2008 SOUTHEASTERN NATURALIST 7(1):19–26 Age-related Differences in Kleptoparasitic Behavior of Magnificent Frigatebirds Lesley P. Bulluck1,2,* and Jason F. Bulluck1,3 Abstract - Kleptoparasitism, the stealing of food from individuals of either the same or a different species, is a common behavior among seabirds. Little is known about the age-related differences in kleptoparasitism behaviors, which may elucidate how this behavior emerged and is maintained in populations. We observed the kleptoparasitic behavior of Fregata magnificens (Magnificent Frigatebirds) on the Dry Tortugas, a group of islands west of Key West, FL. For each kleptoparasitic event, we recorded whether an adult or a sub-adult frigatebird made the attack; whether the potential host was approached while it was in the air, in the water, or on the ground; the duration of the chase; and whether an individual or group of hosts was approached. Adult females most often approached potential hosts in the air (92% of recorded encounters), while sub-adults approached more potential hosts on the ground (61% of recorded encounters). Water approaches were rarely performed by sub-adults and never by adults. Adult females tended to spend signifi- cantly more time on each chase than did sub-adults, and adult females sought out individual hosts (69% of recorded encounters), while sub-adults seemed to prefer groups of hosts (78% of recorded encounters). These age-related differences in feeding behaviors may represent a period of learning in young birds that will make them more effective kleptoparasites as adults. In general, these age-related differences in behavior may lead to a better understanding of the pressures that have led to the development and maintenance of kleptoparasitic feeding strategies in frigatebirds. Introduction Kleptoparasitism, also called piracy, is a foraging strategy practiced when individuals of one species steal food already procured by individuals of the same or another species (Brockmann and Barnard 1979). This behavior is known to occur in a variety of taxa from mammals (Bergan 1990; Carbone et al. 1997, 2005) to fish (Nillson and Bronmark 1999) to invertebrates (Henaut 2000, Whitehouse 1997), but it is widespread and most studied in birds (Brockmann and Barnard 1979, Shealer et al. 2005). Birds in the orders Falconiformes and Charadriiformes, specifically Stercorariidae (skuas) and Laridae (gulls), in addition to birds in the genus Fregata (frigatebirds), are the most well-known avian kleptoparasites (Brockmann and Barnard 1979). Some behavioral and environmental conditions suggested to favor the emergence and maintenance of this feeding strategy are: (1) a variety of 1Biology Department, Appalachian State University, Boone, NC 28608. 2Current address - Department of Forestry, Wildlife and Fisheries, University of Tennessee, Knoxville, TN 37996. 3Current address - Division of Natural Heritage, Department of Conservation and Recreation, Commonwealth of Virginia, Richmond, VA. *Corresponding author - lbulluck@utk.edu. 20 Southeastern Naturalist Vol.7, No. 1 available hosts (e.g., mixed-species feeding fl ocks), (2) a high concentration of hosts, (3) hosts that exhibit predictable feeding behavior (i.e., returning periodically to the nest with food), and (4) opportunistic feeding tendencies with the ability to be acrobatic and agile pursuers of hosts (Brockmann and Barnard 1979). Based on these criteria, it is not surprising that seabirds breeding in mixed species colonies commonly exhibit this behavior. Interestingly, kleptoparasitism has been suggested to be a density-dependent behavior, such that the success of an individual depends on the number and success of other parasites in the population. Kleptoparasitic individuals can also employ non-parasitic strategies, thereby creating a mixed evolutionary state. As a result, an equilibrium ratio of two comparable strategies may be seen either in an individual or in the population as a whole (Brockmann and Barnard 1979). Fregata magnificens Mathews (Magnificent Frigatebird) is an example of an avian kleptoparasite that uses more than one foraging strategy. Whether these alternative strategies occur at the individual or population level is not known because of the lack of studies using individually marked birds. In addition to piracy, Magnificent Frigatebirds also prey on seabird eggs and nestlings, young turtles, and fish and squid from the surface of the water; they also consume offal from fishing vessels (Calixto-Abarran and Osorno 2000, Diamond and Schreiber 2002). The fact that non-parasitic feeding behaviors dominate is often a surprise to those who have observed frigatebirds at breeding colonies, because colony-based piracy is a conspicuous behavior. However, the frequency or success of these acts may be low for frigatebirds, which would explain why kleptoparasitism serves merely to supplement the diet rather than to exclusively sustain the birds (Cummins 1995, Nelson 1975, Osorno et al. 1992). Despite the fact that piracy is not the dominant feeding strategy of the Magnificent Frigatebird, the development and maintenance of this behavior in this and other species is fascinating both ecologically and evolutionarily. By discerning how kleptoparasitic behavior varies among individuals within a population, we can better understand how this behavior is maintained. Age-related differences in feeding behaviors have been studied in several frigatebird species with contradictory results regarding whether or not success rates differ significantly. Gibbs and Gibbs (1987), Gochfeld and Burger (1981), and Osorno et al. (1992) found no difference between adult and juvenile success rates for Magnificent Frigatebirds. On the other hand, Gilardi (1994) found that the success of kleptoparasitic events increased with age for F. minor Gmelin (Great Frigatebirds); likewise, Hesp and Barnard (1989) found that adult Larus ridibundus Linnaeus (Black-headed Gulls) were twice as successful as immature birds. This may support the idea that complex and potentially expensive feeding behaviors such as kleptoparasitism may mandate a period of both experiential and social learning by young individuals. Gilardi (1994) found that group chase events (when more than one bird approached a host) were more often employed by sub-adult 2008 L.P. Bulluck and J.F. Bulluck 21 Great Frigatebirds and were more successful than solitary chase events, which were more commonly employed by adults. Such group chases may be compensating for the juvenile’s supposed ineptitude. Aside from success rates, little research has assessed age-related differences in host approach strategies with regard to kleptoparasitic behavior in frigatebirds. No studies have documented whether a certain age class of frigatebirds more frequently approach their hosts on land, water, or in the air, or whether solitary versus aggregated hosts are preferred by certain age classes. We might suspect that the foraging behaviors we see today are the result of selection pressures on foraging strategies that have led to overall greater success rates. In addition, these foraging behaviors are likely infl uenced by learning in individuals. For example, we might expect immature birds to expend more energy and time than experienced adults per unit of food sought. Our objective for this observational study is to document whether age-related differences in kleptoparasitism strategies exist for a population of Magnificent Frigatebird on the Dry Tortugas, FL. Specifically, we assess potential differences related to host location, host aggregation, and chase duration employed by adults and sub-adults. We expect that adults will chase solitary hosts in the air and for longer periods of time compared with sub-adults. We base these expectations on the presumption that these activities require more skill and adults should have more experience and skill with acts of piracy. Study Area and Methods Magnificent Frigatebirds were observed in the Dry Tortugas, FL (24°38'N, 82°55'12"W), for two hours per day between the days of March 15 to 18, 2000. All observation periods took place in the afternoon and evening (1500–1900) when activity of the hosts and Magnificent Frigatebirds tends to be greatest (Osorno et al. 1992; L.P. Bulluck and J.F. Bulluck, pers. observ.). We observed frigatebirds from atop the southeast corner of Fort Jefferson, which comprises the majority of the land area of Garden Key. This elevated position provided an excellent view of Bush and Long Keys where many potential hosts and frigatebirds nested, respectively. We observed frigatebirds pursuing the following host species: Sterna maximus Boddaert (Royal Terns), S. sandvicensis Latham (Sandwich Terns), S. fuscata Linnaeus (Sooty Terns), Anous stolidus Linnaeus (Brown Noddies), Larus argentatus Pontoppidan (Herring Gulls), L. atricilla Linnaeus (Laughing Gulls), L. delawarensis Ord (Ring-billed Gulls), and Pelecanus occidentalis Linnaeus (Brown Pelicans). We recorded all kleptoparasitic attempts initiated by Magnificent Frigatebirds that could be discerned with 10 x 45 binoculars or a spotting scope. For each observed event, we recorded: (1) whether a solitary host or a group of hosts was approached; (2) if the host was approached while on land, on water, or in the air; and (3) if the frigatebird pursuit was made by an adult, sub-adult, or a group. We differentiated adults from sub-adults 22 Southeastern Naturalist Vol.7, No. 1 using differences in plumage (Diamond and Schreiber 2002). Chase durations were also recorded using a stopwatch to the nearest second, and we compared the frequency of chases lasting greater than 10 sec, less than or equal to 10 sec, and those kleptoparasitic events that resulted in no chase at all (i.e., the frigatebird approached the host aggressively, but the interaction did not result in a chase). We did not specifically record the success of each attempt. We used chi-squared goodness of fit and contingency analyses (Cox 1996) to determine whether there were significant differences in the frequency of adult and sub-adult (1) piracy of hosts located on the ground, water, or in the air; (2) piracy of solitary hosts or hosts in groups; and (3) use of the three chase durations. Frigatebirds were not individually marked, so it is possible that we inadvertently resampled individuals. We estimated the colony to be approximately 100–150 Magnificent Frigatebirds. Results In total, we recorded 36 kleptoparasitic attempts over the four-day period. Thirteen piracy events were recorded for adult females (36%), and twenty-three events for sub-adults (64%); sexes were not distinguishable in sub-adults. Adult males were effectively absent from the population because they typically leave the colony after the young are 3–4 months old (Diamond 1973, Diamond and Schreiber 2002). The frequencies of adult female approaches made in the air, over the ground, and over the water were 12 (92%), 1 (8%), and 0 (0%), respectively (Fig. 1). The frequencies of approaches made by sub-adults toward hosts in the air, on the ground, and on the water were 7 (30%), 14 (61%), and 2 (9%), respectively (Fig. 1). Figure 1. Proportion of observed adult female (n = 13) and sub-adult (n = 23) kleptoparasitic attempts occurring in the air, over the ground, and over water for Magnificent Frigatebirds (Fregata magnificens) in the Dry Tortugas, FL. 2008 L.P. Bulluck and J.F. Bulluck 23 There was a significant difference in the frequencies at which adult females and sub-adults approached hosts located in the air, on the ground, or on the water (χ2 = 12.8, df = 2, P < 0.005). In 4 of the 13 adult female attempts (31%), the individual approached a group of hosts, and in 18 of the 23 subadult encounters (78%), the sub-adult approached a group of hosts (Fig. 2). Sub-adults preferred approaching groups of hosts while adult females more often pursued solitary hosts (χ2 = 7.88, df = 1, P < 0.01). The majority of kleptoparasitic attempts made by adult females (8 of 13 or 61.5%) lasted longer than 10 seconds, while only one of the sub-adult attempts (4.3%) lasted longer than 10 seconds (Fig. 3). Adult females chased hosts for significantly longer durations than did sub-adults (χ2 = 14.87, df = 2, P < 0.001). Discussion Despite the small sample size of observations, we documented significant age-related differences in kleptoparasitic behaviors in this colony of Magnificent Frigatebirds on the Dry Tortugas. Adult females more often chased solitary hosts in the air compared to sub-adults, which seemed to prefer aggregated hosts on the ground. Adult females also chased each host for significantly longer durations than was observed for sub-adults. That adult females exhibited more approaches in the air than did sub-adults correlates with their apparent preference for solitary hosts, because most hosts in fl ight were solitary. Likewise the sub-adults’ proclivity for approaches over ground correlates with their preference for aggregated hosts because mixed-species fl ocks on the peninsula of Bush Key were the most common terrestrial targets. We propose that the sub-adults’ preference for aggregated hosts could Figure 2. Proportion of observed adult female (n = 13) and sub-adult (n = 23) kleptoparasitic attempts against group and solitary hosts for Magnificent Frigatebirds (Fregata magnificens) in the Dry Tortugas, FL. 24 Southeastern Naturalist Vol.7, No. 1 be a strategy to compensate for their lack of fine-tuned aerial skill, similar to the finding that immature Great Frigatebirds more often pursue their hosts as a group (i.e., group chases; Gilardi 1994). In either case, the young bird may be more likely to obtain a food item. For example, when a frigatebird chases a group of hosts, the chances of encountering a host bearing food may be greater than when chasing an individual, especially before the young bird has learned the important cues given by individuals not bearing food (Cummins 1995). On the other hand, when a young frigatebird joins a group to pursue a host, there may be a greater chance the host will give up its food item (Gilardi 1994, Osorno et al. 1992); however, the chance that each pursuer will obtain any food decreases as the group size increases. Cummins (1995) found that adult Great Frigatebirds frequently terminate chases after the host gives a call that sounds as if it has an empty crop. This implies that adults spend less time in any particular chase if they are attuned to subtle cues given by the host that indicate a futile chase. Our results seem to contradict this idea and show a significant tendency by the adult females for longer overall chase times. However, our results could mean that adult females are more experienced with assessing the hosts’ food-bearing status and were thus observed in longer chases after food-bearing hosts. Adult females may have only chased hosts actually bearing food, while juveniles chased often and futilely. Gochfeld and Burger (1981) identified a similar account of attentiveness displayed by adult Magnificent Frigatebirds relative to sub-adults in an experiment where they threw both large and small chunks of food out to a feeding fl ock of birds. The adults showed a preference to pursue hosts with larger pieces, while sub-adults showed no preference for hosts with large or small food items. Figure 3. Proportion of observed adult female (n = 13) and sub-adult (n = 23) kleptoparasitic attempts that resulted in chases of >10 seconds, ≤10 seconds, or no chase at all for Magnificent Frigatebirds (Fregata magnificens) in the Dry Tortugas, FL. 2008 L.P. Bulluck and J.F. Bulluck 25 The paucity of data regarding age-related kleptoparasitism success rates and the differences in feeding strategies exhibited by adult and subadult frigatebirds leave many questions unanswered. To what degree are social and experiential learning occurring in the kleptoparasitic behavior of frigatebirds? Our results suggest that immature Magnificent Frigatebirds are using different foraging strategies than adults, and these behaviors may be allowing them to obtain the necessary cues to make them effective adult kleptoparasites. In other words, the different foraging strategies displayed by young and adult birds likely represent a period of learning for the younger individuals. Magnificent Frigatebirds on the Dry Tortugas are worthy of further study. At the very least, we suggest repetition of this study at this site and at other sites with more field data including success rates of piracy attempts by age. 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