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Behavioral Syndromes: an Ecological and Evolutionary Overview Review TRENDS in Ecology and Evolution Vol.19 No.7 July 2004 Behavioral syndromes: an ecological and evolutionary overview Andrew Sih1, Alison Bell2 and J. Chadwick Johnson3 1Department of Environmental Science and Policy, University of California, Davis, CA 95616, USA 2Department of Environmental and Evolutionary Biology, Graham Kerr Building, University of Glasgow, UK, G12 8QQ 3Division of Life Sciences, University of Toronto at Scarborough, 1265 Military Trail, Toronto, Ontario, Canada, M1C 1A4 Recent studies suggest that populations and species for example, life-history or dispersal syndromes [4,5]. We often exhibit behavioral syndromes; that is, suites of therefore refer to suites of correlated behaviors as BEHA- correlated behaviors across situations. An example is VIORAL SYNDROMES. A population or species can exhibit a an aggression syndrome where some individuals are behavioral syndrome with each individual showing a beha- more aggressive, whereas others are less aggressive vioral type (e.g. more bold or more shy). Alternatively, a group across a range of situations and contexts. The existence of species can exhibit a syndrome with each species having a of behavioral syndromes focuses the attention of beha- behavioral type (e.g. species that are more bold versus those vioral ecologists on limited (less than optimal) beha- that are more shy). vioral plasticity and behavioral carryovers across The idea of studying correlated suites of behaviors situations, rather than on optimal plasticity in each iso- across situations represents an important shift in how lated situation. Behavioral syndromes can explain beha- behavioral ecologists typically address behavior [6]. In viors that appear strikingly non-adaptive in an isolated essence, when traits are correlated, they should be studied context (e.g. inappropriately high activity when preda- together, as a package, rather than as isolated units. Here, tors are present, or excessive sexual cannibalism). we describe why behavioral syndromes should be import- Behavioral syndromes can also help to explain the ant and we review recent studies that show that maintenance of individual variation in behavioral types, behavioral syndromes have major effects on individual a phenomenon that is ubiquitous, but often ignored. fitness, species distributions (including species invasions) Recent studies suggest that the behavioral type of an and speciation rates. We also identify crucial directions for individual, population or species can have important future empirical and theoretical work. ecological and evolutionary implications, including major effects on species distributions, on the relative Why are behavioral syndromes important? tendencies of species to be invasive or to respond well Consider an aggression syndrome where some individuals to environmental change, and on speciation rates. are more aggressive than others across a range of Although most studies of behavioral syndromes to date situations. All individuals shift their aggression levels have focused on a few organisms, mainly in the labora- up or down depending on the situation; however, some tory, further work on other species, particularly in the remain consistently more aggressive than others (i.e. their field, should yield numerous new insights. rank order is maintained). More aggressive individuals should do well in competitive situations where aggression Humans show consistent individual differences in person- is favored; however, if the general aggressive tendency ality [1]. For example, some people are generally more bold, whereas others are generally more shy. In statistical Glossary terms, the tendency for individuals to differ consistently in behavior (e.g. in boldness) across SITUATIONS (see Glos- Behavioral correlation across situations: between-individual consistency across situations that can either involve the same context but in different sary) is quantified as a BEHAVIORAL CORRELATION ACROSS situations (e.g. feeding activity in the presence versus absence of predators), SITUATIONS. The analog of personality has been studied in or different contexts in different situations (e.g. aggression towards con- considerable detail in a few primates, domesticated specifics in the absence of predators versus feeding activity in the presence of predators). animals and laboratory rodents [2,3], with much of the Behavioral syndrome: a suite of correlated behaviors reflecting between- focus being on the genetic and neuroendocrine bases of individual consistency in behavior across multiple (two or more) situations. A population or species can exhibit a behavioral syndrome. Within the variation in BEHAVIORAL TYPE. However, recent studies by syndrome, individuals have a behavioral type (e.g. more aggressive versus ethologists and behavioral ecologists have documented less aggressive behavioral types). ‘animal personalities’ in a broad range of ‘non-model Context: a functional behavioral category; e.g. feeding, mating, antipredator, parental care, contest or dispersal contexts. organisms’, including several mammals, birds, lizards, Situation: a given set of conditions at one point in time. Different situations amphibians, fish, mollusks and arthropods [3]. Evolutionary could involve different levels along an environmental gradient (e.g. different ecologists refer to suites of correlated traits as syndromes; levels of predation risk) or different sets of conditions across time (e.g. the breeding season versus the non-breeding season). Corresponding author: Andrew Sih ([email protected]). www.sciencedirect.com 0169-5347/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2004.04.009 Review TRENDS in Ecology and Evolution Vol.19 No.7 July 2004 373 carries over into other situations, aggressive individuals predatory sunfish Lepomis cyanellus [9]. Separate studies might be unsuitably aggressive in CONTEXTS where found that activity of A. barbouri in the absence of caution or care are more appropriate (e.g. in an predators is correlated to growth rates [13] and that antipredator or parental care context). Conversely, activity results in high sunfish predation [14]. Brodin and less aggressive individuals might do well in situations Johansson [15] found parallel results in the damselfly where low aggression is favored, but poorly in Coenagrion hastulatum. competitive situations. Another ecologically important behavioral axis is This simple notion shifts classic thinking in behavioral aggressiveness, or the tendency to attack other individ- ecology in several ways [6]. First, whereas behavioral uals. For example, more aggressive funnel web spiders ecologists typically treat behavior as being potentially Agelenopsis aperta are quicker to attack both prey and infinitely plastic (all individuals can exhibit the optimal conspecific territorial intruders than are less aggressive behavior in all contexts), the notion of behavioral spiders [16]. Subsequent work showed that aggressive syndromes implies limited behavioral plasticity. The spiders also exhibit higher levels of non-adaptive wasteful very idea that we can classify individuals as being more killing, where spiders kill but then do not consume prey versus less aggressive implies a limit to their range of [17]. A particularly intriguing consequence of this syn- plasticity. Second, whereas behavioral ecologists tend to drome is a spillover to sexual cannibalism (where females study ecological situations (e.g. behavior during mating attack and consume courting males). Arnqvist and versus non-mating seasons) in isolation from each other, Henriksson [18] documented non-adaptive, excess pre- the behavioral syndrome idea suggests the need to track copulatory sexual cannibalism in a fishing spider where individual behavior and performance across situations some females apparently attack every male that they (i.e. to study aspects of an overall syndrome in an encounter and thus do not mate. The authors hypothesized integrated fashion). For example, to understand individ- that this behavior could be explained as a non-adaptive ual variation in parental care behavior fully, it might be carryover from a general feeding aggression syndrome; necessary to study how it is correlated with contest that is, strong selection favoring high feeding voracity behavior, or antipredator behavior, and vice versa. The in juvenile females (owing to strong food limitation) existence of limited plasticity and behavioral correlations might spillover to cause an inappropriately high can cause individuals to often exhibit behavior that tendency for those females (when they mature to appears suboptimal when viewed in isolation. Finally, adulthood) to attack males. whereas behavioral ecology often ignores individual Several studies have found that aggressiveness is variation in behavior (focusing instead on shifts in average correlated to boldness. One of the first studies to document behavior in response to environmental variation [7,8]), correlations between behaviors in different contexts the behavioral syndrome framework quantifies individ- showed that individual male stickleback Gasterosteus ual variation in behavior and attempts to explain the aculeatus hypothesized that this correlation might reflect maintenance of this variation. the shared effects of gonadal steroids on both behaviors [19]. Riechert and Hedrick [16] also found that more Types of ecologically important behavioral syndromes aggressive female spiders were more bold (quicker to Tradeoffs play a crucial role in explaining many
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