is prevalent among birds. It is often restricted to particular times of year – solitary
species often forage socially, at least during migration – or it can be characteristic of
particular developmental stages. After breeding season, many corvids and parrots form persistent
flocks of juveniles and non-breeding adults. The main advantages of group living are well known.
Most obviously, there is safety in numbers. A group has many watchful eyes, alert to the approach
of danger, so social foragers can pay more individual attention to finding food, while distributing
the demands for security across a wider set of flock members (Hamilton 1971). The second benefit
is foraging efficiency. Food tends to be patchily distributed, so it pays to keep watch on the
successes of other individuals. Where those birds have had good results, the watchers probably
will, too (Vickery et al. 1991; reviewed in Krause & Ruxton 2002). When these ecological
influences are not present, group living is much less common: predatory birds seldom forage
together, presumably because they are not worried about being attacked, and when they do obtain
food, there is not usually enough of it to allow others to partake.
But a diverse set of
avian species go beyond opportunistic aggregations. They hang out together throughout much of
the year, foraging in flocks, breeding communally, and interacting repeatedly with the same group
of birds for long periods of time. Under these circumstances, the group ceases to be a society
of strangers. The birds come to know one another as individuals, to recognize the virtues,
strengths, and weaknesses of others, and to make use of this knowledge in developing and refining
their own life decisions. There is a popular belief that living in such “individualized”
societies imposes greater cognitive demands. As Satchel Paige remarked, “the social ramble ain’t
restful (1953).” And because of this burden of additional memory and information processing,
individualized social systems are thought to provide an important selective force for the
evolution of intelligence. This has been
termed the “social complexity” or “social brain” hypothesis. The accumulated literature is enormous
(reviewed in part by de Waal & Tyack 2009; Emery, Clayton & Frith 2007), but there has been
surprisingly little substantive research on the underlying cognitive mechanisms. Just how
challenging is it really to live in a persisting, individualized social group? What are the
primary capabilities that must be acquired or enhanced?
There is no single
module for social cognition, no brain lobe specifically
dedicated to handling representations of other individuals and their relationships. Social life
draws on a disparate collection of capabilities, all of which have overlapping applications in
other cognitive domains. Highly social birds need to be able to recognize a large number of
other individuals, both by appearance and by voice. And they need excellent episodic memory to
encode and recall salient interactions – aggression, mating, allofeeding, allogrooming, play –
enabling them to construct a cognitive representation of the network of relationships among
flock members. They need detailed representations of at least the most important individuals
in their group, modules that will link to indications of how trustworthy they are, how reliably
they reveal locations of food, what novel foraging techniques they have developed. And because
social groups are dynamic, constantly changing in membership and internal structure, highly
social birds need to be cognitively flexible, able to change their representations on the fly
to accord with recent events.
To study this
assemblage of faculties under controlled conditions, Balda, Kamil, and Bednekoff
suggested that highly social pinyon jays (Gymnorhinus cyanocephalus) might be an
appropriate experimental species. A great deal is known about their natural history
(Marzluff & Balda, 1992). They are one of the most highly social corvids in North America,
foraging and breeding in permanent groups of up to several hundred individuals. And their
social system contrasts strongly with that of other, related jays, enabling comparative
studies of social cognition across species. The most experimentally accessible aspect of
their social system is their dominance hierarchy. Females are dominant to all juveniles, males
are dominant to all females, but within male pinyon jay society, there is a well-established, linear
dominance structure that determines priority in feeding opportunities.
In a group of 200 jays, that still makes for a large number of other birds to recognize and to
remember their relationships. In such large social groups, individual birds cannot rely solely
on their own interactions with other group members to learn their position in the hierarchy.
For groups larger than about 20, the probability of having had an extended direct encounter with any
other, randomly chosen male becomes vanishingly small (Seyfarth & Cheney 1990,
especially pp. 80-86).
So we would expect
that highly social species should be very good at making use of heuristics to fill in the blanks
in their social network (Watts 1999). Given that the dominance hierarchy is linear, the
simplest heuristic for extrapolating relative dominance is transitive inference. The mechanism
works like this: Consider three pinyon jays in the same flock. Let’s call them Arthur, Basil,
and Charlie. Suppose that sometime in the past, Charlie was defeated in an aggressive interaction
with Basil. Charlie now behaves submissively whenever he and Basil encounter one another. Later
on, Charlie sees Basil behaving submissively to Arthur, a bird with whom Charlie has never
interacted. When Charlie subsequently meets up with Arthur in person, Charlie uses his known
relationship to Basil and Basil’s observed relationship to Arthur to predict the likely outcome
of the interaction. So on the basis of prior information alone, Charlie initially behaves
submissively to Arthur, even without a confirmatory fight. If a jay knows that C < B,
and observes that B < A, it can infer that C < A. Birds don’t employ
mathematical logic, but knowledge of a social network can be used for the same purpose.
We conducted three lines of investigation related to social inference of dominance status. In
the first, we constructed virtual dominance hierarchies in contests between pairs of captive
male pinyon jays, testing for their ability to infer their status relative to that of strangers
(Paz-y-Miño, Bond, Kamil & Balda 2004;
see the Social Inference
page). Prior to this work, transitive social inference had never been demonstrated
under controlled conditions in animals. In this experiment, we found that pinyon jays did,
in fact, draw sophisticated inferences about their own dominance status based on interactions
that they observed, the first direct demonstration that animals use transitive inference in
Our second research thread involved comparing the transitive inference abilities of pinyon
jays to that of related corvids that do not live in large, persistent flocks. Several of the
comparison species could not be tested reliably in pair-wise encounters: they would not
establish tolerant relationships when confined together in a small cage. So we transposed
the task to an operant design, using transitive inference of the reward relationships among
a set of colored symbolic targets (von Fersen et al. 1991; reviewed in Lazareva 2012). We first
compared pinyon jays to relatively nonsocial western scrub jays (Aphelocoma californica). Pinyon jays learned to track multiple dyadic relationships more rapidly than scrub jays and
displayed a more robust and accurate mechanism of transitive inference
(Bond, Kamil, & Balda 2003;
see the Symbolic Inference page). This work was later
extended to additional comparison species with more nuanced results: both social complexity and
reliance on cached food independently promoted high accuracy in symbolic transitive inference
(Bond, Wei, & Kamil 2010).
The results provided a clear demonstration of the association between social complexity
and cognition in birds and confirmed that similarly challenging ecological
processes can convergently promote some of the same cognitive abilities.
The third line of research explored whether complex sociality in jays was associated with
higher flexibility. Because social networks are plastic structures, changing in both composition
and organization over time, we predicted that species that experience higher levels of social
complexity should also be more flexible in dealing with modifications and reversals in
hierarchical order. We first tested pinyon jays, scrub jays, and Clark’s nutcrackers
(Nucifraga columbiana) in serial reversal learning, a classical operant design in
which subjects learn to respond differentially to two stimuli. When the task is fully acquired,
reward contingencies are reversed, requiring the subject to relearn the altered associations.
This alternation of acquisition and reversal can be repeated many times, and the ability of a
species to adapt to this regimen has been considered as a primary indication of behavioral
flexibility. Pinyon jays displayed significantly lower error rates than did nutcrackers or
scrub jays after reversal of reward contingencies for both spatial and color stimuli
(Bond, Kamil & Balda 2007).
In a later study,
we used a list-linking procedure (Treichler & Van Tilburg, 1996) to explore
the processes by which pinyon jays flexibly assemble cognitive structures from fragmentary and often
contradictory data. The jays were trained to a high level of accuracy on two implicit transitive
lists -- A > B > C > D > E and
1 > 2 > 3 > 4 > 5. They were then trained on just
E > 1, informing
them of the relationship of the single pair that would link the two lists into a composite,
10-item hierarchy. Following linkage training, the birds were tested on nonadjacent probe pairs
drawn both from within (B‑D and 2‑4) and between
(D‑1, E‑2, B‑2, C‑3) each of the original lists. Linkage
training resulted in a significant transitory disruption in performance, and the adjustment to the
resulting implicit hierarchy was hardly instantaneous. But the birds all recovered their original
accuracy, forming a reliable 10-item sequence, and they did so much more rapidly than would
be expected from a simple associative learning process. Detailed analysis of the course of the
disruption and its subsequent recovery provided important insights into the cognitive mechanism
underlying symbolic inference
(Wei, Kamil & Bond 2014).
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