as either dark or light. Ninety-three percent of the Brown Noddy One of the study areas was used to record sea- chicks of above-ground nests and 82% of ground sonal variation in Great Frigatebird predation nests survived to fledging (n = 87 and 44, re- on Brown Noddy chicks between 21 December spectively, Fisher exact test, P = 0.11). Light- 1989 and 12 November 1992. The number of colored chicks fledged at the same rate as dark- new eggslaid, eggslost, and newly-hatched chicks colored chicks, regardlessof nest location (Fisher within this area were recorded every other day. exact test, P = 0.27). In all years, chicks that Noddy chicks that reached 21 d of age within hatched between mid-February and mid-May this plot were banded and considered fledged were more likely to survive to fledging than those while missingchicks were consideredpreyed upon hatching after this date (Fisher exact test, n = by Great Frigatebirds; dead chicks found in the 754, P < 0.001). plot were recorded and considered unrelated to We recorded 126 Great Frigatebird predation frigatebird predation. events on nesting Brown Noddies in 118.3 hr of During 1989-l 99 1, we made continuous ob- observation during ten days from 1989-1991 servations of frigatebirds hunting with obser- (Table 1). Predation occurredthroughout the day vation days based on peak Brown Noddy hatch- but was greatestduring 08:01-10:00 and 16:01- ing. No observations were made when noddies 20:00 hr (x2 = 15.70, df = 6, P = 0.02). Adult were incubating eggsor when fewer than five to females were responsible for 64% of the events; ten chicks were available, hence the lack of ob- subadults were recorded during the remaining servations during mid-January and mid-July. events; and no adult males were seen hunting. Observations began at about 06:OOhr and ceased There were a minimum of two subadults and ten at about 20:00 hr from atop a utility shed 25 m adult females identified during 118.3 observa- to the south of the study plot. For each Great tion hours, and some individuals were observed Frigatebird observedhunting within the plot, age, as many as seven times in one day. All subadults sex and outcome of each hunting event were re- observedhunting in the plot had red orbital rings. corded. Age of each individual was recorded as Though subadults were observed hunting less adult, subadult or juvenile (< 1 year of age) ac- frequently, they were successfulin obtaining prey cording to plumage. It was not possible to de- 37.8% of the time, whereas adult females were termine the breeding status of adults observed successfulduring 37.0% of the events (Pearson hunting. Sex was recorded as male or female ac- x2 = 0.007, df = 1, P = 0.93). cording to plumage. Sex of all subadults and ju- We observed no predation by Great Frigate- veniles was recorded as unknown although or- birds as a result of researchersentering the study bital ring color of subadults was recorded, as area to record Brown Noddy nest status.Nesting Diamond (1975) and Nelson (1976) attribute this Brown Noddies did not leave the nesting area 324 JENNIFER LYNN MEGYESI AND CURTICE R. GRIFFIN

TABLE 1. Great Frigatebird predation of Brown Noddy chicks on Tern Island, French Frigate Shoals,Hawaii, 1989-1991.

No. of failur& No. of takes! Hours of No. potential Date observation prey’ available Female Subadult’ FlZtlale Subadult+

12/23/89 12/24/89 11.711.5 5-10 00 : : : 01/13/90 8.8 25-30 0 01/20/90 4.0 40-50 : : : 0 07/16/90 14.0 50-100 ; 0 7 0 07/17/90 14.0 50-100 z 4 2 08/02/90 13.3 50-100 11 7 3 08/04/90 07/01/91 13.014.0 50-100 114 71 : : 07/02/9 1 14.0 50-100 7 3 2 4

’ Numbersof Brown Noddy chicksin studyplot at the beginningof eachobservation period. b Predationevent accordineto behavior observed:attempts - refer to individuals attemptingunsuccessfully to take chicks;takes refer to individuals successfullycapturing chicks: =Subadult, presumably females (see Diamond 1975, Nelson 1976). when the researcherpassed through the colony, recordedas missing. Chicks were not able to bur- but remained hovering above or diving at the row under coralline rubble, and there was no intruder. Frigatebirds were not observed keying vegetation in the study area suitable for chicks into or following in the wake of the observer. to hide and go unnoticed. We are confident that 1,256 chicks could not have been missed by re- searchersand conclude that they were taken from DISCUSSION the study area by Great Frigatebirds. PREDATION EFFECTS ON BROWN NODDY We suggestthat Great Frigatebirds were re- REPRODUCTIVE SUCCESS sponsible for 95% (n = 1,329) of mortality ob- There are no mammalian land predators within served in Brown Noddy chicks lessthan 24 days French Frigate Shoals, and the only resident of age on Tern Island. The size of the chick and predator of tern chicks on Tern Island is the wing growth may preclude frigatebirds from Great Frigatebird (USFWS personnel, unpubl. swallowing noddy chicks older than 21 days in observ., Honolulu HI 1979-1988; Megyesi, pers. fact, the five cases of predation that occurred observ. 1989-1992). after 21 days were subadults that were unsuc- Ruddy Turnstones (Arenaria interpres)and cessful in swallowing the chicks. Predation oc- Bristle-thighed Curlews (Numeniustahitiensis) curred throughout each of the observation days, are winter migrants at French Frigate Shoalsand but may have been greater between 08:00-10:00 were observed preying on Sooty Tern, Brown hr and 16:00-20:00 hr as a result of roosting Noddy, White Tern (Gygisalba) and Gray-backed frigatebirds leaving or returning to roost on the Tern (Sternalunata) eggs, but they are not known island, respectively (see also Cummins 1995). to prey on seabird chicks here or at other seabird Given the extensive period that our study colonies (Crossin and Huber 1970, Loftin and spans, Great Frigatebird predation is probably Sutton 1979, Morris and Wiggins 1986, Marks an annual occurrenceon Tern Island and a lim- and Hall 1992). We also observed ghost crabs iting factor of Brown Noddy reproductive suc- (Ocypodelaevis and 0. ceratophthalma)preying cess. Most noddy chicks were taken after they on dead and dying Pacific Golden Plovers (Plu- were exposed by brooding noddies flying up to vialisfulva)and a Wedge-tailed Shearwaterchick defend against the attacker, although some fri- (Pz.@nuspacificus); however, no ghost crabs oc- gatebirds were observed grabbing the tails of cur near the Brown Noddy study areas, and no brooding adults, lifting them from the nest into ghost crab predation of tern specieson Tern Is- the air and swooping back to the ground to re- land was documented during 1979-1992 (M. trieve the exposedchick. Both females and sub- Rauzon, B. Flint, P. Sievert, K. Niethammer, adults persisted in preying on Brown Noddy pers. comm.). From 21 December 1989 to 12 chicks despite a successrate of just 37.0% and November 1992 no Brown Noddy chicks were 37.8%, respectively. The persistencyof brooding rediscoveredin new locations after they had been noddy adults in protecting their chick, and the GREAT FRIGATEBIRD PREDATION 325 difficulty frigatebirds had locating exposedprey, on Tern Island, over 550 pairs of frigatebirds may explain these low successrates. In contrast, nest on the island. Thus, males are abundant and Cummins (1995) and Osomo et al. (1992) found it is unlikely that unequal sex ratios alone can successrates of 4.0% and 5.8%, respectively for explain why adult males were never observed kleptoparasitic behaviors. preying on Brown Noddy chicks. Although the rate of disappearance from the Gibbs and Gibbs (1987) suggestedthat male nest did not differ with respect to down colora- frigatebirds may be able to pursue prey more tion or nest location, Brown Noddy chicks may easily becauseof their lower wing-loading. Nel- have higher survival prior to mid-May when more son (1976), Fairchild et al. (1985) and Jehl and abundant and easily obtained Sooty Tern chicks Murray (1986) reported that a male frigatebird’s are available (Megyesi and Griffin, in press).Be- smaller size allows greater agility in collecting tween 55,000 and 100,000 pairs of Sooty Terns nest material and in perching atop potential nest breed on Tern Island (B. Flint, pers. comm.; Me- sites to display to females flying overhead. Our gyesi pers. observ.). We frequently observed fe- observations of female adults and subadults tak- male adult and subadult fiigatebirds taking Sooty ing Brown Noddy chicks did not suggestthat this Tern chicks from all parts of the island between type of predatory behavior requires much agility. April and July, though these observations were Additionally, the weight of l-l 5 day old Brown not quantified. Beard (1939) noted that Magnif- Noddy chick (average 28-125 g, Megyesi, pers. icent Frigatebirds preyed on Sooty Tern chicks observ.) is less than a typical fish and squid prey on the Dry Tortugas, although he found no ev- (average 122-l 80 g, Diamond 1975) suggesting idence that Brown Noddy chicks were taken. He that prey size and wing-loading ability are not attributed this to the more tenacious behavior of effecting this behavior. brooding noddy adults. Indeed, Brown Noddy Asymmetrical parental investment in chick adults on Tern Island will dive aggressively at rearing could motivate female fi-igatebirdsto for- all intruders to the colony, while Sooty Terns age closer to the breeding colony (Osomo et al. will stand and defend the nest, usually pecking 1992, Gochfeld and Burger 1981, Gibbs and at a human intruder’s hands and feet or scurrying Gibbs 1987). Diamond (1972) and Trivelpiece away when approached(Megyesi, pers. observ.). and Ferraris (1987) documented differences in Brown (1973) also noted that Sooty Tern chicks parental investment in Magnificent Frigatebirds, took significantly longer to gain mobility than wherebyfemales provided post-fledglingcare, and did Brown Noddy chicks. Both of these behav- annual breedingwas precluded.On Midway Atoll, ioral differences may make Sooty Tern chicks Gilardi (1994) observedannual breeding in male more vulnerable than Brown Noddy chicks to Great Frigatebirds, and year-old chicks were fed frigatebird predation and may explain why Brown exclusivelyby females.In contrast,Nelson (1976) Noddy chicks hatched by mid-May were more and de Vries (1984) observed both Great Fri- likely to survive to fledging. gatebird parents feeding their chicks for up to 16 months on Tower Island, Galapagos. Coello et SEX-SPECIFIC AND AGE-RELATED al. (1977) observed that male and female Great DIFFERENCES IN FRIGATEBIRD Frigatebirds shared chick rearing on Genovesa PREDATION BEHAVIOR Island, Galapagos, though males provided more Our results show that seabird chick predation by nocturnal feedings than females. We, too, ob- frigatebirds on Tern Island was sex-specific to servedthat both sexesfeed young during all stages females only. Though no comparative frigatebird of development on Tern Island during 1989- predation studies exist, a number of works have 1992. Resourcepartitioning may help to explain examined age-relatedand sex-specificdifferences the sex-specificity of predatory behaviors ob- in fiigatebird kleptoparasitic behaviors (Dia- served on Tern Island, but it does not explain mond 1972, Gochfeld and Burger 198 1, Osomo why only a few adult females and subadults ex- et al. 1992, Gilardi 1994, Cummins 1995). We hibit this behavior rather than all females, as our considered the potential effects of unequal sex data suggest. ratios, differencesin wing-loading, resourcepar- Both Gilardi (1994) and Cummins (1995) pro- titioning, parental investment, and age-related posed a correlation between the size of the fri- foraging ability to explain our findings. gatebird and the host’s size, where the smaller Although roosting females outnumber males males kleptoparasitized noddies and Wedge- 326 JENNIFER LYNN MEGYESI AND CURTICE R. GRIFFIN tailed Shearwaters, and the larger females pre- BEARD,D. B. 1939. Man-o’-war-birds prey on East- ferred Masked Boobies(Sula dactylatra)and Red- em Sooty Terns. Auk 56327-329. tailed Tropicbirds (Phaethon rubricauda). Our BROWN,W. Y. 1973. The breeding biology of Sooty Terns and Brown Noddies on Manana or Rabbit observations of females foraging for Brown Nod- Island, Oahu, Hawaii. PhD. diss. University of dy chicks at the colony suggestthat feeding areas Hawaii, Oahu. and energy requirements rather than prey size COELLO,F., C. HERNAND~, ORTEGA,M. L., AND TJ. could partition the sexes. DE VRIES. 1977. Reproduction y frecuenciaali- menticia de Fregata minor en Genovesay Fregata We found no differences in foraging success magnifrcensen Seymour, Galapagos._ - Rev. de la between adult female and subadult Great Fri- U&Catolica delEcuador 5:71-l 10. gatebirds, though we only observed subadults CROSSIN.R. S.. AND L. N. HLJBER.1970. Sootv Tern during 36% of the events. In contrast to our re- egg predation by Ruddy Turnstones. Condor 72: 372-373. sults, Gilardi (1994) found that successof Great CUMMINS,R. E. 1995. Sex-biasedhost selectionand Frigatebird kleptoparasites improved with age successof kleptoparasitic behavior of the Great on Midway Atoll, and Ashmole (1963) suggested Frigatebirdin the Northwestern Hawaiian Islands. that subadult frigatebirds on Ascension Island Condor 97:811-814. were lessefficient in capturing Sooty Tern chicks DE VRIES,TJ. 1984. Why are Frigate-Birds colonial? Noticias de Galapagos40: 19-22. than were adults, although differences were not DL~MOND, A. W. 1972. Sexualdimorphism in breed- significant. The subadultswe observedmay have ing cycles and unequal sex ratio in Magnificent been specialists who were highly proficient in Frigate-Birds. Ibis 114:395-398. hunting noddy chicks. DIAMOND.A. W. 1975. Biology and behavior of Fri- gatebirdsFregata spp.on Aldabra Atoll. Ibis 117: Given the relatively small proportion of fri- 302-323. gatebirds that hunt seabird chicks on the island, FAIRCHILD,L., S. A. MAHONEY,AND R. W. SCHREIBER. we suspectthat this behavior is not widespread 1985. Nest material preferencesof Great Frigate- throughout the Tern Island frigatebird colony. birds. J. Field. Omithol. 56:236-245. Thus, only a limited number of fiigatebirds prac- GIBBS, H. L., ANDJ. P. GIBBS. 1987. Prey robbery by non-breeding Magnificent Frigatebirds (Fregata tice this foraging behavior. Resourcepartitioning mug&ens). Wilson Bull. 99:101-104. and differences in energy requirements may in GILARDI,J. D. 1994. Great Frigatebird kleptopara- part explain why this behavior is sex-specificto sitism: sex-specific host choice and age-related females, but studies of marked individuals are proficiency. Condor 96:987-993. GOCHFELD, M., AND J. BURGER. 1981. Age-related needed to understand what motivates these few differencesin piracy of Frigatebirdsfrom Laughing female adults and subadults to prey on seabird Gulls. Condor 83:79-82. chicks on Tern Island. It is clear, however, that JEHL,J. R., JR., AND B. G. MURRAY,JR. 1986. The the impact of these individuals is substantial on evolution of normal and reverse sexual size di- reproductive successof Brown Noddies breeding morphism in shorebirdsand other birds, p. l-76. In R. F. Johnson [ed.], Current Ornithology. Vol. between mid-May and mid-February. 3. Plenum Press, New York. Lorrr~, R. W., AND S. Surro~. 1979. Ruddy Tum- ACKNOWLEDGMENTS stones destroy Royal Tern colony. Wilson Bull. 91:133-135. We thank the many staff and volunteers at the North- MARKS, J. S., AND C. S. HALL. 1992. Tool use by westernHawaiian Islands National Wildlife Refugefor Bristle-thighedCurlews feeding on Albatross eggs. help in collecting these data, especially John Andre, Condor 94: 1032-1034. Beth Flint, Ken Niethammer, Darcy Hu, Paul Sievert, MEGYESI, J. L. 1995. Breeding biology of the Brown Mitch Craig, Scott Hall and Ken McDermond. We also Noddy Anous stoliduspileatus on Tern Island, thank Stanley Lemeshow and Thomas French, James Hawaii. M.Sc.thesis. Univ. MassachusettsAm- Gilardi and an anonymous reviewer for suggestions herst. and commentson an earlier version of this manuscript. MEOYESI,J. L. AND C. R. GRIFFIN. 1996. Breeding biology of the Brown Noddy Anousstolidus pilea- LITERATURE CITED tus on Tern Island, Hawaii. Wilson Bull.: in press. MORRIS,R. D., AND D. A. WIGGINS. 1986. Ruddy AMERSON,A. B., JR. 1971. The natural history of Turnstones,Great Homed Owls and eggloss from French Frigate Shoals,Northwestern Hawaiian Is- Common Tern clutches.Wilson Bull. 98: 10l-l 09. lands. Smithsonian Inst., Atoll Res. Bull. 150. NELSON,J. B. 1976. The breeding biology of frigate- Washington, DC. birds, a comparative review. Living Bird 14:113- ASHMOLE,N. P. 1963. The biology of the wideawake 156. or Sooty Tern Sternafuscata on AscensionIsland. OSORNO,J. L., Tomuss, R., AND C. MACLAS GARCIA. Ibis 103b:297-364. 1992. Kleptoparasitic behavior of the Magnifi- GREAT FRIGATEBIRD PREDATION 327

cent Frigatebird: sex bias and success.Condor 94: chicks (Sterna flcata). Abstract. Pac. Seabird 692-698. Group Bull. 10:55-56. SCHREIBER, R. W., ANDN. P. ASHMOLE.1970. Seabird SPRUNT,A., JR. 1948. The tern colonies of the Dry breeding seasons on Christmas Island, Pacific Tortugas Keys. Auk 65: 1-19. Ocean. Ibis 112:363-394. TRIVELPIECE,W. Z., ANDJ. D. FEFCRARIS. 1987. Notes SHEA,R. E., AND S. A. MAHONEY. 1983. Great Fri- on the behavioural ecologyof the Magnificent Fri- gatebird (Fregata minor) predation on Sooty Tern gatebird Fregutu mugnzjicens.Ibis 129:168-174.