Principles of Animal Behavior (Second Edition)

definition usually represents or leads to a testable hypothesis. For example, if a researcher chooses to call all social transmission in animals

selection-based evolution—then I'm

not yet convinced that it is present in any nonhuman species. To answer this intriguing question we would

"culture" because he believes that

need much more information about

the nongenetic transmission process is the most important ingredient of culture, then his definition represents a testable hypothesis, and therefore contributes to progress in the field.

the dynamics of social transmission in animals, and particularly about the fidelity with which behaviorial variants are copied across successive links in a transmission chain. If adaptive innovations are not transmitted

If you had to make an educated guess, how common would you say that cultural transmission is in nonprimates? There are many kinds of social

faithfully, then an inheritance system based on social learning cannot have effects comparable to those of genebased selection.

especially "clever," they all have the potential to yield very substantial adaptive advantages. Therefore, if "culture" is understood liberally to mean behavior affected by social learning, then I think it's very common in nonprimate as well as primate taxa. The phenotype of any animal

neurons could mediate imitation or

copying of very specific features of behavior—the shape or topography of body movements. But, due to doubts

that monkeys are able to copy at this level of specificity, many people have rejected this idea, and instead focused

on the possibility that mirror neurons are involved in action understanding, theory of mind, or empathy, processes that are not so closely related to culture. I think that was a mistake.

Looking into the crystal ball, I predict that the connection between imitation and mirror neurons—in the

premotor cortex and elsewhere in the brain, in monkeys and in other

learning and, although most of them

do not require the learner to be

At first glance, it looks like mirror

How do you see advances in neurobiology impacting the study of animal culture over the next five

years?

The discovery of "mirror neurons" in the premotor cortex of macaque monkeys has caused a huge stir among those who study imitation and related processes in humans.

that lives in a social group, and in an environment that is sufficiently variable to warrant adaptation through learning, is likely to be influenced by social learning. When Iwas a graduate student,

These cells fire when the animal

I had the bright idea that adult Syrian hamsters may have poor social learning ability because they are "solitary"; except when mating, they are highly intolerant of even the presence of mature conspecifics. However, my attempts to show this

neurons does not seem to have had

executes an action—for example, grasping an object—but also when the animal passively observes a human performing the same action. Curiously, the discovery of mirror such a dramatic impact on those studying social learning in animals. Part of the reason for this may be that there are still many gaps

taxa—will be "rediscovered," and

that well-integrated behavioral and neurobiological studies will begin to answer important questions about mirror neurons. This will be

greatly assisted by more widespread availability of scanners for functional magnetic resonance imaging (fMRI) of primates and rodents. The most important question, in my mind, is: Where do mirror neurons come from? Are some animals born with mirror

neurons for a range of behaviors, or are mirror neurons made through associative learning? The answer to this question will tell us a great deal about the origins of the capacity to imitate and, insofar as imitation is involved in cultural transmission,

about the origins of culture.

between research on the functions and mechanisms of animal behavior.

experimentally, by comparing the

The work of neurobiologists,

social learning ability of adult and predispersal juvenile hamsters, were a rank failure. In each experimental task, the adult hamsters cheerfully learned

psychologists, and ethologists is becoming ever more integrated, but these are still, to some extent, three separate scientific cultures. However, there may be another, more specific reason why those studying social learning and culture

strictly—for example, as a system of

in animals have not run with the

Dr. Cecilia Heyes is a professor at University College London in England. Herresearch focuses on the evolution of cognition. She is a co-editor of Social Learning in Animals: The Roots of Culture (Academic Press, 1996J, and Evolution of Cognition (MIT Press,

inheritance that allows cumulative,

lead provided by mirror neurons.

2000J.

from their "demonstrators," and

thereby heartlessly proved me wrong. If culture is defined more

INTERVIEW WITH DR. CECILIA HEYES I 185

SUMMARY

1. Cultural transmission involves the transfer and acquisition ol information via social learning and leaching and may represent a powerful force for the acquisition and spread of behaviors both within and between generations of animals.

2. Cultural transmission differs Irom learning about other parts ol the environment. Unlike other environmental influences, what is learned

via cultural transmission is passed on Irom individual to individual. This can translate into the behavior ol a single individual shifting the behavior patterns seen in an entire group. Furthermore, when cultural transmission is in play, what is learned by one individual may he passed down through many generations. 3. Cultural transmission involves a "model" individual and an "observer" who

learns a specific behavior or response Irom the model. There are situations. however, that involve an interaction between observers and models, hut that

do not constitute cultural transmission because observers do not learn any particular behavior or response from models. Twoexamples of this are local enhancement and social facilitation.

4. Cultural transmission can occur through learning from other individuals via social learning (copying or imitation) and/or leaching. 5. To demonstrate imitation, there must he some new behavior learned from

others, and that behavior must involve some sortof new spatial (topographic) manipulation as well as lead to the achievement of some goal. Copying

differs Irom imitation in that what iscopied need not he no^el and need not involve learning some new topographical action. 6. Teaching, when rigorously defined, implies that one individual serves as an instructor and at least one other individual acts as a student who learns

from the teacher. Teaching entails providing an immediate benefit to the

student hut not to the teacher, instructing naive "students." and imparting some new information to students faster than they would otherwise receive it.

7. Cultural transmission may occur via vertical, horizontal, or oblique trans mission. Vertical cultural transmission involves the transfer of information

from parent to child, horizontal cultural transmission occurs when infor mation comes from peers, and oblique cultural transmission is the transfer of information from older to younger individuals, excluding transfers from parents to offspring.

8. Genetic and cultural transmission can operate independently onanimals, but oftentheyinteract ininteresting ways, asexhibited in the cultural transmission ot birdsong in finches and the evolution of male choice in guppies. 9. Dataon more than 100 species of nonhuman primates have shown that there is a significant positive correlation between brain size and both innovation and tool-use frequency. It appears that it is the absolute size of the primate brain, not brain size in relation to body size, that correlates best with social learning, tool use, and innovation. A similar trend between large brain size and an increased propensity toward innovation was found for birds in North America, Britain, and Australia.

186 I CHAPTER 5 I CULTU RAL TRANSMISSION

DISCUSSION QUESTIONS

1. Why do you suppose it took so long for ethologists to focus on the possibility that cultural transmission was an important force in animals? Can you imagine any biases—scientific, ideological, and so on—that might be responsible for this? 2. Suppose I run an experiment in which I take a bird (the observer) and let him view another bird (thedemonstrator) opening a sealed cup by pecking at a circle on the cover ol the cup. I then test the observer and see that he now opens the cup by pecking at the circle. What can I infer about social learning here? What other critical treatment is missing from this experiment?

3. Imagine that adults in some population of monkeys appeared to pick up new innovations (for example, potato washing, stone play) from observing others. How might you disentangle vertical, horizontal, and obliquecultural transmission as possible explanatory forces? 4. List the pros and cons of Hauser and Cams definition ol teaching. How might you modify this definition to address what you listed on the "con" side of your ledger? 5. Suppose that after extensive observations, you determine that certain animals in a population appear to rely on social learning much more often than other individuals, and that such differences are due to genetic variation. How might you use the truncation selection technique described in Chapter 2 to examine the narrow-sense heritahility of the tendency to employ social learning?

SUGGESTED READING

Bonner. J. T. (1980). The evolution of culture in animals. Princeton: Princeton University Press. One of the earliest books looking at culture from an evolutionary perspective. This is a fun read and informative as well.

Boyd, R., & Richerson P.J. (1985). Culture and the evolutionary process. Chicago: University of Chicago Press. Probably the best hook on the evolution of culture. This book can gel very technical, but it is worth the effort to work through it. Brass, M., & Heyes, C. (2005). Imitation: Is cognitive neuroscience solving the correspondence problem? Trends in Cognitive Sciences. 9, 489-495. An interesting paper on the role of neuroscience in explaining a long-standing "perspective-taking" problem in the study of imitation. I[eyes, C. M. (1994). Social learning in animals: Categories and mechanisms. Biological Reviews ofthe Cambridge Philosophical Society. 69, 207-231. Also Heyes C. M., & Ray E. D. (2000). What is the significance of imitation in animals? Advances in the Study oj Behavior, 29, 215-245. Two overviews on social learning and cultural transmission. Lefcbvre, L.. Reader, S. M., & Sol, D. (,2004). Brains, innovations and evolution

in birds and primates. Brain Behavior and Evolution. 63. 233-246. A nice review paper that compares published data on brain size, innovation, and cultural transmission in both primates and birds.

SUGGESTED READING

I 187

their relatives much more frequently than unrelated individuals. Being able to recognize kin has clear advantages, as ingesting kin would generally be selected against whenever alternative food sources were available. But as the costs and

benefits of eating kin change, we expect the tadpoles' behavior to change. And indeed, the researchers found that cannibalistic toads were much less picky when they had been starved lor twenty-four hours or more—that is, when they were very hungry, they woidd occasionally eat even genetic kin (Figure 8.29). MHC, KINSHIP, AND TEMPLATES. In Chapter 6, we learned that animals

sometimes use potential partners' Major Histocompatibility Complex (MHC) genes, which they identify by odor, to determine which mate to choose. Ml IC also plays a role in kin recognition (Frommen et ak, 2007; Manning et ak, 1992). Jo Manning and her colleagues examined this role in house mice (A/as musculus domesticus), a species in which females nest together and nurse all offspring at their nest (Manninget ak, 1992). When the female mice nest together, they all receive a benefit, which is protection from infanticidal males that sometimes attack and kill offspring that are not theirown (Manning etak, 1995). At the same time, communal nesting creates a situation in which females can be "cheated"— this occurs when other Females at their nest are protected Irom danger, but do not nurse all pups present. One way to minimize the cheater problem, and to maximize inclusive fitness benefits, would be for Females to Form communal

nests with their genetic relatives. And because Ml IC differences are correlated with differences in odor, one way that females may discriminate among kin and nonkin is through odors associated with the MFIC (Packer et ak, 1992). Manning and her colleagues worked with six wild populations ol house mice, individually marking each mouse and determining its Ml IC "haplolype"

(similar to a genotype). They observed pregnant females and examined whether females who had just given birth opted to nest alone or in a communal nest. Ninety percent of the females chose to nest communally. With respect to kin recognition, when females selected which communal nests to join, they chose

24 hours

48 hours

24 hours

ABC

Interval between meals

FIGURE 8.29. Hunger and carnivorous toads. The carnivorous

morph of spadefoot toads prefers to eat nonkin over kin. When starved for

24 hours (A), only a little more than 10 percent of individuals eaten were kin. If starved for 48 hours, this figure rises. As a control, toads were again starved for 24 hours (C), and results were similar to the original 24-hour deprivation treatment (A). The solid horizontal line represents the value expected if cannibalism were random with respect to kinship. (Based on Pfennig et at., 1993)

nests with individuals who had an Ml IC similar to their own. While this does

not definitively show that females use MFIC as a cue for kinship, it is consistent with such a hypothesis.

RULE-OF-THUMB MODELS OF KIN RECOGNITION

As we saw in the penguin studies discussed earlier, in species in which individuals do not raise their offspring in dense colonies, but instead live in discrete nests that are physically separated, a second, and in some sense simpler, form ol kin recognition may evolve. In such scenarios, natural selection might Favor a kin recognition ride of the form "if it lives in your nest/cave/territory, then treat it like kin" (Blaustein, 1983: Ilolmes and Sherman. 1983; Sherman and Holmes, 1985; Waldman, 1987).

Tosee how such a rule ofthumb might work, imagine a population ol animals in which family units live in a fixed area—let's call it a nest—that is set apart from other nests. In such a population, all of the machinery (cognitive, genetic, sensory) necessary to distinguish kin from nonkin may be superfluous. It may be that a rule that instructs individuals to treat all individuals in their nest as

kin works just as well in terms of kin recognition as the more complicated rules

associated with matching. After all, if everyone in a nest is almost always kin, KIN RECOGNITION

I 289

INTERVIEW WITH

Dr. Francis Ratnieks Why has so much work on animal behavior and kinship been done in the social insects? How did you decide to work with this group? Becoming a social insect biologist was literally plan B. On completing my BSc in Ecology at the University

discoveries have been made with the

I often tell students that Hamilton's

honeybee alone, which is only one of 20,000 social insect species. Social

inclusive fitness theory is as important to the field of evolution

insects have been very useful for testing Hamilton's theory because relatedness, the theory's central parameter, varies both within and

and behavior as Einstein's e=mc2 is to

physicists. Is that an overstatement? It is not an overstatement. Both

decided to study pest management.

are elegant and concise mathematical representations of a fundamental underlying relationship. Hamilton's

I felt this would be useful and would

Rule tells us the condition under which

combine my interests in insects and ecology. I applied to do a Ph.D. in the Department of Entomology at Cornell University as this seemed the best place for studying insects. The professor of apiculture, the late Roger Morse, offered me a studentship. Although studying honeybees was something I had never thought of, I accepted. I quickly became enthusiastic about honeybees and beekeeping. More gradually, I developed interests and ideas about

any behavior or trait that affects other individuals of the same species will

of Ulster in Northern Ireland, I

social evolution and behavior, and

taught myself how to model social evolution. I also expanded into wasps

between species because queens can be mated to one or more males,

and ants.

because there can be different

most important group of organisms for testing predictions arising from

numbers of queens per colony, and because haplodiploidy (in ants, bees, and wasps) causes relatedness to

William Hamilton's inclusive fitness

differ between the sexes. Insect

theory. It has been a two-way street. Social insects have played a key role in validating the theory, and

colonies are also very practical to study. Acolony of ants can be kept in a plastic box. A colony of honeybees can be kept in a hive. Honeybees are

Social insects have been the

the theory has revolutionized our understanding of social insects,

especially how eusociality evolved and the reproductive behavior of

by viewing the dancing bees through

insect societies.

Social insects can be used to

study practically any question. They are literally a gateway to biology. An immense number of important

290 I CHAPTER 8

easy to study once you know how. Some honeybee studies are even based on decoding waggle dances

I KINSHIP

the glass walls of an observation hive. This is the only case in animal behavior where the animals "talk to" the researchers.

be favored or disfavored by natural selection. Einstein's equation tells us the relationship between mass and energy. The relationship in Einstein's equation is inviolable. Technically speaking, Hamilton's Rule is not inviolable because gene frequencies, and therefore the traits they code for, can also be affected by genetic drift as well as by natural selection. Does that make Einstein's equation more important? I don't think so. It just reflects a difference between physics and biology. How is it that a simple mathematical rule can be so

important? The reason is simple. Many biological processes can be represented mathematically. For example, population growth can be represented by multiplication. The relatedness term in Hamilton's Rule

comes from the simple fact that each gene in an organism has a precise

probability of being passed on to an

offspring. The probability is usually 0.5, but can be 1, for example, from a haploid male bee to his daughter. Hamilton's Rule is also a good example of the importance of mathematics in biolog/. The

mathematics is not hard. High school algebra is enough to understand it. The hard part for the student is combining the mathematics with the biology. The best way is to jump in and have a go!

Kinship isn't the only factor that promotes social behavior and altruism in animals—is it?

Kinship is very important. Consider the evolution of eusociality. The problem is to explain altruismhow can natural selection select for

individuals to forego reproduction to help others? Eusociality evolved within families, with offspring helping their parents rear more brothers and sisters. Helpers are as closely related to the individuals reared (brothers and sisters) as to their own sons and daughters. (Although many queen bees, wasps, and ants mate to several males, which diminishes relatedness, this evolved after eusociality.) But if all that is needed for

eusociality to evolve is high relatedness, why is eusociality not more common? Two other things are

needed. First, a nest or some way of keeping the family together, so that help is directed to kin. Second, some way of helping, such as by providing food or by defending. Eusociality arose many times in the Hymenoptera because many species have nests to which the mother brings food for her offspring. Helpers can help simply by bringing more food. In termites food was not needed as the family was living inside its food—a log. Here, defense was the key. In many modern-day insect societies, worker altruism is also

caused by social pressure. Workers in most bee, wasp, and ant species have ovaries and can lay eggs. But in many such species, worker reproduction is rare. In the honeybee, fewer than o.i percent of the workers lay eggs.

Egg laying by workers is deterred by an effective policing system that kills worker-laid eggs. This means

that worker honeybees are better off working rather than laying eggs, given

that almost all their eggs will be killed if they lay any.

Do the terms "kinship" and "family" differ in meaning when discussed in ethology as opposed to when they are used by nonscientists in the course of normal conversation? How so?

I don't think there is much

difference. Sometimes people will refer to other individuals as a brother

or sister when they are not true relatives. But the people using these words probably know the difference. By referring to someone unrelated to you as brother or sister is often a way of showing that you have a common interest because you belong to the same group within society. The fact that we humans have what seems

like a keen natural understanding of kinship suggests that it is important to us and is a human universal. That is,

it is something innate in being human, rather than something that is purely cultural. Given the importance of relatedness in social behavior, this is

not surprising.

Can you envision a day when sociologists and animal behaviorists will be using a common framework for studying kinship and behavior? What might such a framework look like? A common interdisciplinary framework is something that is possible. However, even if this is established, the subjects and goals of the different disciplines may be sufficiently different that they may be using very different parts of a large and unwieldy framework. This is especially true when studying humans, given the vast number of disciplines involved, including history,

economics, anthropology, sociology, political science, criminology, psychology, and biology. What insights would a historian studying the Tudors take from evolutionary biology, for example? The value of a common framework

can be seen when some important insight from one discipline is ignored in another discipline. For example, studies by evolutionary biologists Martin Daly and Margo Wilson have shown that kinship may influence abuse of children by parents and stepparents. This idea, which comes

from Hamilton's theory (and is also part of common knowledge, given well-known stories like Cinderella), ran counter to the way that sociologists were trained. The question then is, why were sociologists not trained to consider this and are they now doing so?

The debate triggered by the publication of the book Sociobiology by E. 0. Wilson in 1975 is a good example of the friction that can be caused

when disciplines and ideologies collide. It is easy for more heat than light to be generated. The value of ideas or theories originating in one discipline and exported to another can be gauged by the new insights they give and the degree that they unify previously disparate fields when tested with real data. Interdisciplinary cross-pollination is not just one way, from biology to social science. The study of animal behavior has greatly benefited from insights from game theory, which was originally developed within the social sciences.

Dr. Francis Ratnieks is a professor at Sussex University, England. His seminal work on social behavior

has focused on the role ofgenetic relatedness in shaping insect societies.

INTERVIEW WITH DR. FRANCIS RATNIEKS

I 291

selection should favor the simplest possible kin recognition ride. ()l course, such kin recognition rules are subject to cheating. Cowbirds and cuckoo birds, for example, lay their eggs in the nests of other species, who then raise those chicks as il they were their own (Ortega, 1998; Figure 8.30). Such "nest parasites" are in an evolutionary arms race with their hosts—hosts are selected to detect and

reject loreign eggs, and nest parasites to circumvent any detection system that might evolve in their host (Dawkins and Krebs, 1979).

Spatial cues and kin recognition rules can often change through the

lifetime of an individual. For example, in bank swallows (Ifoparia riparid), parents initially feed any chick in their nest, thus adopting the ride •"if il is in my burrow, it is likely kin" (Hoogland and Sherman, 1976; see Figure 8.5). This

makes good sense, because for the first three weeks oflife chicks cannot fly, and il is therefore extremely likely that any chick in a burrow is kin. At three weeks,

however, chicks learn to fly and there is consequently much more mixing among young. Michael Beecher has found that when their chicks are about twenty FIGURE 8.30. Kin recognition breakdown. While adopting an "if it's in your nest, it is your offspring" rule often works for mothers, the system can

days old, bank swallow mothers switch from their rule of ihum i (Iced what is in your nest) to usingdistinctive vocal cues (that is, a template-based system) to recognize and feed their offspring(Beecher et ak, 1981a, 1981b, 1986).

mother dunnock is feeding a baby cuckoo

Thestudyofanimal behaviorwasrevolutionized by the introduction of inclusive fitness models. Since W. D. Hamilton introduced these models in the early 1960s,

that has been dumped into her nest. (Photo credit: Eric and David Hosking/

or anotherthought about whether kinship plays a role in the system that he or she

be sabotaged by "nest parasites." Here a

almost every animal behaviorist who has studied social behavior has at one time is studying. As we have seen, kinship theory not only allows researchers to make predictions about when animals should be cooperative and altruistic toward their kin, but it also makes predictions about when they should not be so (as in parentollspring conflict, siblingrivalry). Inclusive fitness continues to be one ol the most actively researched areas in ethology, with modern work employing molecular genetic and phylogenetic analyses to expand the Ironliers of research in this area.

Corbis)

SUMMARY

1. W. D. Hamilton's "inclusive fitness" or "kinship" theory has revolutionized the way that scientists understand evolution and ethology 2. In evolutionary terms, relatedness centers on the probability that individuals share genes that they have inherited Irom some common ancestor—parents,

grandparents, andsoon. The essence of inclusive Illness models is that they add on to '"classical" models of natural selection by considering the effect of a gene not onlyon the individual that bears il, but also on those sharing genes that are identical by descent (thai is, genetic kin). 3. The decision to aid family members is a function of how rek led individuals are, and how high or low the costs and benefits associated wilh the trait turn out lo be. When individuals are highly related and a gene codes for an action thai provides a huge benefit at a small cost, selection strongly lavors this trait.

4. Parents should be particularly willing lo go to great lengths to help their offspring. But a zone of parent-offspring conflict is also predicted under basic kinship theory. 5. While sibling rivalry is most often associated with the held of psychology, basic kinship theory also defines the conditions under which sibling rivalry should be favored, including competition lor lood. 292 I CHAPTER 8

I KINSHIP

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FIGURE 10.23. Brain size, innovation, andsurvival in birds. (A) The relationship between mean relative brain size and invasion potential (survival in a newenvironment) acrossavian families. (B) The relationship between mean foraging innovations and invasion potential across avian families. (From Sol et al., 2005a)

over time, it has become clear that animals are capable of other behaviors that we initially believed were uniquely human—for example, tool use—and so ani mal behaviorists have begun to test animals for their ability to plan for the future. Both animal and human behaviorists posit that two requirements must be met to demonstrate planningfor the future. First, the behavior must be novel, so that we can be certain that we are not seeing the manifestation of some innate

action. For example, migration behavior, which has many underlying innate components, may appear "planned," but would not be considered such under

ourdefinition. Second, the behavior in question must not be tied to the current motivational stale of the animal, but ratherto the anticipated motivational state at some point in the future (Shettleworth, 2007: Suddendorf, 2006). Mere, we

will examine a recent study of the ability of western scrub jays {Aphelocowa californica) to modify their foraging behavior in an attempt to plan for the future (Figure 10. 24).

Western scrub jays are a model system for such experiments, as they dis play incredible feats of episodic memory—recollecting specific events or episodes—in that they cache and later uncover large amounts of food. In ad dition, these birds not only remember where they have stored items, but they remember who was watching them when they cached their food and in such cases will later dig up and rehide the food, presumably to protect their stored lood from being stolen (Clayton and Dickinson, 1998; Dally et al., 2006). With such impressive cognitive abilities, the hypothesis that western scrub javs can also plan lor the future seems worth testing, especially considering that studies in humans suggest that the same neurobiological processes involved in episodic memory are involved in planning for the future (Atance and Melt/off, 2005; Okuda et al., 2003; Rosenbaum el al., 2005).

Caroline Raby and her team used a simple, but elegant, experimental procedure to examine whether western scrub jays could plan for the future (Raby et al., 2007). On alternate mornings over the course of six days, birds were exposed to one of two compartments—one compartment contained food

FIGURE 10.24. Western scrub jays and planning for the future. Researchers have examined whether western scrub

jays plan into the future when making foraging decisions. (Photo credit: David A. Northcott/Corbis)

LEARNING AND FORAGING I 359

in the form of ground-up pine nuts, and the other compartment contained no food. On the evening before each test, the birds were not fed any food, and they were therefore hungry during their exposure to test compartments. Alter the six days ofexposure to the two compartments, the birds were denied access toany food for two hours before dark, and then they were unexpectedly provided with

a bowl of whole pine nuts—that is, food that could be cached. They wore then allowed to move freely in the area with the whole pine nuts and could access both of the compartments they had been exposed to earlier. But now each ol the compartments had a "caching tray" added to it, so the birds could cache lood before it got dark, il they so chose.

Remarkably, Raby and her team found that jays cached more nuts in the compartment in which they had consistently received no food in the past, strongly suggesting that they were planning for the fact that, when next exposed to that compartment, there would be no food present unless they cached it there. In an ingenious follow-up experiment, Raby and hercolleagues had birds learn that they would be k'(.\ peanuts in one compartment, but dog kibble in the other (jays like both these food types). When an experiment like the one described above was run, jays cached peanuts in the compartment associated with kibble, and kibble in the compartment associated with peatiuts, suggesting they prefer a varied diet, and that they plan for such a diet accordingly. 'The extent that other animals can plan for the future remains a relatively unexplored question in ethology.

SOCIAL LEARNING AND FORAGING

In addition to learning per se, information about foraging can be culturally transmitted when individuals observe others to see how they find food and what thev eat (recall the work on loragingand cultural transmission in rats in Chapter 1). To understand more about such social learning, we will consider social

learning and foraging in pigeons. Like rats, pigeons (Columbia liv'ui) are an ideal

species in which to examine cultural transmission of feeding behavior (Figure 10.25). Being primarily scavengers feeding on human garbage, pigeons face the same dilemma faced by rats: Which new food items are safe, and which are

FIGURE 10.25. Urban foragers. Pigeons are scavengers, coming across novel food items all the time. Such a species is ideal for studying foraging and cultural transmission. (Photo credit: Blickwinkel/Alamy)

360 I CHAPTER 10 I FORAGING

FIGURE 10.26. Social learning and foraging in pigeons. Pigeons in this experiment need to learn to pierce

the red half of a paper covering a box of seeds. The graph shows average latency to eating for four groups: NM (no model) group—these birds were never exposed to a model; Bl ("blind" imitation) group—these birds observed a model

bird pierce a paper cover but never eat; LE

(local enhancement) group—these birds observed a model bird eat through a hole in the paper made by the experimenters; and OL(observational learning) group — these birds saw a model bird pierce 9

10

the paper and eat the seeds in the box. Pigeons in the NM and Bl treatments

never learned to feed in the experimental

dangerous? Louis Lelebvre and his colleagues Luc-Alain C.iraldeau and Boris

Palemeta have run an intriguing series ofexperiments that attest to the strength ol cultural transmission in shaping diet in the pigeon. This work has focused on three related issues: (1) What type ofinformation do pigeons transfer about food? (2) flow does such information spread or fail to spread through a population of

apparatus. The quickest learning occurred in the OL treatment. (Based on Palameta

and Lefebvre, 1985)

pigeons? (3) What lactors favor the cultural transmission of information over alternative means of acquiring information? Palemeta and Lelebvre set out to examine cultural transmission in a three-

part experiment that used observer and demonstrator animals (Palameta and

Lefebvre, 1985). The task that observer pigeons needed to master was piercing the red half of a half red/half black piece of paper covering a box. Under the paper was a bonanza of seeds for the lucky bird who made it that far. An observer pigeon was placed in an arena with such a food box—with a hall red/hall black paper cover—and exposed to one of four scenarios. In the first group, birds saw no model on the other side of a clear partition. None of lhe pigeons in this group learned how to get at the hidden food, suggesting that this was indeed a difficult task to master through individual learning. In a second group, observers were shown a model that was eating from a hole in the paper. The hole was made by Palameta and Lefebvre, and as such, although observers did see a model eating, they did not see the model solve the hidden lood "puzzle"—that is. they did not see the model pierce the red half of the cover. Once again, pigeons in this treatment failed to learn how to get food from the multicolored box. In the final two treatments of the experiment, birds either saw a model pierce the red side of the paper but get no food, or they saw a model bothpierce the paperand eat. Although birds in both ofthese treatments learned to solve the food-finding dilemma, those in the latter treatment did so much laster (figure 10.26), suggesting an important role for cultural transmission in the loraging behavior of pigeons.

Ihere is an interesting twist to the pigeon story. In many animals that live in groups, there are two strategies for foraging that individuals can adopt: produeingand scrounging. Producers find and procure food, while scroungers make their living parasitizing the food that producers have uncovered (Barnard. 1984; Giraldeau and Caraco, 2000). Layered onto the social learning and loraging story we have seen in pigeons, we find producers and scroungers in LEARNING AND FORAGING I 361

this species as well (Giraldeau and Lefebvre, 1986). And it is the unusual way that producing and scrounging interacts with social learning that makes the pigeon story particularly useful in furthering our understanc ing of cultural transmission and foraging.

Despite Palameta and Lefebvre's work demonstrating social learning in

pigeons in cages, when birds are tested in groups, only a few birds seem to learn new feeding behaviors by observing others. This apparent paradox caused Giraldeau and Lefebvre to examine whether scrounging behavior somehow inhibited cultural transmission (Giraldeau and Lefebvre, 1987). To do so, they

used a different set-up than the one described above (Figure 10.27). In the new experimental protocol, (locks of pigeons were allowed to feed together. Forty-eight little test tubes were placed in a row and live ol these tubes had food. Which five had food was unknown to the birds. To :>pen a tube, an

individual had to learn to peck at a stick in a rubber stopper at the top ol the tube. When this taskwasdonecorrectly, it caused the test tube to open md the contents

to spread over the floor below. Once the food was out, any bird in the vicinity, not just the one that opened the tube, could eat it. The results of this experiment were striking. As predicted based on earlier

work, only two of the sixteen pigeons in their group learned to open tubes— that is, the flock was composed of two producers and fourteen scroungers. Two additional findings suggested to Giraldeau and Lefebvre thai scrounging inhibited an individual from learning how to open tubes via observation. To

begin with, scroungers followed producers and seemed moo interested in where producers were, than in what producers did, to get food the scroungers' attention was not directed at the actions taken by the producers to open the

lubes. Second, by removing the two producers from the group. Giraldeau and

**•*.

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FIGURE 10.27. Producing and scrounging. When a group membei finally opens a tube with food in it, the food spills on the floor and is accessible to all. In Giraldeau and Lefebvre's study using such a scenario, out of sixteen pigeons, only two laarned to open tubes (these were the producers), while fourteen acted as scroungers. Labels show where millet was hidden, but the birds were not privy to this information. 362 I CHAPTER 10 I FORAGING

TABLE 14.3. Penultimate and ultimate contests. Hsu and Wolf examined many combinations of winner and loser effects on contest outcomes through time.WW = win at time T-l, win at Time T; LL = loss at time T-l, loss at time T; WL = winat time

T-l, lossat time T; NN = "neutral," no loss,nowin. Outcomes of(1) and (2) directly measured the effects of penultimate winner and loser experiences. Outcomesof

(3) measured the importance of penultimate versusultimate experience onthe probability of winning. Outcomes of (4) showed the difference between LL-WL and LN-WL, measuring immediate loser effects. Outcomesof (5) showed the difference

between LW-WL and LN-WL, measuring immediate winner effects. Finally, outcomes at (6) showed the difference between WW-LW and NN-LW, measuring the effectsof penultimate andultimate winning experiences. (From Hsu and Wolf, 1999) (6) —

r-OOpponent 1

WW

LL

LW

LN

NN

Opponent 2

LW

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WL

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LW

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power! liI as the outcome of the interaction immediately preceding the interaction underway. In addition, unlike many other species, Rivulns marmoratus showed no asymmetry in winner and loser effects—that is, the loser effect was not stronger than the winner effect, nor vice versa. WINNER AND LOSER EFFECTS IN COPPERHEAD SNAKES. Cordon Schuett

has examined both the behavioral dynamics and endocrinological correlates of winner and loser effects in copperhead snakes (Agkistrodon contortrix) (Schuett. 1997; Schuett and Gillingham, 1989). Because male-male aggression has a significant impact on mating success, Schuett examined whether winner and loser effects had an impact on aggression and mating success. The experimental protocol involved a trial arena that housed a female in the center and one male at each end. Schuett used males that had had no aggressive interactions lor six to twelve months prior to his study, and he pitted two males that differed in size byapproximately 10 percent. In all thirty-two trials, the larger male emerged as dominant and gained reproductive access to the female. Ten winners and ten losers from the "size" contests described above were

chosen, and each was matched against a same-sized male copperhead that had no prior experience. Schuett lound that prior winners were not more likely to win again, nor were they more likely to win than their opponents who had no experience to obtain access to a female. That is, no winner effects were uncovered in copperhead males. A loser effect, however, was uncovered—losers were more likely to lose again and to cede access to reproductivcly active Females to other males. In an interesting twist, Schuett then examined how individuals who had now lost twice (in the initial "size contests and then in loser effect treatments)

Iared against opponents who had no experience and who were about 10 percent smaller. Would the loser el led outweigh the positive size advantage that the

WINNER, LOSER, BYSTANDER, AND AUDIENCE EFFECTS I 475

FIGURE 14.14. Winner and loser

snakes. In copperhead snakes, losses can have a significant effect on future contest outcome. Snake fights in

Agkistrodon contortrix include such aggressive behaviors as: (1) ascend, (2) ventrad-to-ventrad sway, (3) lateradto-laterad sway, (4) ventrad-to-dorsad sway, (5) hook, and (6) stiffen. (Based on Schuettand Gillingham, 1989, p. 248) ,r,., ..*'

losers possessed, or vice versa? Results were crystal clear and pointed to the strength of the loser effect in copperheads—two-time losers lost all contests with smaller opponents (Figure 14.14). Besides the behavioral work, Schuett and his colleagues also studied endo crinology and aggression in copperheads by examining hormonal correlates to the loser effect (Schuett et al., 1996; Schuett and Grober, 2000). Researchers

allowed pairs of males to light when a lemale was present. The snakes were kept together until one male was judged dominant to the other, at which point the individuals were separated and a blood sample was collected for hormonal analysis. In addition to this treatment, two controls were run; in the first, a lone male in his home cage was used, while in the second, a single male and a female were placed in the arena. The researchers took radioimmunoassays of plasma corticosterone in winners, losers, and both classes of control males, and they found that plasma corticosterone was significantly greater in losers than in winners or controls (Figure 14.15). Increased levels ol corticosterone produced dramatic effects in terms of both fighting and courting behavior in male copperheads. Not onlydo males who lose fights, and consequently have raised corticosterone levels, act subordinate, and rarely, if ever, challenge other males, they almost never court any females that are in the vicinity of where they fought.

90

80 70 60 50

40 30 20

10

Winners

Losers

Controls

FIGURE 14.15. Hormones,winning, and losing. Losers show increased levels of plasma corticosterone compared to controls. No such change was found in winners. (Based on Schuett et al., 1996)

476 I CHAPTER 14 I AGGRESSION

Experimental work in a number of other species suggests that the stressrelated hormones, such as glucocorticoids, often inhibit learning and/or memory (de Kloel et al.,1999, 2002; de Quervain, 2006; de Quervain el al., 1998, 2000; Lemaire el al., 2000; Sapolskyet al., 2000). Whether winners and losers differ in their ability to learn as a function of hormonal changes that occur as a result ol fights is a fascinating, but unexplored question.

MATHEMATICAL MODELS OF WINNER AND LOSER EFFECTS. In addition to

empirical work on winner and loser effects, there are a number of mathematical

models that examine the implications of winner and losereffects on the forma tion of animal hierarchies (Beacham, 2003; Bonabeau et al., 1996, 1999; Dugatkin, 1997b; Landau, 1951a, 1951b; Mesterton-Gibbons, 1999). You should recall from the beginning of the chapter that a dominance

hierarchy is usually defined as a rank ordering of individuals in a group based on their aggressive interactions with each other. For example, if individual A wins the majority of fights with B, C, and D, thenA is the top-ranked (or alpha) individual in a hierarchy. If B beats C and D, C beats D, and D beats no one, then a linear hierarchy exists (A > B > C > D) and that hierarchy is said to be transitive, in that if A defeats B and B defeats C, then A defeats C as well.

Part ofthe interest in hierarchy formation nodoubt arises from the difficulty in understanding why an animal would ever "accept" a role other than that of alpha individual in a group (Allee, 1951; Dugatkin, 1995; Reeve and Ratnieks, 1993; Vehrencamp, 1983). Initial work on the impactof winnerand loser effects on hierarchy formation was undertaken by H. G. Landau over fifty years ago (Landau, 1951a, 1951b). Landau was troubled that when he modeled hierarchy formation mathematically, he found that the linear, transitive hierarchies often found in nature did not seem to emerge from his mathematical work—work in which he only considered inherent differences in fighting abilities across individuals. So Landau added winner and loser effects to his models to examine

if linear, transitive hierarchies then emerged. And such hierarchies did emerge from Landau's more complex models. Despite the importance and impact of Landau's papers on research in the area of dominance hierarchies, a number of critical questions surrounding winner and loser effects and how they interact remained unanswered more than forty years after the original papers were published. In particular, Landau did not examine winner and losereffects independently, but he only considered the effect on hierarchy formation when both were present. Furthermore, Landau did not take into consideration the fact that animals assess each other's fighting ability, technically referred to as resource holding power (RHP). Is it possible that when RHP is assessed, winner effects can have different implications for hierarchy formation than losereffects? To address these questions, Dugatkin developed a simple computer sim ulation that independently examinedwinner and loser effects when individuals assessed eachother's fighting abilities and could choose to fight orflee (Dugatkin, 1997b). The most salient result of these models is that the type of hierarchy predicted depends critically on whether winner effects exist alone, loser effects exist alone, or some combination of these forces are acting in a system.

Winner effects alone produce hierarchies in which the rank of individuals all the way from top rank (a) to bottom rank can be unambiguously assigned. Loser effects alone produce hierarchies in which a cleara individual exists, but the relationship among other group members remains murky. The difference between the hierarchies generated by the winnereffect and by the loser effect appears to be that winnereffectscreate a situation in which pairsof individuals primarily interact by fighting, which makes assigning position in the hierarchy fairly straightforward. Conversely, loser effects quickly produce individuals that are notgoing to be aggressive becauseof their low estimate oftheir own fighting ability after a few losses. Hence, with losereffects, most interactions willend in

WINNER, LOSER, BYSTANDER, AND AUDIENCE EFFECTS I 477

TABLE 14.4. Winning, losing, and hierarchy formation. When winnereffects alone are at play (green box), a clear linear hierarchy exists, with the position ofeach individual clearly delineated. When losereffects alone are at play(orange box), onlythe alpha individual is clear. Losereffects tend to outweigh winner effects (red box). (Based on Dugatkin, 19970, p. 585) Winner Effect

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neither individual opting to fight, making it difficult to assign relative ranks to most individuals in a hierarchy (Table 14.4).

BYSTANDER EFFECTS

When the observer of an aggressive interaction between two other individuals changes its assessment ol the fighting abilities of those it has observed, the

bystander effect—sometimes called the"eavesdropper effect"—is inoperation. Through observing, bystanders learn beforehand something about the oppo nents they may face one day in the future (Coultier et al., 1996; Johnsson and Akerman, 1998; Oliveira et al., 1998). Verbal models and computer simulations have found that bystander effects can have important consequences on hierarchy formation (Chase, 1974, 1982, 1985; Dugatkin, 2001b). Experimental work has found bystander effects in birds, mammals, and fish (McGregor, 2005). Bystander effects have been examined in the green swordtail fish (Xiphophorus helleri), a species in which males establish linjar dominance hierarchies where rank-order fights and/orattack-retreat sequences are common

(Beaugrand and Zayan, 1985; Franck et al., 1998). In these experiments, eavesdroppers first observe aggressive interactions and extract information from watching those who are fighting. The eavesdroppers are then tested in later aggressive interactions with those they had previously observed. 478 I CHAPTER 14 I AGGRESSION

To experimentally examine the bystander effect, Earley and Dugatkin had eavesdroppers on one side of an experimental lank and a pairof swordtails who were involved in aggressive interactions on the other side. In one treatment, the

eavesdropper could observe the pair of fish through a one-way mirror (mirror treatment) in which he could see the fish who were fighting but they could not see him and so would not be affected by the eavesdropper's presence. In the

other treatment, the eavesdropper could not see the pair because of an opaque partition placed into the tank (opaque treatment) (Earley and Dugatkin. 2002, 2005). After this observation period, the eavesdropper was pitted against either the winner of the observed fight or the loser of the observed fight. The opaque partition treatment served as a control for winner and loser

effects. Since the eavesdropper could not observe the interaction between pairs of individuals in the opaque partition treatment, the dynamics of the subsequent interaction between the eavesdropper and the winner, or between the eavesdropper and the loser, were the result of winner and loser effects, respectively. In contrast, both bystander effects and winner and loser effects could affect contests between the eavesdropper and winners and losers in the one-way mirror treatment. This means that when we compare the dynamics of

contests involving eavesdroppers in the opaque treatment (where there are only winner and loser effects) and the one-way mirror treatment (where there are winner, loser, and bystander eflects), we are able to experimentally determine the contribution of bystander effects. Eavesdroppers that observed a contest in the one-way mirror treatment were much more likely to try and avoid the winner of that contest than were fish in the opaque treatment (Figure 14.16). That is, eavesdropping per se affected future interactions with winners. In addition, eavesdroppers avoided observed winners regardless ol how badly they had defeated their prior opponent. The results were quite different when eavesdroppers interacted with losers. In general, eavesdroppers responded in a similar way to all losers, regardless of whether they had witnessed the losers' defeat. But if we break down the data on losers by how badly they lost fights, there is one piece of evidence that suggests

that eavesdroppers deal differently with losers because theyhave observed them lose. Results indicate that in the one-way mirror treatment (observed contests), eavesdroppers were less likely to initiate aggressive behavior and win against (1) losers that had persisted in their fights, or (2) losers that had escalated their aggressive actions, than thev were to initiate agression against losers that had

FIGURE 14.16 Eavesdroppers, winners, and losers. Eavesdroppers could either observe aggressive interactions between a pair of other fish (one-way mirror treatment; green bars) or such interactions were blocked

from view by an opaque partition

(opaque treatment; orange bars). When eavesdroppers were then paired against

winners of the previous contests, those who had observed the previous contests • 0.8

Mirror treatment

were less likely to (A) initiate interactions, and (B) escalate aggressive interactions.

• Opaque treatment

Those who were paired with the losers a

o.6

of the previous contest were more likely

0.4

S- 0.2

Loser

Winner

1

..1 Loser

to initiate aggressive contests, whether

or not they had been able to observe the previous contests, and less likely to escalate contests. That is, the difference

between orange and green bars for losers was not statistically significant. (Based on Earley and Dugatkin, 2005, p. 90)

Winner

WINNER, LOSER, BYSTANDER, AND AUDIENCE EFFECTS I 479

INTERVIEW WITH

Dr. Karen Hollis As a psychologist, what drew you to the study of animal aggression? I first became interested in

aggression as a graduate student working with Betta splendens, a territorial freshwater fish native to

Southeast Asia. Although my project addressed a question of underlying learning processes, not aggression per se, it afforded me a serendipitous observation of aggressive behavior, one that provided the raw material for years of subsequent research. My project required me to transport

years later, as a postdoctoral student at Oxford, I had the opportunity to conduct those experiments with blue gouramis, Trichogaster trichopterus, and, as the data showed pretty convincingly, the best defense is,

indeed, a good offense.

each Betta male in its home tank to another room where it would have

the opportunity to display to a rival. After a few days of this procedure, I noticed that when I approached the shelf on which the males were located

and reached for a particular male's tank, it became quite agitated. After a few more days, each male that I selected began to display—at me. And at eye level that display looked quite ferocious! I recognized that some features of my appearance obviously had become a learned cue for the subsequent interaction with a territorial rival. At that time,

food sites.

Aggression also appears in another mating strategy, called harem defense, in which a few males defend a group of females directly,

What do animals usually fight over? Do they display different types of aggression depending upon what the fight is about? No matter what the situation —

associative learning in B. splendens was pretty well established (even if the experimenter-as-signal was a little

from nest-mate aggression and sibling rivalry to parent-offspring conflict and territorial behavior—aggression

unconventional). However, what was even more interesting to me was the realization that this kind of learning could be a wonderfully adaptive

is all about resources. Moreover, as behavioral ecologists have demonstrated quite convincingly

mechanism, providing a territory owner with a definitive competitive edge: Confronting a potential usurper with a full-blown aggressive display could be a very effective aggressive strategy for a territory owner. A few

480 I CHAPTER 14

I AGGRESSION

males, defend a resource that is in

short supply, critical for females, and defendable, both in terms of the reliability of its location and its quality. That resource—and, thus, what males fight over—could be anything that meets these criteria. Many species of freshwater fish, including my own study species, blue gouramis, defend a location where aspects of the habitat, such as the temperature and pH of the water, are favorable for the development of eggs and fry. Territoria. lizards defend spots safe from predators. Some birds defend shady spots, necessary for the development of eggs. And, of course, many animals, from territorial male bumblebees and green frogs to sunbirds and burrowing owls, defend

across a variety of taxa, particular forms of aggressive behavior emerge under particular selection pressures. For example, aggressive behavior in the context of resource-defense

polygyny is a mating strategy in which individuals of one sex, typically

rather than a needed resource. Harem

defense polygyny is characteristic of grizzly bears, red deer, and elephant seals. Because the benefits of winning are tied more directly to reproductive success whenever males are defending access to reproductively active females than when they are defending only the resources to which females are drawn, and because only a few males, namely those powerful enough to mount this kind of defense, are able to reproduce, the aggressive behavior differs enormously. Males are much more aggressive, and injuries are potentially more lethal, wherever harems are concerned.

So, yes, aggressive benavior differs