"Ant colonies: culture or personality?" an essay by John Hartigan

Army ants (Eciton hamatum) connecting together to form scaffolding for their living bivouac. 

John Hartigan is a professor in the Department of Anthropology at UT Austin. He has written a short reflection on my recent BE article that discuses the merits of using "culture" in place of "collective personality" for colony-level behavioral tendencies. Read the essay here or below. 

Perhaps choosing preferred terminologies comes down to two main factors: the level of biological organization in focus, and the underlying factors driving behavioral patterns.

There is certainly good evidence of non-human animal culture. When I think about what defines animal culture, I imagine certain behaviors, tendencies, or preferences are transmitted socially between individuals and across generations. This may be happening in ant colonies, especially since individual ant behavior can be heavily influenced by social cues from their nestmates. I'm particularly excited about the notion he brings up that culture can be independent of local ecology - that perhaps strong preferences and tendencies arise due to random drift and reinforced by repetition and experience. I can think of some interesting experiments to test for this . . .

John Hartigan
website: https://liberalarts.utexas.edu/anthropology/faculty/hartigan
email: johnhartigan@austin.utexas.edu
twitter: https://twitter.com/aesopsanthro

Ant Colonies: Culture or Personality?

Recent work on “colony personality” among ants prompts the question of why myrmecologists aren’t thinking of these forms of patterned social variation in terms of culture instead. That it’s now commonplace for entomologists to talk about personality is notable, since, like tool use, it was once assumed to be a uniquely human trait—so, yet another crumbling support for the “golden barrier” goes down. Probably though, the news that culture, too, no longer stands as a uniquely human characteristics has yet to influence the analytical frames brought to bear on social insects. But the reason for doing so should be clear; the core question in research on “colony personality” concerns locally patterned forms of social behavior. And culture is the preeminent means for assessing behavioral variation within a species as it is socially structured and patterned in relation to local ecologies. The choice to frame this as “personality,” instead, reflects an interest in finding biological or genetic mechanisms that might enhance evolutionary fitness. In arguing to change this framing—from personality to culture—the advantage lies in opening up an analytical register in addition to “intrinsic” and “environmental” factors as “possible drivers of behavioral difference.” There is, additionally, the matter of how such a framing, in turn, generates more interesting questions about culture, even in relations to humans.

A new article in Behavioral Ecology, “Colony personality and plant health in the Azteca-Cecropia mutualism” (Marting et al. 2018), poses a key question: “Might there be differences in colony behavior depending on the Cecropia species they occupy?” Azteca constructor is a neotropical arboreal ant species, which form obligate mutualist relations with Cecropia trees. In its tightest formulation, this research question concerns whether Azteca colonies vary in their degrees of aggressiveness or boldness in relation to fending off threats in to the trees they colonize. But at its broadest, and formulated in terms of culture instead of personality, this question speaks to larger concerns about social dynamics between species, including those involving humans. How do our cultures vary depending upon companion species relations? Domestication is mutualism writ large and, since it entails cultivation, is the very basis by which we conceptualized culture in the first place. That “colony personality” as kind of superorganism opens up as a mode of inquiry via the question of interspecies mutualism suggests, in turn, that culture is key to driving these kinds of questions and studies further. One has to only consider the resonance here with Alfred Kroeber’s formulation of the “superorganic” as a means to delineate culture as a distinct domain over and against evolution. The issue is how to understand those “super” dynamics that exceed mechanistic explanation in terms of individual organisms and their varying degrees of fitness, evolutionarily or socially.

Marting et al. studied colony-level behavioral traits related to exploratory behavior and boldness in response to threats against the ants and their host. Think anteaters or woodpeckers assailing the colony and sloths or monkeys attacking the trees. The necessity of a massive social or “colony-level” response stems from the fact that the workers don’t have stingers and must rely on their mandibles to dissuade attacking vertebrates. Since most workers will die in these defensive measures, their massing in response to “vibrational disturbance indicates colony defensive aggressiveness and risk-taking boldness.” Sure enough, they found notable variation along a docile-aggressive continuum: “Our results support the existence of a collective behavioral syndrome for colonies of Azteca constructor. We found that colonies differ substantially and repeatably in 2 distinct behavioral traits, all of which were positively related.” Some were more active, responsive, and aggressive than others. “Furthermore, colony behavioral types were correlated with their host plants’ health such that trees containing more aggressive colonies also exhibited less leaf damage.” This is where it makes most sense to bring culture to bear on these dynamics, because the behavioral variation within this species turns on local conditions—life-histories of colonies and environmental factors, such as host trees’ internode size and ants’ nutrition, as influenced by light environment and soil nutrients. And because the central concern is the plasticity of behavior in relation to these local circumstances, as highlighted in the article’s “discussion” section: “The fact that exploration behavior was not consistent over time highlights the importance of assessing a range of colony traits because some behaviors have more plasticity than others.” Quite possibly, this plasticity better understood as a cultural dynamic rather than a matter of personality. This matter turns on whether in the formulation “superorganism,” the focus falls on scaling these dynamics to the explanatory frame of “organism,” just extrapolated, or instead distinctively regarding the “super” aspect that exceeds the individual organism. The latter are exactly why we have the culture concept.

Abstract

Peter R. Marting, William T. Wcislo, and Stephen C. Pratt, “Colony personality and plant health in the Azteca-Cecropiamutualism,” Behavioral Ecology 29, no. 1 (January 2018): 264–71, https://doi.org/10.1093/beheco/arx165.

For interspecific mutualisms, the behavior of one partner can influence the fitness of the other, especially in the case of symbiotic mutualisms where partners live in close physical association for much of their lives. Behavioral effects on fitness may be particularly important if either species in these long-term relationships displays personality. We conducted a field study on collective personality in Azteca constructor colonies that live in Cecropia trees, one of the most successful and prominent mutualisms of the neotropics. These pioneer plants provide hollow internodes for nesting and nutrient-rich food bodies; in return, the ants provide protection from herbivores and encroaching vines. We tested the consistency and correlation of 5 colony-level behavioral traits, censused colonies, and measured the amount of leaf damage for each plant. Four of five traits were both consistent within colonies and correlated among colonies. This reveals a behavioral syndrome along a docile-aggressive axis, with higher-scoring colonies showing greater activity, aggression, and responsiveness. Scores varied substantially between colonies and were independent of colony size and age. Host plants of more active, aggressive colonies had less leaf damage, suggesting a link between a colony’s personality and effective defense of its host, though the directionality of this link remains uncertain. Our field study shows that colony personality is an ecologically relevant phenomenon and sheds light on the importance of behavioral differences within mutualism dynamics.

Anteaters: A Neglected Cost to Ant-Plants?

The tamandua, an arboreal anteater, pondering the potential meal waiting in a nearby Cecropia tree.

The benefits of hosting an ant colony often outweigh the costs for Cecropia trees, which is why the mutualism exists in the first place. Typically, we think of costs in terms of the services the plant provides for the ants; producing food bodies and allowing sap-sucking scale insects to feed. In one extreme example, some species of ants trim the flowers of their plants, reducing fitness in their Cordia hosts.

The unsatiable beast barreling through the understory.

However, a possible cost that has received less attention is anteater attraction. Hosting a colony invites the risk of a potentially catastrophic anteater attack, especially for younger, developing Cecropia trees. I have gathered a few anecdotal observations over the years where I arrive at a long-monitored Cecropia tree, ready to start a behavioral experiment, and find a dismal scene: the tree ripped apart, the stem snapped in half, internodes exposed, ants scattered, and leaves uneaten. I have yet to catch a culprit red-handed, but it was clear the beast was interested in the ants, not the plant. Furthermore, the incisions that opened the internodes looked like the work of precise claws and not brute force, pointing to the tamandua, an arboreal anteater. Regardless of the perpetrator's identity, the plants clearly suffered a serious blow merely by being between the predator and its prey. A setback like this could be detrimental for a pioneer plant in the fast-paced, competitive environment of a light gap.

The scene of the crime - incision points expose the meat of the colony and ignore the foliage. 

Another downed tree with internode incisions. 

Cecropia trees might be a particularly susceptible ant-plant because Azteca ants don't have venomous stings like Pseudomyrmex ants in Acacia trees. Though Azteca are fast and bitey and swift to remove insects, they are likely less effective at deterring large vertebrates like anteaters, leaving their tree exposed to a big risk-by-association. 

Many questions remain - how often does this happen? Can ants and plants recover? Do anteaters target certain sizes or ages of trees? Of course, these ponderings must be tested. Experimental planning is underway.

An instance of attack where the stem was not snapped, but there were still incisions in the internodes.

Presentation at SICB 2018 in San Francisco

Azteca ants gobble up food bodies after they were prevented from accessing them for 24 hours during the greenhouse experiment.

The annual meeting for the Society for Integrative and Comparative Biology is taking place in San Francisco this week, and I'll be presenting part of the findings from the huge, multi-year  greenhouse experiment. How did soil nutrients affect colony aggression and consistency? Come find out this Thursday morning at 10:45 in Nob Hill A-B.