Thursday, December 16, 2004

Did Crows Eat Your Brain? (Full Text - Html) (PDF)

The Mentality of Crows: Convergent
Evolution of Intelligence in Corvids and Apes

Nathan J. Emery1* and Nicola S. Clayton2

Discussions of the evolution of intelligence have focused on monkeys and apes because
of their close evolutionary relationship to humans. Other large-brained social animals,
such as corvids, also understand their physical and social worlds. Here we review recent
studies of tool manufacture, mental time travel, and social cognition in corvids, and
suggest that complex cognition depends on a ‘‘tool kit’’ consisting of causal reasoning,
flexibility, imagination, and prospection. Because corvids and apes share these cognitive
tools, we argue that complex cognitive abilities evolved multiple times in distantly
related species with vastly different brain structures in order to solve similar
socioecological problems.
In Aesop_s fable, a thirsty crow spied a
pitcher containing a small amount of
water. Unfortunately, the water was out
of reach of the crow_s bill, but next to the
pitcher was a pile of stones. The crow began
placing the stones in the pitcher, thereby
raising the water until it could drink. Did the
crow understand that its actions would
increase the water level?
Throughout folklore, the corvids (crows,
jays, ravens, and jackdaws) (Fig. 1) have
been credited with intelligence. Recent
experiments investigating the cognitive abilities
of corvids have begun to reveal that this
reputation has a factual basis. These studies
have found that some corvids are not only
superior in intelligence to birds of other avian
species (perhaps with the exception of some
parrots), but also rival many nonhuman
primates. Traditionally, studies of complex
cognition have focused on monkeys and apes
(1). However, there is no reason to assume
that complex cognition is restricted only to
the primates (2). Indeed, the social intelligence
hypothesis (3) states that intelligence
evolved not to solve physical problems, but
to process and use social information, such as
who is allied with whom and who is related
to whom, and to use this information for
deception (4). There is evidence that some
other large-brained social animals, such as
cetaceans, demonstrate similar levels of intelligence
as primates (5). Corvids also
appear to meet many of the criteria for the
use of social knowledge in their interactions
with conspecifics (6).
Do Corvids Have the Brains for
Complex Cognition?
The crow has a brain significantly larger
than would be predicted for its body size (7),
and it is relatively the same size as the
chimpanzee brain. The relative size of the
forebrain in corvids is significantly larger
than in other birds (with the exception of
some parrots) (2), particularly those areas
thought to be analogous to the mammalian
prefrontal cortex: the nidopallium and mesopallium
(Fig. 2B) (8, 9). This enlargement of
the ‘‘avian prefrontal cortex’’ may reflect an
increase in primate-like intelligence in corvids
(10, 11).

An Overview of Corvid Cognitive

To fully appreciate how corvid and ape
psychology are similar, it is important to describe
how corvids may represent their physical
and social worlds, and how these forms
of mental representation may be similar or
dissimilar to those used by apes in solving
similar problems. We use the term ‘‘understanding’’
to convey the idea that corvids
and apes reason about a domain (physical or
social) in a way that transcends basic associative
and reinforcement processes.
Tool use and manufacture. Tool use is
defined as ‘‘the use of an external object as a
functional extension of mouth, beak, hand,
or claw, in the attainment of an immediate
goal’’ (12). Although many birds, primates,
and other animals use tools, it is not clear
whether any of these species appreciate how
tools work and the forces underlying their
function. Perhaps the most convincing candidates
are New Caledonian crows, who
display extraordinary skills in making and
using tools to acquire otherwise unobtainable
foods. In the wild, they make two types of
tools. Hook tools are crafted from twigs by
trimming and sculpting until a functional
hook has been fashioned (13) and are used to
poke out insect larvae from holes in trees
using slow deliberate movements (14).
The crows also manufacture stepped-cut
Pandanus leaves (14), which are used to
probe for prey under leaf detritus, using a
series of rapid back-and-forth movements or
slow deliberate movements that spear the
prey onto the sharpened end or the barbs
of the leaf, if the prey is located in a hole.
These tools are consistently made to a standardized
pattern and are carried around on
foraging expeditions (15). The manufacture
of stepped tools appears to be lateralized at
the population level (16) and tool use at the
individual level (17, 18).
Observations of the crows’ tool use in the
wild suggest complex cognition. For example,
there is potential cumulative evolution in
the complexity of stepped tools (increasing
the number of steps required to make a more
complex tool), which are analogous to minor
technological innovations in humans (19).
There are also population differences in the
types of tools manufactured (19), seemingly
independent of ecological variability, which
has been suggested as a form of culture in
chimpanzees (20).
Laboratory experiments have confirmed
the sophisticated cognitive abilities of these
crows. One of them, Betty, appears to be
capable of reasoning by analogy with her
previous experience with hooks, by modifying
nonfunctional novel material (metal
wire) into hook-like shapes to retrieve food
in a bucket inside a vertical tube (21). Furthermore,
she chooses the correct length or
diameter of tool out of a ‘‘tool box’’ containing
tools of different lengths and widths
to reach normally inaccessible food (22, 23).
Traveling mentally in time and space.
Many corvids cache food for future consumption;
either a large amount of seeds cached
over a wide area, which are stored seasonally,
or a smaller amount of higher-quality,
perishable material, which is recovered hours
or days later. These differences may require
different cognitive abilities for successful
retrieval. Clark’s nutcrackers living at high
elevations cache up to 30,000 pine seeds
over a wide area and can recover them up to
6 months later (24). By contrast, western scrub
jays living in more temperate environments
cache fewer of a wider variety of food items
that differ in their level of perishability and
are recovered after much shorter periods (25).
Cache recovery may require more than
simply remembering where their caches are
hidden, for species that cache many types of
food. These species may need to process
information about the location of the cache
site, the type and perishability of the cached
item, and the social context of caching (26).
When caching perishable food, it is prudent
to learn something about the decay rates of
the food, and if two or more perishable foods
are cached, to learn their relative decay rates,
in order to recover food when it is still fresh
and edible. Laboratory studies have capitalized
on the fact that western scrub jays readily
cache perishable foods but will not consume
these items when they have degraded.
When jays were allowed to cache perishable
and nonperishable foods, they were able
to remember not only which foods they
cached where, but also how long ago they
had cached them. If a short time had elapsed
between caching and recovery, then they
recovered the perishable food. But if they
had cached a long time ago, they did not
attempt to recover the rotten degraded food
and selectively searched for the nonperishable
caches (27, 28). Furthermore, they could
recall when they cached different foods in the
same location and could even distinguish
between two caches of the same food type
that had been cached at different times (29).
These results suggest that scrub jays remember
the ‘‘what, where, and when’’ of specific
caching events (episodic-like memory). This
representation of the time since caching is
essential for the efficient recovery of perishable
food items (25, 26).
Social cognition of cache protection and
pilfering. Food storers should also be sensitive
to the social context of caching, because
caches are susceptible to pilfering (30). For
pilferers, the ability to quickly and efficiently
locate caches made by others may be the
difference between successful pilfering and
attack by the storer. A number of corvids observe
conspecifics caching and demonstrate
excellent observational spatial memory for the
location of another bird’s caches (25, 31, 32).
The use of observational spatial memory
as a pilfering strategy may differ between
species depending on level of sociality, and
as such may be an adaptive specialization
(33). Do social pinyon and Mexican jays,
and territorial Clark’s nutcrackers, remember
where another bird has cached (31, 34)?
Pinyon jays remembered the specific location
of others’ caches after 1 and 2 days, as did
Mexican jays, whereas Clark’s nutcrackers
were only as accurate as chance after 1 day.
After 2 days, the Clark’s nutcrackers were
only accurate at recovering their own caches,
not those they had observed. (34). This finding
supports the adaptive specialization of
the social learning hypothesis in corvids;
however, another study is more ambiguous
(35). Furthermore, western scrub jays are
semiterritorial, and they have highly accurate
observational spatial memories (25).
The social context of caching may be
viewed as an arms race between storers and
pilferers, in which storers use counterstrategies
to minimize the risk of having their
caches pilfered (36). However, individual
birds can play both roles. Storers engage in a
number of cache protection strategies, which
may or may not be dependent on cognitive
processes. Examples of such strategies include
hiding food behind barriers so that
pilferers cannot see them (37, 38), waiting
until pilferers are distracted before resuming
caching (32, 39), leading competitors away
from the location of caches (40), or making
false caches that contain either an inedible
item, such as a stone, or nothing at all (41).
Some corvids return alone to caches they had
hidden in the presence of conspecifics and
readily recache them in new places unknown
to the potential thief (41, 42).
One strategy that may decrease the
probability that a pilferer will successfully
steal another’s caches is to eliminate or
reduce the information available to the pilferer
at the time of caching, such as caching
behind a barrier (37). Of course, this behavior
could be explained as ‘‘out of sight, out of
mind’’ (that is, cache when you no longer see
others present), as opposed to understanding
what another can or cannot see. There is some
evidence, however, that when given a choice
of two cache sites that an observer can see,
storers prefer to cache in the sites least visible
to the observer, such as in a darkened part of a
cage as compared to an illuminated part (43).
An experimental approach is crucial for
understanding the processes underlying these
behaviors and determining the effects of
experience, particularly in relation to theory
of mind. Consider the observation of birds
moving food they had hidden in the presence
of other individuals and recaching the items
in new places when those observers were
no longer present. In
the wild, one might
explain the presence
or absence of another
bird as being
purely coincidental
to the caching and
recaching events. To
test this, hand-raised
western scrub jays
were allowed to cache
either in private or
while a conspecific
was watching and
then recover their
caches in private
(42). Individuals with
prior experience of
pilfering another
bird’s caches subsequently
recached food
in new sites, but only
when they had been
observed during caching. Because the two
conditions were identical at the time of
recovery, the birds had to remember whether
or not they had been watched during
caching, and if so, whether to recache during
recovery and whether in new or old sites.
Note that jays without experience of themselves
being pilferers did not move their
caches to new sites. The inference is that
these birds, who had been thieves in the past,
engage in experience projection (2); that is,
they relate information about their previous
experience as a pilferer to the possibility of
future stealing by another individual, and
modify their recovery strategy appropriately.
By focusing on the counterstrategies of the
storer when previously observed by a potential
thief, this experiment raises the possibility
that recaching behavior is based on
simulation of another’s viewpoint (one form
of mental attribution) (2).

A Cognitive Tool Kit for Corvids and

Our review of corvid cognition suggests that
these birds display similar intelligent behavior
as the great apes. However, is the content
of the cognitive processes based on a similar
or different mental foundation? One reason
why the processes may be similar is that corvids
and apes face many of the same socioecological
challenges, such as locating perishable
food distributed in time and space or understanding
the relationships between different
individuals within large social groups. We suggest
that these environmental problems are
solved by using four cognitive tools that have
driven the evolution of complex cognition in
corvids and apes: causal reasoning, flexibility,
imagination, and prospection (Fig. 3).
Causal reasoning. Some of the examples
of tool use and manipulation described
earlier suggest that some corvids, like apes,
may understand the causal relationships by
which these tools operate or are effective. In
the absence of detailed knowledge about the
acquisition of tool use in the wild, the role of
basic instrumental conditioning processes
remains unclear (44). However, what may
suggest that corvid tool use transcends such
noncognitive processes is Betty’s innovative
tool manufacture in the lab (21). The fact
that she transformed a novel piece of wire
into a hook-like tool suggests some appreciation
of mechanical causation.
Although an understanding of physical
causation suffices for interactions with inanimate
objects, transactions within the social
realm also require representations of mental
causation. Do animals also realize that
mental states (beliefs, desires, and intentions)
can be causally effective? This question
is best studied in the sphere of social
cognition by investigating whether an animal
can represent the behavior of conspecifics
(or heterospecifics) as caused by their intentions,
beliefs, and desires; in other words,
can represent that these animate beings are
intentional agents. Animate beings are distinct
from inanimate objects: Although they
can be acted on by external forces, they also
have mental states. This is an essential precursor
for predicting a conspecific’s or
heterospecific’s behavior and manipulating
another for personal benefit (tactical deception).
Although still controversial, corvids
and apes appear to demonstrate a similar propensity
for representing animate beings as
causal agents (6, 45, 46).
Flexibility. The ability to act on information
flexibly is one of the cornerstones of
intelligent behavior. Deployment of flexible
learning strategies may form the basis for
creativity as demonstrated in social and object
play (47) and innovation (48). Here we
focus on experimental evidence. In the food
perishability experiments described earlier,
scrub jays integrated information about the
what, where, and when of a trial-unique
caching event to influence their cache recovery
decisions (29). However, for a bird that
caches perishable food items in fluctuating
temperatures (ranging from cold to extreme
heat), it is critical that the bird be able to
update its knowledge about decay rates and
apply this knowledge to information already
encoded. To investigate this, scrub jays were
allowed to cache preferred, perishable
crickets and less preferred, nonperishable
peanuts (49). After caching, but before
recovery, the jays gained new information
that the crickets decayed more quickly than
they had expected when they had cached
them.When tested, the scrub jays used this new
information and switched to recovering the
peanuts rather than the now-inedible crickets.
One important aspect underlying all flexible
behavior is the ability to generalize learned
rules in order to apply them to novel stimuli or
situations. This ability to solve transfer problems
by abstracting general rules is what
distinguishes rule learners from rote learners.
When presented with a series of different
discriminations to learn, corvids (blue jays,
rooks, jackdaws, and Eurasian jays), like monkeys
and apes, extract the general rule, such
as win-stay, lose-shift rather than having to
learn each new discrimination afresh. By
contrast, pigeons appeared to be rote learners,
solving the task eventually by learning
each discrimination individually (50, 51).
Corvids also demonstrate superior abilities
in other transfer problems. One case is
the ability of some corvids (pinyon jays and
western scrub jays) to solve transitive
inference problems (A 9 B 9 C 9 D), in
which the birds are trained on an ordered set
of various pairwise comparisons (such as
A_ B–, B_ C–, etc.). When tested, they
must transfer information about the dyadic
relationships to novel pairs (such as B versus
D) to solve the task. Pinyon jays outperform
scrub jays on some aspects of this task
(although their learning curves are similar),
which has been attributed to differences in
sociality (52). Indeed, pinyon jays appear to
use transitive inference to rank unknown individuals
in a dominance hierarchy and use
this information in their subsequent social interactions
(53). Finally, corvids are proficient
in transferring to novel stimuli in matching and
oddity discriminations. Rooks, jays, and jackdaws
outperform pigeons on these problems
(51). What is common to these various transfer
tasks—from learning sets to transitive
inference—is the ability to abstract general
rules or relationships that transcend the basic
learning experience. Abstraction might be an
important process underlying this flexibility.
Imagination. Imagination refers to the
process by which scenarios and situations
that are not currently available to perception
are formed in the mind’s eye. One advantage
of imagination is that possible situations can
be practiced internally (simulated) before they
are actually performed, which may be important
when encountering novel stimuli within a
familiar context. The ability to form representations
of objects that are outside of perception
(object permanence) may be a precursor
of imagination. In food-caching corvids, object
permanence is essential for the successful recovery
of cached food; in young magpies, it develops
around the same time as caching (54).
Insight, cognitive maps, and experience
projection are three candidates that indicate
the use of imagination. In a classic study of
insight, a group of chimpanzees was presented
with a problem (a banana hanging on string
out of their reach), some sticks, and a series of
boxes (55), which they appeared to spontaneously
use to reach the banana. The implication
has been that the chimpanzees imagined the
solution to the problem before performing it,
although this explanation has been disregarded
as trial-and-error learning (44). Recent experiments
in ravens may provide clearer evidence.
Hand-raised ravens encountered a novel problem
(meat attached to string hanging from a
perch) (56). The only successful method was
to pull the string up, place the foot on the
string after each pull up, and repeat this multiple
times until the food was in reach, a solution
some ravens reached on the first trial (that
is, without recourse to trial-and-error learning).
Furthermore, the ravens chose the correct
string from a number of alternatives, choosing
the string attached to the food, as opposed
to a similarly sized stone. They did not
fly off with the attached food, nor did they
attempt to pull up items that were too heavy.
A second candidate for imagination is the
use of a cognitive map (a mental representation
of the major landmarks in the environment)
to aid in navigation, particularly
when novel routes are required. Although the
issue of whether animals possess cognitive
maps remains controversial (57), the enhanced
spatial memory of the food-caching
corvids might be a prime candidate for indicating
their existence. It has been suggested
that Clark’s nutcrackers may use something
akin to a cognitive map to locate a hidden
goal object, even when the position of the
fixed distal landmarks changed with respect
to the local landmarks and the goal (58).
A final candidate for imagination is
experience projection or role taking, in
which an individual simulates another’s
experiences and perspective (2). This ability
implies that an observer forms a representation
of a model’s perspective or experiences
that are similar to or different from their
own. In a cooperative task to investigate role
taking, chimpanzees, but not rhesus monkeys,
reversed the roles they were trained on
(59, 60), suggesting that the chimpanzees
may have taken their partner’s perspective;
however, both monkeys and chimpanzees
failed to immediately transfer to the opposite
role on the first trial (61).
The example of recaching demonstrated
by western scrub jays may present a case for
imagination, because the jays needed to have
remembered the relevant previous social
context, used their own experience of having
been a thief to predict the behavior of a pilferer,
and determined the safest course of action
to protect the caches from pilferage (42).
Prospection. In the previous discussion of
imagination, an agent could simulate scenarios
with respect to past events; however, one
function of simulation may be to imagine
possible future events, so-called prospection.
Although various behaviors have been proposed
as examples of future thinking, it is
important to distinguish between those behaviors
that are tuned to current thinking and
motivational states and those that are tuned
to future thinking and motivational states
(62, 63). Caching would appear to provide a
natural example of future planning. Food is
hidden in the present to provide sustenance
for the future. However, if caching is controled
by hunger, then this current motivational
state may facilitate caching without
any appreciation of becoming hungry in the
future (63).
The example of recaching by scrub jays
may also provide the best evidence for prospection
(42). Recaching items in new sites
when an observer saw the placement of caches,
but not when the caches were made in private,
suggests that the jays were using a strategy
to protect their caches from future cache
pilfering, not because of hunger levels. It is
important to stress that prospection is highly
reliant on retrospection (63).


There are many aspects of corvid and ape
cognition that appear to use the same
cognitive tool kit: causal reasoning, flexibility,
imagination, and prospection. We suggest
that nonverbal complex cognition may
be constructed through a combination of
these tools. Although corvids and apes may
share these cognitive tools, this convergent
evolution of cognition has not been built on a
convergent evolution of brains. Although the
ape neocortex and corvid nidopallium are both
significantly enlarged, their structures are very
different, with the ape neocortex having a
laminar arrangement and the avian pallium
having a nuclear arrangement (2). It is unclear
what implications these structural differences
have. However, cognition in corvids and
apes must have evolved through a process
of divergent brain evolution with convergent
mental evolution. This conclusion has important
implications for understanding the
evolution of intelligence, given that it can
evolve in the absence of a prefrontal cortex.

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64. N.J.E. is supported by a Royal Society Research Fellowship.
The writing of this review was supported by
grants from the Biotechnology and Biological Sciences
Research Council (grants S16565 and BBS/B/05354),
the Royal Society, and the University of Cambridge.
We thank A. Dickinson, S. de Kort, C. Rutte, G. Hunt,
and A. Kacelnik for comments on the manuscript.

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