Behavioral syndromes

behavior_syndromes

Hundreds, perhaps thousands of studies have looked at foraging behavior or antipredator behavior, or mating behavior, or other social behaviors.  Individual animals, however, exhibit all of these types of behaviors over their lifetime, and all of them can influence individual overall fitness and population and community interactions.  My lab has emerged as a conceptual leader in looking at the ecological and evolutionary implications of correlations among behavior across contexts (behavioral syndromes).  For example, a rapidly growing literature shows that individuals that are more aggressive than others in contests or bolder with predators are also generally more aggressive or bold than others in feeding or mating contexts.  Key questions are: what explains these suites of correlated behaviors?  How do they evolve?  And, how do they affect social and ecological dynamics?

The study of behavioral syndromes (aka animal personalities) has emerged as a very ‘hot’ area in behavioral ecology.  For almost a decade, most major behavior conferences have included symposia or special workshops on the topic.  A workshop at the International Society for Behavioral Ecology conference in 2006 even provocatively asked, “Behavioral syndromes: is it a new paradigm in behavioral ecology?” In 2004, my lab group published two influential, widely cited conceptual overview papers on the topic (Sih, Bell & Johnson 2004a; Sih et al. 2004b) written with a PhD student, Chad Johnson (now an associate professor at Arizona State West) and a postdoc, Alison Bell (now an assistant professor at U. Illinois).  A follow-up paper that updated our thoughts on future directions for the field has also been widely cited (Sih & Bell 2008). The interest in behavioral syndromes has also spilled over into the popular press.  The New York Times ran a full-length magazine section cover article on it (January 22, 2006) – with much of the article devoted to work in my lab.  Other articles on my work on this topic have appeared in the LA Times, the NY Times science section, Science News, Bioscience etc.

My lab’s earlier work on behavioral syndromes included studies on how behavioral carryovers across contexts can help to explain apparently suboptimal behavior including inappropriately high prey activity with predators present (Sih, Kats & Maurer 2003), and excess sexual cannibalism in fishing spiders (Johnson & Sih 2005; Johnson & Sih 2007).  Other experimental studies looked at how the mix of behavioral types (BTs) in a social group influences mating dynamics in water striders (Sih & Watters 2005) and how predation and predation risk can generate a positive correlation between boldness and aggressiveness in stickleback fish (Bell & Sih 2007).

Current, ongoing work in my lab on behavioral syndromes has focused on the following topics.

 

a) Behavioral syndromes and ecological invasions.  In a sense, successful invasive species seem to violate the principle of ecological tradeoffs in that they seem to be good at everything.  They disperse well, colonize and establish well under a broad range of conditions, and build up to high densities and have high impacts; they do well at both low and high densities.  Empirical studies in my lab suggest that part of the success of invasive mosquitofish and signal crayfish might lie in their having a behavioral type (BT) that includes positive correlations between foraging activity or efficiency under a broad range of conditions (at low and high density, with or without risk, on novel or familiar foods), and aggressiveness with competitors (Pintor, Sih & Bauer 2008; Pintor, Sih & Kerby 2009; Rehage, Barnett & Sih 2005b, a; Rehage & Sih 2004).  In particular, current work looks at the importance of BT-dependent dispersal – the tendency for dispersers to be bolder, more exploratory and/or more asocial than resident individuals that do not disperse readily. The notion that dispersers tend to be different from average is part of a conventional view on American history – that American culture can be explained, in part, by the fact that we are a melting pot of the bold, aggressive, fortune-seeking mavericks that chose to migrate to America rather than stay in their home country.  While this idea is intriguing for humans, it is easier to study experimentally in other invasive taxa.  Work in my lab found, for example, that in invasive mosquitofish (officially listed as one of the Top 100 most important invasive species in the world), dispersers tend to be more asocial (and perhaps bolder) than residents that do not disperse (Cote et al. 2010b).  This paper was featured as a new research highlight by both Nature and the Society for Conservation Biology).  Follow-up work added that dispersal tendencies depend not just on the focal individual’s BT, but also on the group’s average BT (Cote et al. 2011).  Additional recent papers provide a conceptual overview on the ecological and evolutionary importance of BT-dependent, or more generally, phenotype-dependent dispersal (Cote et al. 2010a) and on the importance of having a mix of BTs (e.g., both social and asocial individuals) in explaining the ability of invasive species to do well under a broad range of conditions (Fogarty, Cote & Sih 2011).  This work has involved three PhD students (Jenn Rehage (now an assistant professor at Florida International U), Lauren Pintor (now an assistant professor at Ohio State U), and Sean Fogarty) and three postdocs (Julien Cote, Tomas Brodin and Shannon McCauley – all three now have faculty positions at U. Toulouse, U. Umea, U. Toronto, respectively).

b) Developing a ‘theory of behavioral syndromes’.  Although empiricists have examined behavioral syndromes in dozens of species in a broad range of taxa, and found variation in the phenomenon (e.g., while some studies find stable BTs or significant correlations between boldness and aggressiveness, others do not), theoreticians have only begun to develop explicit theory on the topic.  Without theory, empiricists have been documenting patterns, but not testing predictions on the phenomenon. To date, the issue that has most intrigued theoreticians is – if having a BT (e.g., being aggressive or bold) is associated with limited behavioral plasticity that can spillover to result in suboptimal behavior (Johnson & Sih 2005; Johnson JC 2007; Sih et al. 2003), then why do animals have a BT?  Why not be optimally flexible?  We first noted in a note in Nature, the importance of positive feedback loops between individual state (e.g., condition or vigor, information state, skill level) and behavior in plausibly explaining the existence of behavioral syndromes (McElreath et al. 2007).  We followed up with a model that predicts how ecological conditions (risk, resource levels) should influence the expression and stability over ontogeny of BTs (Luttbeg & Sih 2010).  To my knowledge, this is the first model to generate predictions on both when we expect to observe vs not observe behavioral syndromes.  Luttbeg and I are working on a series of further theoretical papers on state-dependent behavioral syndromes.

c) Social ecology of behavioral syndromes.  The notion that outcomes in social situations are frequency-dependent (e.g., depend on the relative frequency of ‘hawks vs doves’ or ‘cooperators vs defectors’) is a fundamental tenet of game theory.  To date, however, surprisingly few studies on behavioral syndromes have looked at how individual behavior and fitness and group outcomes depend not just on the individual’s BT, but on the mix of BTs in the social group.  We discussed this topic, along with numerous other issues on the interface between game theory, social ecology and behavioral syndromes in recent conceptual papers (Sih & Bell 2008) Sih 2013).  In addition, a current NSF grant has supported a series of experiments examining how the mix of BTs in a social group affects social dynamics and sexual selection in water striders.  These studies have produced a large data set involving about 100 observations of multiple behaviors and mating success for each of several hundred water striders, each observed in 3 different experimentally-determined social settings.  These data are allowing us to address numerous potentially important, under-studied topics including how social selection, social skill, social networks and group selection influence sexual selection, and in particular, on how social situation choice (the option of leaving a group when the social situation is suboptimal) influences social and mating dynamics.  While we, of course, feel that there are numerous interesting aspects of this project, most innovative might be our focus on social skill. Sexual selection studies typically focus on the role of male size or ornaments (visual, acoustic or chemical) in determining his mating success. We suggest that in our water striders and perhaps in most systems, variation among males in their behavioral skill also plays a major role in governing mating success.  Key aspects of behavioral (social) skill include ability to choose good places to search for females, ability to efficiently choose which females to attempt to mate with, and ability to exhibit behaviors that most effectively convince those females to mate with you.  In even a ‘simple’ animal like the water strider, variation in social skill appears to have major effects on mating success.  This project involves 2 PhD students (Ann Chang, Sean Fogarty), a visiting PhD student (Pierre-Olivier Montiglio), and a NSF-funded bioinformatics postdoc, Tina Wey.

d) Behavioral syndromes and parasitism.  Parasites are ubiquitous and have important effects on individuals, populations, communities and even ecosystem dynamics, but are relatively under-studied.  In particular, few studies have looked at how behavior affects parasitism and vice versa, and even fewer have looked at how an animal’s BT might relate to parasitism.  In collaboration with Michael Bull (Flinders U, Australia), we are studying how BTs (activity, aggressiveness, sociability) influence social network contacts that govern tick transmission in the sleepy lizard, a large, abundant lizard in south central Australia.  Our project is almost unique in that every adult lizard (N=60) at our study site has a GPS data logger that allows us to know where every individual is all of the time during the entire active season.  Experiments (e.g., habitat manipulations, releases of genetically marked ticks) allow us to gain a perhaps unprecedented understanding of the connections between BT, social networks and parasites/disease are of general interest, but rarely quantified.  A second project on behavioral syndromes and parasites (led by a PhD student, Kelly Weinersmith) focuses on a trematode that encysts in the brain of its killifish host and manipulates its host into exhibiting highly conspicuous (active, bold,) behaviors that often result in the fish being eaten by the parasite’s next host, a wading bird.  Kelly is testing the hypothesis that the fish’s BT (activity, boldness) affects its rate of picking up parasites that further alter the fish’s BT resulting in further accumulation of parasites in a positive feedback loop that eventually results in the fishes demise.  Kelly’s work integrates studies of hormonal mechanisms (and potentially gene expression in the brain), with behavior that has major effects on predation rates and thus on trophic dynamics and energy flow from aquatic to terrestrial ecosystems.  Her work is done in collaboration with Ryan Earley (endocrinologist, U. Alabama) and ecological parasitologists (Ryan Hechinger, Kevin Lafferty, Armand Kuris, UC/Santa Barbara).

e) Implications of behavioral syndromes for other fields. 

Ecological implications of behavioral syndromes.  A group of graduate students and postdocs in the lab collaborated to write a paper published in Ecology Letters (Sih et al. 2012) on how the hallmarks of behavioral syndromes (behavioral correlations across time and across contexts, individual differences within species in behavioral type, and behavioral-type dependent dispersal) yield new insights and predictions for major issues in ecology including: ecological invasions and other aspects of spatial ecology, species distributions per se, population dynamics, species interactions, and species responses to environmental change.

Effects of early stress on the development of behavior and stress response systems.  Neuroscience and Biobehavioral Reviews, a major review journal in this field, ran a special issue on this topic.  The other papers were largely from a human, primate or lab rodent perspective.  They provided me with the papers by the other authors, and asked me to contribute a paper on how my behavioral ecology/behavioral syndromes approach might provide new insights on this issue (Sih 2011).    My paper stimulated new collaborations with internationally recognized evolutionary developmental psychologists (Jay Belsky, Marco Del Giudice).

Behavioral syndromes and animal cognition.  I was invited to contribute a paper on this topic to a Royal Society symposium on animal cognition that was published in the Philosophical Transactions of the Royal Society (Sih & Del Giudice 2012).  My paper focused on an integrative approach for generating predictions (many, new to the field), based largely on the notion that ‘fast’, ‘high risk, high reward’ behavioral types (bold, aggressive, active, exploratory) also exhibit ‘fast, shallow’ cognitive styles (less sampling, less information storage, faster decisions, more intuitive).

Behavioral syndromes and social insects.  After an invitation to speak at a symposium at a major Social Insect conference, I collaborated with a group of scientists from around the world that study behavioral syndromes in social insects to write a conceptual review paper on insights that each field can gain from the other; e.g., insights from  the concept of studying colony personalities, and how they can emerge from non-linear interactions among the personalities of individual within the colony.  The paper has been provisionally accepted by Biological Reviews.

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