The Ecology of Collective Behavior

One of the most familiar examples of collective behaviour is swarming, where large numbers of animals move in a coordinated fashion. However, collective behaviour can take many different forms and it has proven tricky to develop a general theory that successfully captures its diversity. This book proposes a research programme to figure out both how collective behaviour responds to changing environmental conditions, and how it evolves. As far as Gordon is concerned, one things that holds us back is reductionism: "it is not possible to learn how natural systems function collectively by considering the components separately and independently of the world they inhabit [as it] severs the relations that matter" (p. 2).

Gordon's goal here is to outline how she researches collective behaviour. She is particularly interested in how it changes in response to the ever-changing environment. You start to see why studying this can be quite challenging as you are effectively considering second-order dynamics (the dynamics of dynamic behaviour). The book's nine chapters break down into roughly three parts that I will discuss further below.

Chapters 2 to 4 introduce the two ant species that she has worked on for several decades: the desert-dwelling red harvester ant Pogonomyrmex barbatus and the rainforest-dwelling turtle ant Cephalotes goniodontus. Their collective behaviour differs and, as later chapters explore, this can be linked to differences in their environment. She then considers how collective behaviour results from individual interactions and reflects on that buzzword "emergence". A younger Gordon was once a fan; today she is ready "to replace its mystical glow with something more substantial" (p. 33).

The next two chapters present her core framework that explains how collective behaviour depends on, and responds to, environmental dynamics. To reiterate: collective behaviour consists of individuals interacting with each other. She considers three parameters of collective behaviour: rate (fast/slow: how quickly interactions respond to environmental change), feedback (stimulation/inhibition: how interactions change the collective behaviour), and modularity (uniform/modular: a description of network structure in terms of node connectivity, i.e. are all individuals in contact with each other or do they form distinct, internally connected clusters). She then links these three behavioural parameters to three environmental parameters: stability (stable/unstable: how prone the environment is to large or frequent changes), resource distribution (patchy/uniform: how resources are distributed in time and space), and energy flow (low/high: the ratio of energy or resources obtained versus spent; economists also speak of EROI: energy return on investment).

These two sets of three parameters relate to each other as follows, as exemplified by the ant species she studies. Rate depends on stability and resource distribution. Harvester ants live in stable desert environments with uniformly distributed resources and adjust their foraging activity slowly. Turtle ants live in the exuberant chaos of a rainforest where they form rapidly changing foraging trails to exploit ephemeral resources. Feedback depends on stability and energy flow. For harvester ants, foraging is energetically expensive and they need stimulation (positive feedback) from patrollers before they leave the nest. For turtle ants, foraging is energetically cheaper and they will continue to forage until inhibited (negative feedback) by e.g. a shortage of mouths to receive the liquid food they carry home. Modularity (like rate) depends on stability and resource distribution. In harvester ants, modularity is low and individuals are highly connected with information transfer happening in a centralized fashion in the nest. In turtle ants, modularity is high, with foraging decisions resolved locally through interactions of small groups of ants. If the above all seems rather impenetrable, that will be my attempt to condense her framework into just two paragraphs. Fortunately, her treatment of it is more accessible: she presents it as a verbal argument and pads it out with lists of examples from across the biological spectrum.

The third part, then, wraps up the discussion. One chapter provides a very practical research programme for investigating how collective behaviour works: observation followed by experimental disruption. There are some excellent tips here on how to disrupt (stay within the ordinary range of fluctuations) which she contrasts with other standard approaches. She illustrates her approach by taking the reader through decades of her research on harvester ants.

The last two chapters consider the evolution of collective behaviour. In some ways, this is little provocative: participation in collective behaviour is an aspect of an organism's phenotype and thus a trait subject to natural selection, just like any other trait. Where it gets more provocative (depending on your viewpoint) is that, as a pupil of Richard Lewontin, she embraces the Extended Synthesis, including environments (in addition to genes) influencing phenotypic expression, organisms altering their environment (niche construction), and the always hotly debated notion of group selection. Gordon offers interesting critiques here of divisions such as nature/nurture and how they are holding back our understanding of collective behaviour. Particularly insightful is the last chapter that contrasts her framework with the prevailing idea that collective behaviour is marked by a conflict of interest between the individual and the group, i.e. that individuals always prioritize fitness maximization over the collective good. If I understand her correctly, she argues that, because collective behaviour has consequences for individuals, selection can act on how individuals produce collective behaviour. In other words, selection can act on multiple levels simultaneously, without group selection necessarily conflicting with individual selection.

Are there limitations to Gordon's ideas? She indeed expects that her hypotheses will not cover all possible ways that collective behaviour can interact with a changing environment and calls her a framework rather than a deductive theory. Though this book is aimed at biologists studying collective behaviour, the subject matter here is easily accessible to ecologists and evolutionary biologists more generally. The verbal argumentation and numerous examples also put this book within reach of interested general readers. The emphasis on an actionable framework illustrated by her decades-long research on ants makes for a particularly grounded, can-do book. Overall, a very interesting perspective.