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Home , Booby, Cormorant, Frigatebird, Magnificent frigatebird

The Condor94692498 Q The CooperOmithological Society 1992

KLEPTOPARASITIC BEHAVIOR OF THE MAGNIFICENT : SEX BIAS AND SUCCESS ’

J. L. OSORNO,R. TORRESAND C. MACIASGARCIA Centro de Ecologia, UniversidadNational Autdnoma de Mtixico. A. P. 70-275, DelegacibnCoyoachn. C. P. 04510, D.F.,

Abstract. (the stealingof food) by the (Fregata magnijicens)was recorded over three breeding seasonsat Isla Isabel, Nayarit, Mexico. Observation of chaseson the principal target, the Blue-footed (&la nebouxii) were made in front of their joint breeding colonies. Most attacks were conducted by female and juvenile ; male fiigatebirds were not kleptoparasiticnear their breeding colony. The proportion of chasesprovoking the target to regurgitate(success rate) was low (0.059) and only on 67% of those casesdid the fiigatebird get any food. Attacks were more frequent in the afternoon, when the were returning to their breeding colony and were likely to be transporting food. In addition, frigatebirds may be evaluating the target’s profitability in short chases, since longer chasesprovided a proportionately higher success.If so, the successreported above underestimatesthe profitability of these behaviors becauseit con- siders all chasesequally. Group pursuits were three times more successfulthan those per- formed by single individuals. We did not find differences in the successand sexual bias in the kleptoparasitictendencies between winter (frigatebirds’ courtshipand laying season)and spring (tiigatebirds’ feeding season)observations. Kev words: Kleutouarasitism;_fiigatebirds; - foraging success;foraging sexual bias; sea- ;diet.

INTRODUCTION For some speciesof birds, piracy contributes Kleptoparasitism, or piracy, is defined as the significantly to an individual’s diet (Brockmann stealing of food (Curio 1976, Brockmann and and Barnard 1979, Fumess 1987, Thompson Barnard 1979, Barnard 1984). This is a foraging 1986). Piracy seemsto disproportionately occur pattern which reducesthe cost (energy and risks) in raptors and marine birds (Brockmann and associatedwith direct foraging, but requires that Barnard 1979). In frigatebirds (Fregata spp.) the pirates successfullyout-maneuver their vic- kleptoparasitism is mainly performed on boo- tims (hereafter referred to as targets; Gochfeld bies (Mu spp.). It has often been reported as an and Burger 1983, Barnard 1984). If kleptopar- important alternative to direct fishing by fiigate- asitism produces a greater return or a lower cost birds (Nelson 1975). In fact, the highly acrobatic than direct foraging, natural selection should fa- capabilities of these have been inter- vor such specialization (Barnard 1984, Vollrath preted as an adaptation to kleptoparasitism (Nel- 1984). Brockmann and Barnard (1979) conclud- son 1975, Brockmann and Barnard 1979, Fur- ed that kleptoparasitism may be profitable when ness 1987). However, the scanty evidence several ethological and ecological factors exist: indicates poor performance of frigates in piracy. (1) the pirates need to be opportunistic feeders Fumess (1987) found no difference in the success with acrobatic flying capabilities, (2) large host rate of frigatebirds, skuas,jaegers and generalist concentrations in open habitats must occur (also pirates such as . Some incidental reports in- Paulson 1985), and (3) hosts must predictably dicate low successrate as well as differences in transport large quantities of food to a fixed place. frequency and successof piracy between males In addition, the incidence of kleptoparasitism in and females, and among different age classesand seabirds seems to be more frequent in surface- localities; such reports do not mention the con- feedingseabirds than in speciesthat dive or plunge text in which kleptoparasitism occurs. to get their food (depth hypothesis; Due 1980, Theory predicts that frigatebirds could reduce 1982). costsby evaluating the profitability of potential targets, and by searching for targets when and 1Received 20 November 1991. Accepted 1 May where there is a high probability of them carrying 1992. food (Fumess 1987). Here we report on sexual

[6921 KLEPTOPARASITISM IN FRIGATEBIRDS 693 bias, profitability, successrates and mechanisms TABLE 1. Absolute frequency(percent) of chasesby to reduce costs of piracy by fiigatebirds. frigatebirdson severalspecies of seabirdsfound on Isla Isabel. On Isla Isabel, kleptoparasitism by the Mag- nificent Frigatebird (Fregata magnificens)on the Identity of the targets’ FR&pellCy w Blue-footed Booby (Ma nebouxii) combines characteristicssuggested by Brockmann and Bar- Magnificent Frigatebird nard (1979) as likely to promote the (Fregata magm$cens) 5 (0.24) Blue-footed Booby of avian piracy. Frigatebirds harassthe target by (Sula nebouxiQ 1,723 (84.13) chasing closely, often pulling its tail , thus unbalancing and frequently causing the vic- (S. leucogaster) 179 (8.74) tim to fall into the sea. If the target regurgitates, Heermanns’ the pirate stopspursuit and takes the food before (Larus heermanm) 107 (5.22) Brown it falls into the sea. This style of piracy contrasts (Pelecanusoccidentalis) 12 (0.59) with the stealing-from-the- technique used Sooty by frigatebirds against other (e.g., gulls; (Anousstolidus) 3 (0.15) Gochfeld and Burger 1983). Tropic (Phaethon aethereus) 19 (0.93) STUDY AREA AND METHODS Red-footed Booby (S. sula) 0 (0.00) We recorded the kleptoparasitic behavior of the Total 2,048 Magnificent Frigatebird on Isla Isabel, Nayarit, *S&XCieS~WMlg.X I in of decreasingabundance on the Island. Mexico (21’5 l’N, 105’54’W) in three annual vis- ~;~$=,n,ode”ab’e.!~gum on the nu@ers of birds of any specieson its totaling 19 days (13-19 December 1985, 19- {~u~~~$ti&t 26 December 1986 and 7, 8, 10 and 11 June 1987). These birds breed on Isla Isabel together with three speciesof boobies and other Pelecan- iform birds. The observations were made from or until the parasite moved out of the target’s two siteson the east side of the island: Las Monas path. In some instances, the chasedbird fell into Beach, in front of a breeding colony of Blue- the sea. When this happened, the frigatebird of- footed Boobies (1985, 1986 and 1987), and the ten circled over it for several seconds,and some- Acantilado Oriental (1985 and 1987), in front of times resumed the chase if the chased bird at- a roosting place for Blue-footed and Brown Boo- tempted to fly. In thesecases, a chasewas judged bies. Pairs of observers (observer and recorder) to have terminated when the fiigatebird finally recorded all chasesthat occurred over the beach left the target. From 1986, we differentiated those and sea within 200 m of the observation points, chasesperformed by single birds from those car- where virtually all the interactions occur. A chase ried out by groups (group size, n 2 2), although was defined as any interaction starting with a we were unable to accurately assessthe number frigatebird positioning itself behind, and subse- of frigatebirds on a group chase. quently following closely, any flying bird. Con- In 1987, we also recorded the frequency of tinuous observations were made from O7:3O to arrivals and departures of Boobies to and from 17:30 hr using 8 x 30 or 8 x 50 binoculars. their breeding area and roosting place. Teams alternated every two hours. Distinct pat- RESULTS of plumage coloration allowed us to make a reliable assessmentof the age class and sex of SPECIES CHASED AND SUCCESS RATE the pirate in each chase (Nelson 1975). Regur- In total we recorded 2,048 kleptoparasitic chases. gitation by the target was used as the criterion The most frequent targets were sulids, mainly of success.For each chase we recorded time of the Blue-footed Booby; gulls and other seabirds day, age and sex of pirate (male, female or ju- were attacked much less frequently (Table 1). venile), speciesof the target (also from plumage), Frigatebirds were equally successfulin robbing and successor failure of chase. In the case of the two most common species of sulids (Blue- successfulchases, we recordedwhich bird(s) ben- footed Booby, n = 1,723,5.6% successful;Brown efited by obtaining all or part of the pirated food. Booby S. leucogaster,n = 179, 5.0% successful; Additionally, we recorded the duration of the G-test = 0.1, df = 1, P > 0.05). chase from its initiation until successfulpiracy Piracy near the island against Blue-footed Boo- 694 J. L. OSORNO, R. TORRES AND C. MACIAS GARCIA

TABLE 2. Frequency of success(%) of chaseson Blue-footed Boobies by sex and age classof the fiigatebirds.

Females Males Juveniles Breeding season YGU SUCCW n SUCCeSS n SUCCeSS n

E=lY 1985 48 (5.1) 938 4 l(l.3) 76 Early 1986 27 (7.1) 379 4 2 (15.3) 13 Late 1987 16 (6.7) 236 0 6 (3.7) 162 Both Total 91 (5.8) 1,553 8 9 (3.6) 251

bieswas mostly carried out by females(n = 1,553) a and juveniles (n = 162). Males only rarely chased other birds near their breeding area (n = 8; Table 2). We have no data on whether some individuals had a greater tendency to engagein kleptopara- sitism than others, nor the number of potential

-0.6 pirates simultaneously present at the observation sites. Absolute successof kleptoparasitism was low; only 91 of the 1,553 chasesinitiated by females against Blue-footed Boobies resulted in regurgi- tation (5.8%), and only 58 ofthese casesresulted 4 20 36 52 66 64 100116160 in gain for the pirate. There was no significant difference between the value for females and the mean value (3.7%) for juveniles (G-test = 1.28, b df= 1, P > 0.05). ATTACKS ON BLUE-FOOTED BOOBY Considering only the successful chases by fe- males on Blue-footed Boobies (n = 9 l), fiigate- birds that joined but were not necessarilypresent at the onset of the chasebenefited in 22 instances (24.2%). Heermann’s Gull (Law heermannz], reported elsewhere to be both targets and para- sites of frigatebirds (Brockmann and Barnard 1979), joined the chasesopportunistically at Isla 4 20 36 52 66 64 100116160 Isabel, obtaining a substantial proportion of the rewards (43 of 9 1 successfulchases, 43.3%). Considering all the chasesperformed by adult females against Blue-footed Boobies (n = 1,153), frigatebirds were more successfulin front of the

1

0.0 t FIGURE 1. Frequency of piracy (bars) and relative 0.6 success(line) as a function of the duration of the chase. Chasesby singlebirds (a) and groupsib), distinguished 0.4 only in the records of 1986 and 1987, did not differ significantly in their time distributions (Kolmogorov- 0.2 Smimov test, D = 0.2353, n = 17 time-intervals, P > 0.1). In (c). all the data from 1985, 1986 and 1987 are 0 plotted together;the proportion of successin long chas- 4 20 36 52 66 64 100116166 es is higher than in short ones, but the small numbers of lengthy interactions render non-significant the cor- Duration of chase relation (Spearman’s p = 0.158, P > 0.1). KLEPTOPARASITISM IN FRIGATEBIRDS 695

j-0.1

300

2 250

5 200

$ 150

c 100

50

0 7:oo 9:oo ll:oo 13:oo 15:oo Hour of day FIGURE 2. Frequencyof piracy(bars) and proportionof success(line) by hour of day.

target’s breeding place (7.0%, n = 1,09 1) than in and late (7.3%, n = 236; G-test = 0.42, df = 1, front of the roosting place (3.0%, n = 462; P > 0.05) part of the frigatebird breeding season. G-test = 9.54, df = 1, P < 0.01). Additionally, group attacks were three times more successful DISCUSSION than the ones conducted by single individuals (group 15.0%, at = 140; single 5.1%, n = 432; SPECIESOF BIRD CHASED G-test = 12.28, df = 1, P < 0.001). Most chases The bias toward attacking Blue-footed Boobies (46.2%) between female frigatebirds and Blue- is probably related to the abundance of these footed Boobies were of short duration (range I- birds on Isla Isabel, especially near the obser- 8 set). However, relative successwas greater in vation sites.The Red-footed Booby (S. sulu), the longer chases(Fig. l), a pattern that was apparent most common reported target of F. magnificens for both chasesmade by singlebirds and by groups elsewhere(Nelson 1975, Diamond 1975), is very (Fig. la, b). rarely found on Isla Isabel (10 nestsin 1987, pers. Chases were more frequent in the afternoon, observ.). but the proportion of successwas independent Although there are reports of differential pi- of both frequency of chases(Spearman ’s p = 0.15, racy successof frigatebirds on several speciesof P > 0.05) and hour of occurrence (p = 0.17, P seabirds in other locations (Nelson 1975, Dia- > 0.05; Fig. 2). Frigatebird piracy concentrated mond 1975), our data show similar successrates on boobies arriving at the breeding colony (p = against Blue-footed and Brown Boobies, proba- 0.7 1, P < 0.022) rather than those departing for bly suggestingthat thesetwo speciespose similar the sea (p = -0.74, P < 0.015; Fig. 3a). Boobies robbing difficulties. arriving are more likely to be returning with food SEXUAL BIAS IN PIRACY (Anderson and Ricklefs 1987). At the boobies’ roosting place, the activity patterns of both par- The sexual bias in the tendency of frigatebirds asite and target were different (Fig. 3b). Here the to chase sulids near Isla Isabel does not seem correlations between the frequency of piracy and related to the disproportionate abundance of fe- the frequenciesof arrivals or departuresof targets males in the colony. Adult males were not re- were not significant (arrivals: p = -0.12, P > corded to engagein kleptoparasitism in Decem- 0.05; departures: p = -0.27, P > 0.05). The ber when the sex ratio is nearly 1, nor in June proportion of successfulchases did not vary sig- when the sex ratio is strongly female-biased as a nificantly between the early (6.0%, n = 1,3 17) result of seasonal male nest-desertion (Nelson 696 J. L. OSORNO, R. TORRES ANDC. MACIAS GARCIA

artures

. ..x-.. , ’ I I I I I J ok ’ f ’ 7 6 9 IO 11 12 13 14 15 I:

b

70r

, I I , / I / I J 0’ 7 6 9 10 11 12 13 14 15 160

Hour of day

FIGURE 3. Mean frequenciesof arrivals and departuresof the Blue-footed Boobies to/from (a) their breeding colony, and (b) a much visited roosting site; and mean frequency of frigatebird chases over the day. Data presented are 4-day averages.

1975, Trivelpiece and Ferraris 1987). Sex bias ger 1983). Since we did not observe feeding at may occur because males tend to feed far from other places, we have no data to test this idea. their nesting place, while females prefer to feed Females may parasitize in responseto the chicks’ closeto their breeding colony (Gochfeld and Bur- need to be fed frequently, thus making it prof- IUEPTOPARASITISM IN FRIGATEBIRDS 691 itable to fly a few tens of meters off the nest to itability of potential targetsat a distance (Furness chase a passing booby. 1987, Thompson 1986). A pirate may reduce kleptoparasitic costs if it evaluates the profit- ADULTS AND JUVENILES ability of targets. The low frequency of success In contrast to evidence from other seabirds (Or- and subsequently higher successof longer chases ians 1969, Brant 1984, Hesp and Barnard 1989) may suggestthat in the first few secondsof pur- and from frigatebirds in somewhat artificial con- suit the frigatebirdsmay obtain information about ditions (observations were helped by providing the profitability of continuing the chase. If the food to the birds; Gochfeld and Burger 1983), short chasesare the local strategy to obtain in- successrates of females and juveniles did not formation about the target’s profitability as op- differ significantly. However, overall adult effi- posedto, for instance, watching the potential tar- ciency in provoking the target’s regurgitation was getsfrom a long distance (seeFurness 1987), then 0.6 times higher. An inadequate sample of ju- the successrate of piracy reported here is an venile chasescould be responsible for this result underestimate of the real profitability. In that as somejuveniles might have had several months case, our estimates of profitability cannot be di- of experience at attempting piracy. rectly compared with those previously reported in the literature. GROUP CHASES The search for targets, in places and at times The chasesperformed by groups were more suc- predictably more profitable, should enhance the cessful than the ones conducted by a single in- probability of successof this feeding pattern by dividual (see also Barnard 1984). However, it diminishing the sampling costs.The greater pro- would require an averagegroup size of only three portion of successfulattacks and the strong pos- individuals (which is very likely an underesti- itive associationof piracy with the arrival of food- mate) to make the per-capita rate of successfrom bringing boobies at their breeding place suggest group chasesequal to that of individual chases. that the approaching of the potential target to its The data collected do not show whether the nesting colony provides the most profitable con- greater successin group chasesis due to an en- dition. hanced ability to harassthe target or whether the It has been suggestedthat surface-fishingbirds group arisesopportunistically when a chaseseems are subject to wider fluctuations in food avail- likely to succeed.Absence of differences in time ability and are thus more prone to engage in distributions between group and single chases kleptoparasitism than plunging/diving species supports the idea of enhanced harassment by (Dully 1980, 1982). This could explain why frig- groups (Fig. la, b). atebirds chaseand steal for food, but data on the contribution of direct fishing to the diet of fri- PROFITABILITY gatebirds are needed to evaluate the real profit- It is unexpected for a kleptoparasitic specialist ability of kleptoparasitism. to have such a low successrate of piracy, the lowest yet reported (5.4%) compared with 12% ACKNOWLEDGMENTS on Galapagos on Red-footed Booby (Nelson 1975) 18% in Aldabra on Red-footed Booby We are gratefulto Marcela Osorio-Benstain,Cecilia (Diamond 1975) and 63% on Garcia,Maria Guerraand TeresitaArias for helpwith the field work. Thesedata were gatheredduring the on Red-footed Booby (Nelson 1975). This low field portions of three behavioral ecologycourses, and profitability seemseven more striking when the were-obtained by several students of the. Facultad de frequency of theft of the regurgitated food by the Ciencias0fU.N.A.M. CarlosCordero. Linden Hiaains. opportunistic Heermann’s Gull is considered,al- Fedro Guillen, William Sutherland, &lay Mack&zie and two anonymousreviewers made helpful comments most half of the successfulchases resulted in no on the manuscript. L. Higgins kindly helped with the gain for the fiigatebirds. Kleptoparasitism seems English translation of the manuscript. Financial sup- to be a poor feeding strategy at this location. port was provided by Facultad de Ciencias, U.N.A.M. However, if direct fishing is also costly or prey Logistic support was generouslyprovided by Dr. H. scarce,this strategycould make a significant con- Drummond and Centro de Ecologia, U.N.A.M. The Secretariade Desarrollo Urban0 y Ecologla provided tribution to their diet. the correspondingresearch permission. Fishermen from Since boobies carry their food in the gut, the San Blas and Boca de Camichin, Nayarit contributed frigatebird may not be able to evaluate the prof- in several ways. 698 J. L. OSORNO, R. TORRES AND C. MACIAS GARCIA

LITERATURE CITED GCCHEELD, M., AND J. BURGER. 1983. Age-related differencesin piracy of frigatebirds from Laughing ANDERSON, D. J., AND R. E. RICKLEFS.1987. Radio- Gulls. Condor 83:79-82. tracking Masked and Blue footed Boobies (S&I HESP, L. S., AND E. J. BARNARD. 1989. Gulls and spp.) in the Galapagos Islands. Nat. Geogr. Res. plovers: age-related differences in kleptoparasit- 3:152-163. ism among Black-headed Gulls (Larus ridibun- BARNARD,C. J. 1984. The evolution offood-scroung- dus). Behav. Ecol. Sociobiol. 24~297-304. er strategieswithin and between species, p. 95- NELSON, J. B. 1975. The breeding biology of frigate- 126. In C. J. Barnard red.], Producersand scroung- birds: a comparative review. Living Bird 14:113- ers: strategies of exploitation and parasitism. 155. Chapman & Hall, New York. OIUANS,G. H. 1969. Age and hunting successin the B~ANT, C. A. 1984. Age and hunting successin the Pelecunusoccidentalis. Anim. Be- brown pelican: influencesof skill and patch choice hav. 17:316-319. on foraging efficiency. Oecologia 62: 132-l 37. PAULSON, D. R. 1985. The importance of open hab- BR~CKMANN, H. J., ANDC. J. BARNARD. 1979. Klep- itat to the occurrence of kleptoparasitism. toparasitism in birds. Anim. Behav. 27:487-5 14. 1023637439. CURIO,E. 1976. The Ethology of . Springer THOMPSON, D.B.A. 1986. The economics of klepto- Verlag, Berlin. parasitism: optimal foraging, host and prey selec- DIAMOND, A. W. 1975. Biology and behaviour of tion bv aulls. Anim. Behav. 34: 1189-1205. frigatebirds Freguta spp. on Aldabra Atoll. Ibis TRIVELPIE&~~. Z., AND J. D. FERRARIS. 1987. Notes 117:302-323. on the behavioural ecology of the Magnificent DUFFY, D. C. 1980. Patterns of piracy by Peruvian FrigatebirdFregutu mgnificens. Ibis 129:168-l 74. seabirds:a depth hypothesis. Ibis 122:521-525. VOLLRATH, F. 1984. Kleptobiotic interactions in in- DUFFY, D. C. 1982. Patterns of piracy in the seabirds vertebrates, p. 61-94. In C. J. Barnard [ed.], Pro- communities of the GalapagosIslands and south- ducers and scroungers:strategies of exploitation em Africa. 10:7l-80. and Parasitism. Chapman & Hall, New York. FURNESS,R. W. 1987. Kleptoparasitism in seabirds, p. 77-100. In J. P. Croxall [ed.], Seabirds:feeding ecologyand role in marine ecosystems.Cambridge Univ. Press, Cambridge, .