Behavioral Ecology Vol. 11 No. 5: 572-573
© 2000 International Society for Behavioral Ecology
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Colonies as byproducts of commodity selection
a Konrad Lorenz Institute for Comparative Behavioral Research, Austrian Academy of Sciences, Savoyenstrasse 1a, A-1160 Vienna, Austria b Université Pierre et Marie Curie, Institut d'Ecologie, CNRS-URA 258, Bat. A, 7ème Etage, Case 237, 75252, Paris Cedex 05, France
Received 18 May 1999; revised 10 December 1999; accepted 3 January 2000.
When ecologists examine a colony, they tend to ask, what are the benefits
of breeding in aggregations? In contrast, when students of leks examine an
arena of displaying males, they usually ask, what are the mechanisms that
produce aggregations? Here we discuss the differences in these two approaches.
The value of this distinction stems from the frustrating inability of decades
of research to provide a general explanation of the widespread occurrence of
colonial breeding. The traditional approach to studying coloniality is the
measurement of costs and benefits of breeding in high density
(Barclay, 1988
;
Brown and Brown, 1996;
Emlen and Wrege, 1986;
Hoogland and Sherman, 1976;
Møller, 1987;
Wittenberger and Hunt, 1985).
Our aim is to illustrate how individuals can pursue adaptive strategies that
result in their joining breeding aggregations without necessarily obtaining
net benefits from the aggregation.
In a recent review (Danchin and Wagner,
1997), we identified a mechanistic approach to studying
coloniality which synthesizes two new hypotheses. The "habitat
selection" hypothesis proposes that animals imitate the breeding habitat
choices of successful conspecifics to benefit from the same favorable
environmental conditions as successful breeders
(Boulinier and Danchin, 1997;
Danchin et al., 1998). The
sexual selection, or "hidden lek," hypothesis proposes that males
of monogamous, colonial species aggregate their nesting territories by the
same mechanisms that cause males of lekking species to aggregate their display
territories (Wagner, 1993),
1997). These two hypotheses
share a single common assumption that is simple but heterodox to the study of
coloniality; namely, that nesting aggregation may be merely a byproduct of
many individuals selecting commodities such as habitat and mates, and not
necessarily a benefit to the individuals that aggregate. The fact that the
aggregation need not produce benefits does not argue, however, against using
cost-benefit analyses, but rather argues for measuring the costs and benefits
of specific decisions made by individuals that lead them to produce a pattern
of aggregated breeding.
The issue of breeding aggregations fits into the more general problem of
animal group sizes, which was solved by Pulliam and Caraco
(1984) by applying the logic
of the ideal free distribution. The main point of those authors is that group
sizes may be byproducts of other factors, making it futile to search for
optimal group sizes. Despite the success of that approach in other types of
animal aggregations, the question of coloniality continues to be dominated by
the search for optimal group size (e.g.,
Brown and Brown, 1996).
Here we illustrate how the processes of mate selection and breeding habitat
selection can produce aggregation as a byproduct, without individuals
necessarily benefiting from breeding in dense aggregations. First, let us
consider the approach taken by some lek modelers to explain aggregations of
males via processes of sexual selection. Leks are aggregations of males that
females visit for copulation (Bradbury,
1981). One of the three principal models of lek evolution is the
hotshot model, which proposes that less attractive males aggregate around the
top male, or "hotshot," to gain access to females that are
attracted to him (Beehler and Foster,
1988). The hotshot model assumes that the aggregation of males is
a byproduct of female and male behavior; none of the individuals in the lek
benefits from aggregation, yet aggregation occurs. The model assumes three
kinds of players: secondary males, the hotshot male, and females. The reason
secondary males aggregate around the hotshot is to intercept females before
they can obtain a copulation from the hotshot, and, in fact, courtship
disruptions are sometimes the strongest correlate of copulation success
(Pruett-Jones and Pruett-Jones,
1994; Trail and Koutnik,
1986; Wagner,
1992). Thus, hotshots who are capable of attracting females in the
absence of other males will often lose mating opportunities to males that are
aggregated around them. Females also suffer from the aggregation of less
attractive males because they are disrupted from copulating with the top male.
Thus, male aggregation is a byproduct of female behavior and may be costly to
females. In this model, females do not search for leks, but rather for
hotshots and, as a result, incidentally produce leks.
The question remains whether secondary males benefit from aggregation. Clearly, a secondary male can benefit by displaying near a hotshot. However, each individual male may suffer costs from the presence of other secondary males, who are all competing to intercept the same females. Secondary males, therefore, may not benefit from the presence of other secondary males. Thus, individuals of all three types may suffer net costs from the aggregating of others, yet they produce aggregation.
The above example does not contradict the use of a cost-benefit analysis but suggests the appropriate level at which to perform the analysis. For example, the benefit to females of searching for a mate in a lek outweighs the cost of aggression or disruption from secondary males. For secondary males, the benefit of some mating success obtained by displaying near a hotshot outweighs the cost of receiving aggression from other males. For the hotshot, the cost of losing some matings to secondary males might be outweighed by the cost of establishing a new display territory.
The example of the hotshot model is linked to the study of coloniality by
the hidden lek hypothesis, which employs the mechanisms of lek models to
explain colony formation and breeding aggregations in general. The hypothesis
predicts that the lek mechanisms also operate in monogamous species that
pursue extrapair copulations. Just as less attractive males in promiscuous
species aggregate around a hotshot, monogamous males may aggregate around more
attractive males to obtain mates, and females may prefer males that defend
nesting sites near more attractive males to obtain extrapair copulations from
them. If lek mechanisms contribute to colony formation, as suggested by two
field studies (Hoi and Hoi-Leitner,
1997; Wagner et al.,
1996), then nesting aggregation may be a byproduct of mate
choice.
We now illustrate how the processes of breeding habitat selection can also produce aggregations as a byproduct of numerous individuals acting to maximize their fitness. Let's first consider a human example. In the United States and other countries, various regions are periodically discovered to have exceptionally high qualities of life, being free from crime, pollution, and traffic. Such locations are proclaimed by the media to be among the "10 best places to live." As knowledge spreads, individuals imitate the habitat selection choices of their predecessors. Once settlers immigrate to the new area, they do not usually benefit from the arrival of newcomers, who often create the unfavorable conditions they left behind. Thus, it would not be logical to ask how the original inhabitants, now surrounded by a multitude of new neighbors, benefit from living in densely populated areas. The newcomers, likewise, often express the desire to be the last arrivals, indicating that high density settlement can be produced despite net costs to individuals.
Such a simple scenario may often determine animal settlement patterns as
well (Boulinier and Danchin,
1997; Danchin et al.,
1998; Shields et al.,
1988). The habitat selection hypothesis is built on findings in
kittiwakes Rissa tridactyla that suggest that individuals observe the
reproductive success of conspecifics and recruit to the most successful
nesting areas in the following year
(Danchin et al., 1998). The
individuals that occupied the favorable habitat originally often find
themselves surrounded by many new neighbors who do not necessarily provide
them with any benefits. In fact, no benefits of high density nesting are
apparent in kittiwakes, but there is a known cost in the form of increased
ectoparasite transmission (Boulinier,
1995; Boulinier and Danchin,
1996; Danchin,
1992). Thus, the habitat selection hypothesis assumes that
aggregation is a byproduct of many individuals seeking good breeding habitat
by imitating the choices of successful conspecifics. Our point is not to
suggest that there are never benefits to breeding in high density, but rather
that such benefits are not necessary for colony formation.
If aggregation is a byproduct of commodity selection, then we are asking the wrong question when we search for benefits of high-density breeding. Even when individuals receive net benefits from breeding at high density, it is possible that the benefits accrue only after colonies have been produced as byproducts of mate choice and/or breeding habitat selection. If so, we will never learn how colonies form by correlating breeding density with reproductive success, even when benefits of high-density breeding can be identified. Our aim is not to deny the value of correlational studies, but to underline the importance of distinguishing between patterns and processes.
If the need to select breeding habitat and mates produces aggregation as a
byproduct, then why aren't more species colonial? Coloniality occurs in
species that exploit food that is ephemeral and patchily distributed, making
the food uneconomical to defend. Many other species, however, exploit food
that is economically defendable, resulting in large territories that tend to
keep breeders separated by substantial distances. We suggest that even
noncolonial species have a tendency to aggregate, but are constrained from
doing so by the necessity of defending large territories. If this view is
correct, then aggregated breeding can be viewed as the "natural
state" of animals. Although coloniality is implicitly assumed to be
produced by strong selective pressures, the opposite view is now also worth
considering. Perhaps animals do not space widely because it is typically
adaptive to maintain large territories, but rather because they are
constrained against aggregating. Supporting this idea is the occurrence of
aggregated all-purpose territories in areas where habitat quality is uniform
(Ramsay et al., 1999;
Wagner, 1997).
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