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Age differences in kleptoparasitism by laughing gulls (Larus atricilla) on adult and juvenile brown pelicans (Pelecanus occidentalis)
Anirn. Behav., 1985, 33, 201-205
Age differences in kleptoparasitism by laughing gulls (Larus atricilla) on adult and juvenile brown pelicans (Pelecanus occidentalis) S C O T T P. C A R R O L L * & K E N N E T H L. C R A M E R
Department of Zoology, University of Oklahoma, Norman, OK 73019, U.S.A. Abstract. We recorded the choice of victims by a population of adult and first-winter laughing gulls (Larus
atrieilla) making attempts to steal food from adult and juvenile brown pelicans (Pelecanus oeeidentalis). Adult gulls made food theft attempts on juvenile pelicans with a disproportionately great frequency; first-winter gulls appeared to select pelican victims at random. Adult pelicans were more frequently successful in their foraging attempts than juvenile pelicans, suggesting that adults may be more reliable as potential food sources for gulls making theft attempts. However, juvenile pelicans attempted to evade kleptoparasitizing gulls less frequently than did adult pelicans, suggesting that the fish prey of juveniles may be more easily stolen. These patterns are discussed in relation to optimal victim choice by gulls, and to deferred maturity in both species.
Kleptoparasitism is the theft of food or other items. It has been described in many avian families, but appears to be particularly common among gulls (Brockmann & Barnard 1979). Gulls of several species may rely on kleptoparasitism for a significant proportion of their food intake (Ingolfsson 1969; Hatch 1970; Fuchs 1977; K/illander 1977). Age has been shown to correlate positively with foraging success in a variety of avian species (e.g. Tinbergen 1953; Orians 1969; Dunn 1972; Verbeek 1977a,b; Ingolfsson & Estrella 1978; Searcy 1978; Burger et al. 1980; Quinney & Smith 1,980). In general, adults exhibit higher attempt and capture rates than immatures. Orians (1969) observed that adult brown pelicans (Pelecanus oceidentalis) caught prey on a significantly greater percentage of dives than did juveniles, and Burger et al. (1980) described similar findings in age classes of laughing gulls, Larus atricilla. Foraging success via kleptoparasitism may improve with age as well. Burger & Gochfeld (1979) found that adult ring-billed gulls (Larus delawarensis) were more successful than juveniles in taking food from starlings (Sturnus vulgaris). Under conditions of artificial provisioning, Burger & Gochreid (1981) found that adult laughing gulls were more successful than young at intraspecific kleptoparasitism. However, Verbeek (1977a,b) found no positive association between age and kleptoparasitism success in herring gulls, Larus argentatus. In addition, while Burger et al. (1980) report significant age differences in frequencies of attempted * Present address: Department of Biology, University of Utah, Salt Lake City, Utah 84112, U.S.A.
kleptoparasitism for laughing, herring and ringbilled gulls at garbage dumps, they found no such differences in success rates. Gochfeld & Burger (1981) observed the same patterns in adult and juvenile kleptoparasitic frigatebirds, Fregata mag-
n~een~. In this study we investigate the relationship between the age of laughing gulls and their frequencies of kleptoparasitic attempts on brown pelicans of two age classes. We hypothesize that differences between adult and juvenile pelicans in their foraging success and evasive ability may make these two age classes resources of different availability for gulls. Specifically, if adult pelicans capture fish on a greater proportion of dives than juvenile pelicans, gulls may preferentially kleptoparasitize adult pelicans as a more reliable resource. If adult pelicans are more able to avoid kleptoparasitism than juveniles, gulls may preferentially kleptoparasitize juvenile pelicans as a more exploitable resource. If these two potential factors operate together, or neither is important, gulls may show no preference. In addition, we predict that adult gulls are more sensitive than first-winter gulls to any differences in resource availability that might exist between pelican age classes, and exploit them accordingly.
201
METHODS
We conducted our study on 9, 10 and 11 January 1982 along a sandy 3-km section of Miramar Beach (Playa Miramar) on Santiago Bay (Bahia Santiago), approximately 10 km northwest of Man-
Animal Behaviour, 33, 1
202
zanillo, Colima, Mexico. We classified the brown pelicans into two age groups, adult and juvenile, on the basis of easily distinguishable head coloration patterns (Bent 1922). Subadult birds were rarely observed and were grouped with adults. Laughing gulls were also grouped into two age classes: first-winter birds, with a dark head and wings and a dark terminal tail band; and adults in winter plumage, with light head and wings and no tail band. This 'adult' population included a small proportion of second-winter individuals. We observed gull-pelican interactions with 10 x 50 binoculars from positions 10-20 m above the water line. Each time we saw a brown pelican plunge-dive, we recorded the following data: (1) age-class of pelican; (2) success or failure in fish capture, as indicated by the presence of absence of a swallowing motion (Orians 1969); (3) attempts at kleptoparasitism, which we defined as any laughing gull within 1 m of the pelican between the time that the pelican rose to the water surface after diving and the time of swallowing (or departure of the gulls if the dive was unsuccessful); (4) success or failure of kleptoparasitism for gulls of each age class; (5) evasive behaviour of the pelicans. The two evasive behaviours observed were: 'turning in place', in which a recently surfaced pelican rotated from side to side away from gulls, and 'short flight', in which a pelican flew 15-30 m away from the site of resurfacing, swallowing en route. In addition, the proportions of adult and juvenile pelicans and gulls in the local population were assayed from resting groups of each species.
RESULTS Each day about 150 brown pelicans hunted in the surf within 50 m of shore. They were most active from dawn (0730 hours) to 1000 hours, and also hunted in groups between about 1200 and 1400 hours and just before dusk (1630 to 1730 hours). During these periods, several groups of hunting pelicans were present among the breakers, usually moving upwind and diving along the way, then circling back and covering the same area again. Hunting groups were always accompanied by laughing gulls, which flew among the pelicans and rapidly approached diving individuals, Pelicans were accompanied by gulls on 87-2~ of all dives (N = 472), with a mean of 2-0 gulls present per dive. The gulls attempted to take fish protruding from
the pelicans' bills or from the surface of the water near the pelicans. This was done by hovering near a pelican's head, alighting on its head or back, or alighting on the water next to the pelican. When not hunting, the pelicans floated in several groups about 50--75 m offshore. At such times, the gulls rested on the water near them and were generally inactive until the pelicans resumed hunting, at which time the gulls resumed kleptoparasitic behaviour. There were approximately 250 laughing gulls in the study area. In six groups of resting brown pelicans, 55 adults (40. IX) and 82 juveniles (59.9~) were present. In three groups of resting and one group of active laughing gulls, 11 adults (16"7~o) and 55 first-year birds (83.3~) were present. Of 472 pelican dives observed, 295 (62.5~) were made by juveniles, and 177 (37.5~) were made by adults. In the 443 dives for which success or failure was recorded, 227 (81.9~) were successful for juveniles, and 145 (87.3~) were successful for adults (G = 2.31, P > 0.1). These data are a subsample of those collected in concurrent observations by Schnell et al. (1983), which showed adults to be significantly more successful (G = 28.74, P < 0-001, N = 2449). The common prey were schooling fish less than 10 cm long that inhabited the surf in water 1-2 m deep. Of 941 kleptoparasitism attempts observed, 79.3~ (746) were made by first-winter individuals, and 20.7~ (195) were made by adults. Adult gulls directed a significantly greater proportion of attempts towards juvenile pelicans than did firstwinter gulls (72.8~ versus 63.0~, respectively; G=6.76, P<0.01). A comparison of expected attempt frequencies, based on the relative proportions of diving adult and juvenile pelicans, reveals that attempt frequencies of adult gulls deviate significantly from random (G=6.66, P<0.01), while first-winter gull attempts are not significantly different from random (G=0.03, P>0.5). It thus appears that adult gulls preferentially attack juvenile pelicans, and that first winter gulls show no preference. Actual success in kleptoparasitism was difficult to measure, because of the prey's small size and the rapid, inconspicuous swallowing movements of the gulls. In the 195 attempts made by adult gulls, only seven (3-6~) could be definitely scored as successful (five on juveniles, two on adults). Similarly, in 746 attempts by first-winter gulls, 13 (1.7~) were definitely successful (11 on juveniles, 2 on adults).
Carroll & Cramer: Age effects on kleptoparasitism However, our observations probably yield a subtantial underestimate of actual success, such that we do not feel confident in using these samples to compare the foraging success of adult versus first-winter gulls. In addition to attempts at a direct theft from pelicans, the gulls commonly plunged their heads into the water near a surfacing pelican, possibly preying upon disabled fish. We observed no attempts at kleptoparasitism among gulls, nor any dominance interactions that might have influenced the access of members of either age class to preferred food sources. Successful pelicans were vulnerable to kleptoparasitic attack for several seconds between surfacing and swallowing, during which they drained water from their pouches. Adult pelicans used 'short flight' evasion significantly more frequently than did juveniles (47% of 110 dives versus 27% of 218 dives, respectively; G = 8-63, P < 0-005). Adults and juveniles did not differ in their frequencies of 'turning in place' as an evasive behaviour (25% of 110 dives versus 21% of 218 dives, respectively; G=0"87, P > 0 ' I ) . Combining the two types of evasive actions yields a significantly greater frequency of occurrence in adult pelicans (G = 13.21, P<0.001).
DISCUSSION Our observations support the prediction that adult laughing gulls preferentially kleptoparasitize juvenile brown pelicans. This bias in victim choice probably results from differences in the efficiency with which food may be taken from juvenile versus adult pelicans. The availability of food to a kleptoparasite may be estimated from two general parameters: ({) victim reliability, defined here as the probability that a foraging pelican will capture prey and thus become a potential food source for gulls, and (2) victim exploitability, which we define as the probability that food may be stolen from a pelican that has caught fish. Age-related differences in either of these parameters may favour discrimination between victim age classes by kleptoparasites. Our data can be used to obtain general estimates of the reliability and exploitability of adult and juvenile pelicans. Because adult pelicans caught fish in about 9% more of their dives than did juveniles (Schnell et al. 1983), adults were the more reliable class. At the same time, juveniles attempted
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evasion in only 48% of their successful dives, while adults did so in 72% of their successful dives, so juveniles were probably more exploitable. In addition, the tendency of juvenile pelicans to use the seemingly less effective 'turning in place' evasion tactic rather than 'short flight' evasion probably increased their relative susceptibility to prey loss. 'Short flight' evasion, used more frequently by adults, has the advantage of taking a bird directly away from harassing gulls, allowing it to swallow while the gulls are behind it. This is important because pelicans may be especially vulnerable to food theft while making the head-tossing motion of swallowing, during which the bill is opened. While individuals that turned in place postponed swallowing until the bill was directed away from harassing gulls, the gulls were still close enough to make lunging attacks as the pelican tossed its head. Because adult pelicans are more reliable as potential victims and juvenile pelicans are probably more exploitable, either of two opposite predictions for victim choice by gulls could be made. In terms of simple percentages, the gulf between adult and juvenile exploitability is clearly much greater than that between adult and juvenile reliability, and thus is consistent with our observation that adult gulls bias their attacks toward juvenile pelicans. However, a more accurate comparison of the significance of age differences in these two parameters will require a quantified accounting of their effects on the efficiency of kleptoparasitism. At least three additional factors may influence victim choice. First, pelicans sometimes respond aggressively to kleptoparasitic gulls, and such aggression may be more commonly exhibited by adult pelicans (G. Schnell, personal communication). Second, the relative values of reliability and exploitability may vary over time or between sites and populations. For example, Orians (1969) found that compared to our findings, juvenile pelicans in Costa Rica were much less successful in prey capture than were adults. Third, if a gull is actively choosing targets for kleptoparasitism, the cost of passing over some pelicans and waiting for a potentially more profitable target will be influenced by the relative proportions of adult and juvenile pelicans in the population. Such a cost will become more significant as the relative availability of food from one victim class approaches that of the other. Because assessing the value of one victim class versus another and associating this with plumage patterns requires sensitivity to many variables, it is
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Animal Behaviour, 33, 1
not surprising that first-winter gulls showed no discrimination between pelican age classes. This pattern is consistent with findings for several bird species with protracted juvenile development. A prolonged period of foraging skill acquisition is especially common in species in which complex feeding techniques are employed and/or prey is relatively scarce (e.g. Tinbergen 1953; Orians 1969; Ainley & Schlatter 1972; Buckley & Buckley 1974). However, apparently greater foraging efficiency in adults may result, at least in part, from a lower survival rate of the less efficient of the juveniles (Orians 1969). In animals in which the foraging skills necessary for breeding are especially complex, individuals may maximize their lifetime reproductive success by delaying breeding until the necessary skills are attained (Lack 1954, 1966). Our data show that adult gulls concentrate their efforts at kleptoparasitism on the pelican age-class that is likely to be the more vulnerable, and they therefore probably have higher foraging efficiency than first-winter gulls. Adult gulls may even recognize individual pelicans as difficult or easy targets, as opposed to simply distinguishing between two victim classes. If individual juvenile pelicans are regarded as relatively easy victims more frequently than are individual adult pelicans, the predicted patterns of kleptoparasitism would resemble those predicted by the hypothesis that adult gulls discriminate victims by age-class alone. While we do not know at what age improvement in kleptoparasitism ability begins to plateau (if indeed it does), it may not be until the individual is several years old (cf. Searcy 1978). Because kleptoparasitism may provide a substantial portion of a gull's food, the development of highly refined kleptoparasitic skills may be an important prerequisite to successful reproduction. Their plumage ontogeny suggests that laughing gulls probably do not begin to breed until they are at least 3 years old (e.g. Dwight 1925). Correspondingly, juvenile pelicans may lose more food to laughing gulls than do adult pelicans. The mean number of gulls attacking juvenile gulls in 295 plunge-dives was 2.53, while in 177 adult dives, only 1.10 gulls were present per dive (G = 44-2, P < 0"001). Not only may this apparently higher rate of kleptoparasitism contribute to firstyear mortality, it may also hinder foraging efficiency sufficiently to force some additional postponement of the first breeding attempt, which
typically occurs at 3-4 years of age (Blus & Keahey 1978). While the development of facility in the complex plunge-dive hunting of the brown pelican may explain much of its deferred breeding, the acquisition of skills to evade laughing gull kleptoparasitism may be important in this population as well. Our findings show that kleptoparasitizing laughing gulls discriminate between food sources in a way which probably increases their foraging efficiency, and that this ability to choose more profitable sources probably develops with age. Because adult gulls appear to recognize two types of pelican victims, adult and juvenile, this may be an unusually simple natural association with which to test models of optimality in prey (victim) choice. Such studies will require data on the success of gull kleptoparasites, and on the effectiveness of pelican evasive tactics.
ACKNOWLEDGMENTS We thank T. Crowl, M. Gochfeld, J. Loye, D. Mock, J. Quinn, G. SchneI1, J. Thompson, B. Vestal and an anonymous reviewer for helpful discussion and comments on the manuscript. Financial support was provided by the following agencies of the University of Oklahoma: Department of Zoology, Office of Research Administration, and Associates Program.
REFERENCES Ainley, D. G. & Schlatter, R. P. 1972. Chick raising ability in Ad61iePenguins, Auk, 89, 559-566. Bent, A. C. t922. Life histories of North American petrels, pelicans and their allies. U.S. Nat. Mus. Bull., 121, 299-311. Blus, L. J. & Keahey, J. A. 1978. Variation in reproductivity with age in the brown pelican. Auk, 95, 128-134. Brockmann, H. J. & Barnard, C. J. 1979. Kleptoparasitism in birds. Anim. Behav., 27, 487~514. Buckley, F. G. & Buckley, P. A. 1974. Comparative feeding ecology of wintering adult and juvenile royal terns (Aves: Laridae, Sterninae). Ecology, 55, 1053-1063. Burger, J., Fitch, M., Schugart, G. & Werther, W. 1980. Piracy in Larus gulls at a dump in New Jersey. Proc. Colonial Waterbird Group, 3, 8%98. Burger, J, & Gochfeld, M. 1979. Age differences in ring-billed gull kleptoparasitisrn on starlings. Auk, 96, 806-808. Burger, J. & Gochfeld, M. 1981. Age-related differences
Carroll & Cramer: Age effects on kleptoparasitism in piracy behaviour of four species of gulls, Larus. Behaviour, 77, 242-267. Dunn, E. K. 1972. Effect of age on the fishing ability of sandwich terns (Sterna sandvieensis). Ibis, 114, 360-366. Dwight, J. 1925. The gulls (Laridae) of the world: their plumages, moults, variations, relationships, and distribution. Am. Mus. Nat. Hist. Bull., 52, 63-402. Fuchs, E. 1977. Kleptoparasitism of sandwich terns Sterna sandvieensis by black-headed gulls Larus ridibundus. Ibis, 119, 183-190. Gochfeld, M. & Burger, J. 1981. Age-related differences in piracy of frigatebirds from laughing gulls. Condor, 83, 79-82. Hatch, J, J. 1970. Predation and piracy by gulls at a ternery in Maine. Auk, 87, 244-254. Ingolfsson, A. 1969. Behavior of gulls robbing eiders. Bird Study, 16, 45-52. Ingolfsson, A. & Estrella, J. T. 1978. The development of shell-cracking behavior in herring gulls. Auk, 95, 577-579. K/illander, H. 1977. Piracy by black-headed gulls on lapwings. Bird Study, 24, 186-194. Lack, D. 1954. The Natural Regulation of Animal Numbers. New York: Oxford University Press.
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Lack, D. 1966. Population Studies of Birds. New York: Oxford University Press. Orians, G. 1969. Age and hunting success in the brown pelican (Peleeanus occidentalis). Anim. Behav., 17, 316-319. Quinney, T. E. & Smith, P, C. 1980. Comparative foraging behavior and efficiency of adult and juvenile great blue herons. Can. J. Zool., 58, 1168-1173. Schnell, G. D., Woods, B. L. & Ploger, B. J. 1983. Brown pelican foraging success and kleptoparasitism by laughing gulls. Auk, 100, 636-644. Searcy, W. A. 1978. Foraging success in three age classes of glaucous-winged gulls. Auk, 95~ 586-588. Tinbergen, N. 1953. The Herring Gull's World. Garden City, N.Y.: Doubleday. Verbeek, N. A. M. 1977a. Age differences in the digging frequency of herring gulls on a dump. Condor, 79, 123-125. Verbeek, N. A. M. 1977b. Comparative feeding behavior of immature and adult herring gulls. Wilson Bull., 89, 415-421.
(Received 5 October 1983; revised 19 March 1984; MS. number: A4052)
Age differences in kleptoparasitism by laughing gulls (Larus atricilla) on adult and juvenile brown pelicans (Pelecanus occidentalis) S C O T T P. C A R R O L L * & K E N N E T H L. C R A M E R
Department of Zoology, University of Oklahoma, Norman, OK 73019, U.S.A. Abstract. We recorded the choice of victims by a population of adult and first-winter laughing gulls (Larus
atrieilla) making attempts to steal food from adult and juvenile brown pelicans (Pelecanus oeeidentalis). Adult gulls made food theft attempts on juvenile pelicans with a disproportionately great frequency; first-winter gulls appeared to select pelican victims at random. Adult pelicans were more frequently successful in their foraging attempts than juvenile pelicans, suggesting that adults may be more reliable as potential food sources for gulls making theft attempts. However, juvenile pelicans attempted to evade kleptoparasitizing gulls less frequently than did adult pelicans, suggesting that the fish prey of juveniles may be more easily stolen. These patterns are discussed in relation to optimal victim choice by gulls, and to deferred maturity in both species.
Kleptoparasitism is the theft of food or other items. It has been described in many avian families, but appears to be particularly common among gulls (Brockmann & Barnard 1979). Gulls of several species may rely on kleptoparasitism for a significant proportion of their food intake (Ingolfsson 1969; Hatch 1970; Fuchs 1977; K/illander 1977). Age has been shown to correlate positively with foraging success in a variety of avian species (e.g. Tinbergen 1953; Orians 1969; Dunn 1972; Verbeek 1977a,b; Ingolfsson & Estrella 1978; Searcy 1978; Burger et al. 1980; Quinney & Smith 1,980). In general, adults exhibit higher attempt and capture rates than immatures. Orians (1969) observed that adult brown pelicans (Pelecanus oceidentalis) caught prey on a significantly greater percentage of dives than did juveniles, and Burger et al. (1980) described similar findings in age classes of laughing gulls, Larus atricilla. Foraging success via kleptoparasitism may improve with age as well. Burger & Gochfeld (1979) found that adult ring-billed gulls (Larus delawarensis) were more successful than juveniles in taking food from starlings (Sturnus vulgaris). Under conditions of artificial provisioning, Burger & Gochreid (1981) found that adult laughing gulls were more successful than young at intraspecific kleptoparasitism. However, Verbeek (1977a,b) found no positive association between age and kleptoparasitism success in herring gulls, Larus argentatus. In addition, while Burger et al. (1980) report significant age differences in frequencies of attempted * Present address: Department of Biology, University of Utah, Salt Lake City, Utah 84112, U.S.A.
kleptoparasitism for laughing, herring and ringbilled gulls at garbage dumps, they found no such differences in success rates. Gochfeld & Burger (1981) observed the same patterns in adult and juvenile kleptoparasitic frigatebirds, Fregata mag-
n~een~. In this study we investigate the relationship between the age of laughing gulls and their frequencies of kleptoparasitic attempts on brown pelicans of two age classes. We hypothesize that differences between adult and juvenile pelicans in their foraging success and evasive ability may make these two age classes resources of different availability for gulls. Specifically, if adult pelicans capture fish on a greater proportion of dives than juvenile pelicans, gulls may preferentially kleptoparasitize adult pelicans as a more reliable resource. If adult pelicans are more able to avoid kleptoparasitism than juveniles, gulls may preferentially kleptoparasitize juvenile pelicans as a more exploitable resource. If these two potential factors operate together, or neither is important, gulls may show no preference. In addition, we predict that adult gulls are more sensitive than first-winter gulls to any differences in resource availability that might exist between pelican age classes, and exploit them accordingly.
201
METHODS
We conducted our study on 9, 10 and 11 January 1982 along a sandy 3-km section of Miramar Beach (Playa Miramar) on Santiago Bay (Bahia Santiago), approximately 10 km northwest of Man-
Animal Behaviour, 33, 1
202
zanillo, Colima, Mexico. We classified the brown pelicans into two age groups, adult and juvenile, on the basis of easily distinguishable head coloration patterns (Bent 1922). Subadult birds were rarely observed and were grouped with adults. Laughing gulls were also grouped into two age classes: first-winter birds, with a dark head and wings and a dark terminal tail band; and adults in winter plumage, with light head and wings and no tail band. This 'adult' population included a small proportion of second-winter individuals. We observed gull-pelican interactions with 10 x 50 binoculars from positions 10-20 m above the water line. Each time we saw a brown pelican plunge-dive, we recorded the following data: (1) age-class of pelican; (2) success or failure in fish capture, as indicated by the presence of absence of a swallowing motion (Orians 1969); (3) attempts at kleptoparasitism, which we defined as any laughing gull within 1 m of the pelican between the time that the pelican rose to the water surface after diving and the time of swallowing (or departure of the gulls if the dive was unsuccessful); (4) success or failure of kleptoparasitism for gulls of each age class; (5) evasive behaviour of the pelicans. The two evasive behaviours observed were: 'turning in place', in which a recently surfaced pelican rotated from side to side away from gulls, and 'short flight', in which a pelican flew 15-30 m away from the site of resurfacing, swallowing en route. In addition, the proportions of adult and juvenile pelicans and gulls in the local population were assayed from resting groups of each species.
RESULTS Each day about 150 brown pelicans hunted in the surf within 50 m of shore. They were most active from dawn (0730 hours) to 1000 hours, and also hunted in groups between about 1200 and 1400 hours and just before dusk (1630 to 1730 hours). During these periods, several groups of hunting pelicans were present among the breakers, usually moving upwind and diving along the way, then circling back and covering the same area again. Hunting groups were always accompanied by laughing gulls, which flew among the pelicans and rapidly approached diving individuals, Pelicans were accompanied by gulls on 87-2~ of all dives (N = 472), with a mean of 2-0 gulls present per dive. The gulls attempted to take fish protruding from
the pelicans' bills or from the surface of the water near the pelicans. This was done by hovering near a pelican's head, alighting on its head or back, or alighting on the water next to the pelican. When not hunting, the pelicans floated in several groups about 50--75 m offshore. At such times, the gulls rested on the water near them and were generally inactive until the pelicans resumed hunting, at which time the gulls resumed kleptoparasitic behaviour. There were approximately 250 laughing gulls in the study area. In six groups of resting brown pelicans, 55 adults (40. IX) and 82 juveniles (59.9~) were present. In three groups of resting and one group of active laughing gulls, 11 adults (16"7~o) and 55 first-year birds (83.3~) were present. Of 472 pelican dives observed, 295 (62.5~) were made by juveniles, and 177 (37.5~) were made by adults. In the 443 dives for which success or failure was recorded, 227 (81.9~) were successful for juveniles, and 145 (87.3~) were successful for adults (G = 2.31, P > 0.1). These data are a subsample of those collected in concurrent observations by Schnell et al. (1983), which showed adults to be significantly more successful (G = 28.74, P < 0-001, N = 2449). The common prey were schooling fish less than 10 cm long that inhabited the surf in water 1-2 m deep. Of 941 kleptoparasitism attempts observed, 79.3~ (746) were made by first-winter individuals, and 20.7~ (195) were made by adults. Adult gulls directed a significantly greater proportion of attempts towards juvenile pelicans than did firstwinter gulls (72.8~ versus 63.0~, respectively; G=6.76, P<0.01). A comparison of expected attempt frequencies, based on the relative proportions of diving adult and juvenile pelicans, reveals that attempt frequencies of adult gulls deviate significantly from random (G=6.66, P<0.01), while first-winter gull attempts are not significantly different from random (G=0.03, P>0.5). It thus appears that adult gulls preferentially attack juvenile pelicans, and that first winter gulls show no preference. Actual success in kleptoparasitism was difficult to measure, because of the prey's small size and the rapid, inconspicuous swallowing movements of the gulls. In the 195 attempts made by adult gulls, only seven (3-6~) could be definitely scored as successful (five on juveniles, two on adults). Similarly, in 746 attempts by first-winter gulls, 13 (1.7~) were definitely successful (11 on juveniles, 2 on adults).
Carroll & Cramer: Age effects on kleptoparasitism However, our observations probably yield a subtantial underestimate of actual success, such that we do not feel confident in using these samples to compare the foraging success of adult versus first-winter gulls. In addition to attempts at a direct theft from pelicans, the gulls commonly plunged their heads into the water near a surfacing pelican, possibly preying upon disabled fish. We observed no attempts at kleptoparasitism among gulls, nor any dominance interactions that might have influenced the access of members of either age class to preferred food sources. Successful pelicans were vulnerable to kleptoparasitic attack for several seconds between surfacing and swallowing, during which they drained water from their pouches. Adult pelicans used 'short flight' evasion significantly more frequently than did juveniles (47% of 110 dives versus 27% of 218 dives, respectively; G = 8-63, P < 0-005). Adults and juveniles did not differ in their frequencies of 'turning in place' as an evasive behaviour (25% of 110 dives versus 21% of 218 dives, respectively; G=0"87, P > 0 ' I ) . Combining the two types of evasive actions yields a significantly greater frequency of occurrence in adult pelicans (G = 13.21, P<0.001).
DISCUSSION Our observations support the prediction that adult laughing gulls preferentially kleptoparasitize juvenile brown pelicans. This bias in victim choice probably results from differences in the efficiency with which food may be taken from juvenile versus adult pelicans. The availability of food to a kleptoparasite may be estimated from two general parameters: ({) victim reliability, defined here as the probability that a foraging pelican will capture prey and thus become a potential food source for gulls, and (2) victim exploitability, which we define as the probability that food may be stolen from a pelican that has caught fish. Age-related differences in either of these parameters may favour discrimination between victim age classes by kleptoparasites. Our data can be used to obtain general estimates of the reliability and exploitability of adult and juvenile pelicans. Because adult pelicans caught fish in about 9% more of their dives than did juveniles (Schnell et al. 1983), adults were the more reliable class. At the same time, juveniles attempted
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evasion in only 48% of their successful dives, while adults did so in 72% of their successful dives, so juveniles were probably more exploitable. In addition, the tendency of juvenile pelicans to use the seemingly less effective 'turning in place' evasion tactic rather than 'short flight' evasion probably increased their relative susceptibility to prey loss. 'Short flight' evasion, used more frequently by adults, has the advantage of taking a bird directly away from harassing gulls, allowing it to swallow while the gulls are behind it. This is important because pelicans may be especially vulnerable to food theft while making the head-tossing motion of swallowing, during which the bill is opened. While individuals that turned in place postponed swallowing until the bill was directed away from harassing gulls, the gulls were still close enough to make lunging attacks as the pelican tossed its head. Because adult pelicans are more reliable as potential victims and juvenile pelicans are probably more exploitable, either of two opposite predictions for victim choice by gulls could be made. In terms of simple percentages, the gulf between adult and juvenile exploitability is clearly much greater than that between adult and juvenile reliability, and thus is consistent with our observation that adult gulls bias their attacks toward juvenile pelicans. However, a more accurate comparison of the significance of age differences in these two parameters will require a quantified accounting of their effects on the efficiency of kleptoparasitism. At least three additional factors may influence victim choice. First, pelicans sometimes respond aggressively to kleptoparasitic gulls, and such aggression may be more commonly exhibited by adult pelicans (G. Schnell, personal communication). Second, the relative values of reliability and exploitability may vary over time or between sites and populations. For example, Orians (1969) found that compared to our findings, juvenile pelicans in Costa Rica were much less successful in prey capture than were adults. Third, if a gull is actively choosing targets for kleptoparasitism, the cost of passing over some pelicans and waiting for a potentially more profitable target will be influenced by the relative proportions of adult and juvenile pelicans in the population. Such a cost will become more significant as the relative availability of food from one victim class approaches that of the other. Because assessing the value of one victim class versus another and associating this with plumage patterns requires sensitivity to many variables, it is
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not surprising that first-winter gulls showed no discrimination between pelican age classes. This pattern is consistent with findings for several bird species with protracted juvenile development. A prolonged period of foraging skill acquisition is especially common in species in which complex feeding techniques are employed and/or prey is relatively scarce (e.g. Tinbergen 1953; Orians 1969; Ainley & Schlatter 1972; Buckley & Buckley 1974). However, apparently greater foraging efficiency in adults may result, at least in part, from a lower survival rate of the less efficient of the juveniles (Orians 1969). In animals in which the foraging skills necessary for breeding are especially complex, individuals may maximize their lifetime reproductive success by delaying breeding until the necessary skills are attained (Lack 1954, 1966). Our data show that adult gulls concentrate their efforts at kleptoparasitism on the pelican age-class that is likely to be the more vulnerable, and they therefore probably have higher foraging efficiency than first-winter gulls. Adult gulls may even recognize individual pelicans as difficult or easy targets, as opposed to simply distinguishing between two victim classes. If individual juvenile pelicans are regarded as relatively easy victims more frequently than are individual adult pelicans, the predicted patterns of kleptoparasitism would resemble those predicted by the hypothesis that adult gulls discriminate victims by age-class alone. While we do not know at what age improvement in kleptoparasitism ability begins to plateau (if indeed it does), it may not be until the individual is several years old (cf. Searcy 1978). Because kleptoparasitism may provide a substantial portion of a gull's food, the development of highly refined kleptoparasitic skills may be an important prerequisite to successful reproduction. Their plumage ontogeny suggests that laughing gulls probably do not begin to breed until they are at least 3 years old (e.g. Dwight 1925). Correspondingly, juvenile pelicans may lose more food to laughing gulls than do adult pelicans. The mean number of gulls attacking juvenile gulls in 295 plunge-dives was 2.53, while in 177 adult dives, only 1.10 gulls were present per dive (G = 44-2, P < 0"001). Not only may this apparently higher rate of kleptoparasitism contribute to firstyear mortality, it may also hinder foraging efficiency sufficiently to force some additional postponement of the first breeding attempt, which
typically occurs at 3-4 years of age (Blus & Keahey 1978). While the development of facility in the complex plunge-dive hunting of the brown pelican may explain much of its deferred breeding, the acquisition of skills to evade laughing gull kleptoparasitism may be important in this population as well. Our findings show that kleptoparasitizing laughing gulls discriminate between food sources in a way which probably increases their foraging efficiency, and that this ability to choose more profitable sources probably develops with age. Because adult gulls appear to recognize two types of pelican victims, adult and juvenile, this may be an unusually simple natural association with which to test models of optimality in prey (victim) choice. Such studies will require data on the success of gull kleptoparasites, and on the effectiveness of pelican evasive tactics.
ACKNOWLEDGMENTS We thank T. Crowl, M. Gochfeld, J. Loye, D. Mock, J. Quinn, G. SchneI1, J. Thompson, B. Vestal and an anonymous reviewer for helpful discussion and comments on the manuscript. Financial support was provided by the following agencies of the University of Oklahoma: Department of Zoology, Office of Research Administration, and Associates Program.
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(Received 5 October 1983; revised 19 March 1984; MS. number: A4052)