Born This Way? Gender-Based Toy Preferences in Primates

Last week, British parents who had hidden their child’s gender from the world finally revealed that their five year old, now ready to enter school, is a boy. While the parents had hoped to raise their son Sasha in a gender-neutral way (“Stereotypes seem fundamentally stupid. Why would you want to slot people into boxes?”), their approach raised eyebrows and controversy. Were they creating an environment where their child could find his own gender identity, free from crippling societal expectations, or were they conducting a bizarre and possibly harmful experiment on a family member?

Putting aside the issue of whether the parents acted appropriately, the story raises fascinating questions about gender-specific traits and preferences. To what degree are gender differences innate and biological, and to what extent do they arise out of societal modeling and environment?

Some (including Sasha’s parents) may see gender preferences as being primarily influenced by human social pressures, but there are indications of biological influences as well. For example, girls with a particular genetic condition that exposes them to high prenatal levels of androgen often show “masculine” toy preferences, even when their parents strongly encourage them to play with female-typical toys. Given the intertwining impacts of nature and nurture in human societies, can we learn anything from our animal relatives who grow up free from human societal norms?

In this post, I’d like to take a look at two recent studies that examine differing male and female toy preferences in primates.

Male Monkeys Prefer Trucks

First, in 2009 a research team led by Janice Hassett of the Yerkes National Primate Center at Emory University reported on experiments in which they the researchers to see whether rhesus monkeys (Macaca mulatta) would exhibit gender-specific toy preferences similar to those of human children.

In humans, studies have shown that boys gravitate strongly to stereotypically “masculine” toys such as trucks and other vehicles, while girls are less rigid, spending relatively equal amounts of time playing with boy-favored toys and with more traditionally “feminine” toys such as dolls. One hypothesis put forward to explain this difference has been that boys face greater societal discouragement when they play with “girl toys” than girls do in the reverse situation. The researchers figured that by looking at rhesus monkeys, who don’t face comparable social pressures to conform to gender roles, they might be able to illuminate biological influences on toy selection as well.

Of course I'm not playing; you gave me a Raggedy-Ann. Pass me that truck. Now. (photo credit: J.M.Garg, Wikipedia)

In their study, the researchers compared how 34 rhesus monkeys living in a single troop interacted with human toys categorized as either masculine or feminine. The “masculine” set consisted of wheeled toys preferred by human boys (e.g., a wagon, a truck, a car, and a construction vehicle); the “feminine” set was comprised of plush toys comparable to stuffed animals and dolls (e.g., a Raggedy-Ann™ doll, a koala bear hand puppet, an armadillo, a teddy bear, and a turtle). Individual monkeys were released into an outdoor area containing one wheeled toy and one plush toy, with the researchers taping all interactions using separate cameras for each toy, identifying all specific behaviors, and statistically analyzing the results.

The results closely paralleled those found in human children. As with human boys, male rhesus monkeys clearly preferred wheeled toys over plush toys, interacting significantly more frequently and for long durations with the wheeled toys. Also mirroring human behavior, female rhesus monkeys were less specialized, playing with both plush and wheeled toys and not exhibiting significant preferences for one type over the other. Here’s a chart illustrating the similar gender preferences of humans and rhesus monkeys (the information regarding human preferences comes from a 1992 study by Sheri Berenbaum and Melissa Hines):

The researchers noted that these similarities show that distinct male and female toy preferences can arise in the absence of socialization pressures and hypothesized that “there are hormonally organized preferences for specific activities that shape preference for toys that facilitate these activities.”

Barbie Really Is a Stick Figure

Next, in a brief paper published in 2010, Sonya Kahlenberg of Bates College and Richard Wrangham of Harvard University presented the first evidence of wild male and female primates, chimpanzees (Pan troglodytes) in the Kanyawara chimpanzee community of Kibale National Park, Uganda, interacting differently with play objects.

Over a 14 year period, Kahlenberg and Wrangham observed that juvenile Kanyawara chimpanzees tended to carry sticks in a manner suggestive of rudimentary doll play and that the behavior was more common in females than in males. Juvenile chimps, particularly females, would carry around small sticks for hours at time while they engaged in other daily activities such as eating, climbing, sleeping, resting and walking. While the same chimps used sticks as tools for specific purposes, the researchers were unable to discern any practical reason for the stick-carrying. The following chart shows the degree to which female chimps were more likely to engage the in stick carrying behavior:

Age and sex differences in the rate of stick-carrying in chimpanzees. Females: circles, solid line. Males: triangles, dashed line.

The researchers hypothesized that “sex differences in stick-carrying are related to a greater female interest in infant care, with stick-carrying being a form of play-mothering (i.e. carrying sticks like mother chimpanzees carrying infants).” In support of this proposition, they pointed to several factors. First, they never observed stick carrying by any female who had already given birth; that is, stick-carrying ceased with motherhood. Also, the chimps regularly carried sticks into day nests where they “were sometimes seen to play casually with the stick in a manner that evoked maternal play.” Finally, nurturing behavior towards objects like sticks had previously been reported in captive chimps and documented on a couple of occasions in the wild.

Also, the researchers suggested a social rather than biological basis for the behavior. Because regular stick-carrying hasn’t been reported in other wild chimpanzee communities, they proposed that that young Kanyawara chimpanzees may be learning the behavior from each other as a way of practicing for adult roles – a form of social tradition passed between juveniles previously described only in humans. Kahlenberg and Wrangham conclude by noting that:

Our findings suggest that a similar sex difference could have occurred in the human and pre-human lineage at least since our common ancestry with chimpanzees, well before direct socialization became an important influence.

So there you have it. One rhesus monkey study positing a biological and hormonal basis for gender-specific play, and another chimpanzee study emphasizing social learning… At least for now, the threads of nature and nurture impacting gender roles seem difficult to disentangle for non-humans, just as they are for us.

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ResearchBlogging.orgHassett, J., Siebert, E., & Wallen, K. (2008). Sex differences in rhesus monkey toy preferences parallel those of children Hormones and Behavior, 54 (3), 359-364 DOI: 10.1016/j.yhbeh.2008.03.008.

Berenbaum, S., & Hines, M. (1992). EARLY ANDROGENS ARE RELATED TO CHILDHOOD SEX-TYPED TOY PREFERENCES Psychological Science, 3 (3), 203-206 DOI: 10.1111/j.1467-9280.1992.tb00028.x.

Kahlenberg, S., & Wrangham, R. (2010). Sex differences in chimpanzees’ use of sticks as play objects resemble those of children Current Biology, 20 (24) DOI: 10.1016/j.cub.2010.11.024.

Show Me the Honey! Honeyguides and Humans Team Up at Dinnertime

Humans have a long history of spotting superior abilities in other animals, and then training those animals to use those abilities to advance our own interests. Everyone’s familiar with how we’ve trained pigs to sniff out truffles for us with their sensitive snouts and how we’ve domesticated dogs to herd our livestock, alert us to intruders, guide us when our vision fails, and perform other services. Similar but less well-known examples include our training bees to detect the odor of explosives, cormorants to catch fish for us, and llamas to guard our sheep from coyotes and other predators.

It’s far less common, though, to find relationships where non-humans participate on a more equal footing, where they appear to train us at least as much as we train them. (People who are owned by cats should feel free to rebut this statement in the comment section below.)

Today’s post features one such relationship, the partnership between humans and the greater honeyguide (Indicator indicator), a bird that lives in the trees of sub-Saharan Africa.

Honeyguides and humans have very complementary appetites. Honeyguides get most of their food from beehives, feasting on larvae and wax that they extract from honeycombs (yes, they actually eat and can digest the wax!). Of course humans, too, seek out beehives, although our interest lies more in the bees’ sweet honey, and we’re generally more than happy to leave the wax and grubs for others to enjoy.

The bee-related skills of humans and honeyguides are relatively complementary as well. Honeyguides can fly swiftly across large areas and are expert at locating bee colonies, but have difficulty in extricating the combs on their own. Humans move more slowly along the ground and aren’t so adept at finding colonies, but once we have one in our sights, we’re able to overcome bee defenses and dig the combs out, even when the bees have nested deep within rock crevices and other hard-to-reach locations.

Out of this opportunity for mutualistic benefit, honeyguides and humans have worked out an elaborate interspecies communication system that allows them to work in tandem with certain signals understood by both parties.  This partnership has been formally documented in a three year field study conducted in the dry bush country of northern Kenya, focusing on the interactions between honeyguides and the nomadic Boran people who populate the area.

I’m the *real* Greater Honeyguide – don’t let imposters lead you astray! Visit me at http://safari-ecology.blogspot.com/ and see first comment below.

Each partner knows how to get the other’s attention. To attract the birds, the Borans call them with a penetrating whistle (known in the Boran language as Fuulido) that can be heard over a distances of greater than a kilometer and that is made by blowing air into clasped fists, modified snail shells, or hollowed-out palm nuts. Comparably, hungry honeyguides flag down humans by flying up close, moving restlessly from perch to perch, and emitting a double-noted, persistent “tirr-tirr-tirr-tirr” call. (Side note: I’ve been practicing this at home, and it doesn’t seem to attract much other than odd stares and raised eyebrows.)

The joint food expedition commences when the honeyguide flies briefly out of sight and then returns to a nearby, conspicuously visible perch. When the human companion approaches this perch, the honeyguide takes off, displaying its white outer tail feathers, and flies to a new resting place a short distance away, calling loudly when it lands. The Boran partner then approaches the new perch and the bird flies off again, repeating the pattern. As the Borans work with the bird, they whistle and shout to keep the bird interested in guiding. (Again, this doesn’t seem to work too well at home.)

The researchers found that the honeyguides signal the path and distance to the bee colony in a variety of ways. First, they indicate the correct direction through their flight paths, traveling consistently in the direction of the nest and increasing their precision as they near the target. It appears that the know in advance where the nests are located, as the researchers observed the honeyguides briefly visiting nests before dawn, peering into the entrances while it was still dark and the bees were docile.

Also, the honeyguides vary their behavior depending on distance to the hive. For example, when the hive is relatively distant, the birds begin the process with a relatively long disappearance during their first flight; conversely, their first disappearance is briefer when the hive is relatively nearby. Further, the honeyguides stop more frequently and the legs between perches become shorter as they and their human followers approach the nest, especially during the last 200 meters. Finally, the honeyguides select increasingly lower perches as they close in on the colony.

Upon arrival at the destination, the honeyguides perch close to the nest and emits an “indication call.” The researchers describe the scene as follows:

This call differs from the previous guiding call in that it has a softer tone, with longer intervals between successive notes. There is also a diminished response, if any at all, to whistling and shouting by humans. After a few indication calls, the bird remains silent. When approached by the searching gatherer, it flies to another perch close by, sometimes after circling around the nest. The resulting flight path finally reveals the location of the colony to the gatherer. If the honey collector does not (or pretends not to) detect the nest, the bird gives up after a while. It may then leave the area either silently or start a guiding session to another colony. In the latter case, it switches from the indication call to the guiding call and resumes a fairly direct flight pattern. Once the human team members find the nest, it becomes their turn to go to work and hold up their part of the bargain. After using smoky fires to reduce the bees’ aggression, the Boran honey gatherers use tools or their hands to remove the honey comb, and then break off pieces to be shared with their honeyguide partners.

To sum things up, here’s a great BBC video (featuring David Attenborough!) that describes the bird-human partnership and shows the honeyguides in action:

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ResearchBlogging.org
Isack, H., & Reyer, H. (1989). Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic Relationship Science, 243 (4896), 1343-1346 DOI: 10.1126/science.243.4896.1343.

Contagious Yawning Spreads to Birds

Apparently, parrots aren’t just smart, they’re competitive too. A couple of months ago, we covered recent research findings on contagious yawning in animals, reporting on the rarity of the phenomenon and its potential role as a form of social mimicry or even an indication of empathy. While certain primates clearly do yawn contagiously and dogs may yawn contagiously, the behavior hadn’t been reported in other animals and had been expressly ruled out in red-footed tortoises (although the tortoises may have had the last laugh, as they won the celebrated Ig Nobel Prize for their non-yawns).

Word of our mammal-centric coverage seems to have reached the small, oval ears of the always-influential parrot lobby, though, as just last week the journal Behavioural Processes published a study describing social yawning in budgerigars (Melopsittacus undulatus), the small Australian parrot often referred to as the parakeet. This study provides the first support for contagious yawning in a non-mammal, and even ups the ante by documenting what may be the first instance of contagious stretching, another stereotyped behavior that may play a social role for certain animals. Some may say that the paper’s timing is an utter coincidence and that only someone with delusions of grandeur would believe that it was even remotely linked to the AnimalWise post. We, speaking in our usual royal manner, prefer to think otherwise.

Fascinating, simply fascinating...

Michael Miller, Andrew Gallup and other researchers from the University of the Binghamton conducted an observational study of yawning and stretching in a group of approximately 20 adult male and female budgerigars living together in an aviary as an established flock. Over a period of about a year and a half, the research team video recorded the flock on 23 separate occasions. The recording sessions, each of which lasted 90 minutes, were conducted at varying times of the day, and the researchers took a number of precautions (such as ignoring the first 15 minutes of each tape) to ensure that the flock’s behavior was as natural and undisturbed as possible. Trained reviewers then systematically reviewed all of the tapes, recording the time and occurrence of each yawn and stretch, and categorizing each stretch by whether the bird extended one or both legs.

The researchers’ hypothesis was that, if yawning and stretching were spreading contagiously among the birds, the behaviors would occur in nonrandom “clumps” – that is, rather than being evenly dispersed throughout the recording sessions, multiple yawns (or multiple stretches of the same type) would take place in closely-spaced bouts and then be followed by a long interval until a new priming behavior triggered another bout. Further, they predicted that, although there might be might be overall tendencies tied to particular times of the day (for example, the budgerigars might, on average, yawn more frequently during evening sessions), if the yawning and stretching really were being triggered contagiously, then specific clumping patterns would not repeat themselves when multiple same-time-of-day sessions were compared.

To test their hypotheses, the researchers performed detailed, session-by-session analyses of each type of behavior. For example, they tallied how frequently each behavior occurred, measured the time between adjacent stretches and yawns, and sorted the adjacent pairs into different “bins” depending on the length of the interval. They also analyzed each session for clumping by breaking it down into a large number of short (20 to 30 second) intervals, which allowed them to identify “runs” of consecutive intervals that either did, or did not, contain the behavior in question. Finally, they statistically analyzed their data in a variety of ways to identify patterns and associations.

And the results?

Both yawning and stretching behaviors were indeed clustered within trials, and the period between adjacent yawns and stretches was “strongly biased toward very short (< 20 sec) and very long (> 300 sec) intervals,” especially for the yawns. Also, as hypothesized, despite the clustering for both behaviors, “neither behavior routinely occurred at specific times from the start of a session across multiple recordings at the same time of day. This suggests that the clumping of these behaviors was due to social influences, and not to underlying physiological effects as a result of similar circadian patterns.”

The research team summarized its findings and suggested directions for future investigation as follows:

The observational results presented here suggest that yawning and stretching are at least mildly contagious in budgerigars under semi-natural flock-living conditions. In line with each behavior’s presumed physiological function, contagious yawning and stretching may ultimately coordinate mental state and a group’s collective movements, but future research needs to test these predictions.

So, kudos to the budgerigars! Parrots everywhere can take pride in these findings, which point to previously-unknown areas of avian social signaling and coordination, and which may open up new avenues for studying collective behavior.

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ResearchBlogging.orgMiller, M., Gallup, A., Vogel, A., Vicario, S., & Clark, A. (2011). Evidence for contagious behaviors in budgerigars (Melopsittacus undulatus): An observational study of yawning and stretching Behavioural Processes DOI: 10.1016/j.beproc.2011.12.012.

Liebster Award and Nominees

wbLast week, I had the pleasure of receiving a note from science writer Mary Bates, informing me she had nominated AnimalWise for a Liebster Blog Award.

“Liebster” is a German word meaning dearest, beloved or favorite, and the Liebster Award is sort of a chain letter among bloggers that’s intended to showcase exceptional up-and-coming blogs (typically, those with 200 or fewer followers). Now, there’s no evaluation committee or formal award process for the Liebster, but in a way it’s even nicer – it’s recognition that a peer has noticed and appreciated your hard work.

I want to thank Mary very much for the recognition. Please check out her blog, which – with good reason – has already received the Liebster Award. Mary writes engagingly about biology, psychology, neuroscience, ecology, and all flavors of animal behavior. She earned her PhD from Brown University, where she researched bat echolocation and bullfrog chorusing (admit it, you’re jealous!). While you’re there, be sure to watch the video she’s posted about Li’l Drac, the adorable baby bat; you’ll be adopting your very own fruit bat before long.

Now, the rules for the Liebster Award are:

  1. Show thanks to the blogger who gave you the award by linking back to them.
  2. Reveal your top five picks and let them know by leaving a comment on their blog.
  3. Post the award on your blog.
  4. Bask in the love from some of the most supportive people on the internet—other writers and artists.
  5. And best of all – have fun and spread the karma.

Without further ado, here are my five nominees:

  • Endless Forms Most Beautiful: Kimberly Gerson captures and expresses the wonders she sees in the natural world vividly and with grace. Be sure to read about Romeo the wolf and what Kimberly would like you to do if she gets eaten by a polar bear.
  • Inkfish: Elizabeth Preston, the editor of MUSE, the award-winning children’s science magazine, stretches out her tentacles to bring you entertaining accounts of offbeat and fascinating new research studies relating to biology, psychology, evolution, physics, economics, and everything in between. Inkfish is playful and fun, but always accurate and true to the underlying science.
  • Puff the Mutant Dragon: Mutant Dragon breathes fire and writes exquisitely. The blog wraps together biology, biochemistry and history and toasts them into a delectable treat. If history was never your thing and you’ve always avoided chemical equations, I especially invite you to dig in – I think you just may find that you’ve found a new favorite cuisine!
  • Popperfont: David Ng, a molecular geneticist and member of the faculty at the University of British Columbia, has created Popperfont, an eclectic mix of scientific trivia, quotations, graphics, comics, stories and other assorted gems. Stop by Popperfont whenever you’re in the mood for some science fun and fascination.
  • Empirical Zeal: Aatish Bhatia, a Rutgers University grad student, shares his excitement regarding breakthroughs in diverse areas of science, including evolutionary biology, genetics, neuroscience and physics. Empirical Zeal is what great science blogging is all about: wonderful writing that makes technical topics understandable, accessible and exciting. Visit Empirical Zeal and you’ll see what I mean.

So thanks again to Mary, and I hope you enjoy the five nominee blogs as much as I do!