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.
Such data will provide a better understanding of age-related differences as
well as the ontogeny of kleptoparasitism. Moreover, future studies of frigatebird
behavior that are based on populations of marked individuals and
compare populations in different geographic regions, will lend greatest to
our understanding of if and how frigatebirds learn to forage via piracy.
Acknowledgments
We would like to thank Dr. Matthew P. Rowe for the use of his spotting scope,
for early edits to this manuscript, and for instilling in us a curiosity and passion for
understanding bird behavior and ecology. This research was conducted as a class
project in Dr. Rowe’s Animal Behavior class at Appalachian State University in
Boone, NC. We also thank two anonymous reviewers for their helpful comments to
improve the manuscript.
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