Social benefits of non-kin food sharing by female vampire bats

My new paper just came out in Proceedings B. For now, it’s freely available to download at the journal website here.

The paper describes an experiment that ‘failed’ in one sense but yielded another very neat finding nonetheless. The main goals was to detect for contingent reciprocity between close relatives. I kept several pairs of mothers and daughters from feeding each other for 3 weeks. The experiment should have been longer than this, but it was cut short. The positive result would have been evidence that all the bats began strengthening their relationships with other females at the expense of investments in the partner targeted by the experiment (a subtle form of partner switching). The negative result would be no response. What I found was that about half the bats did what I expected, and the other half actually invested more. You can read about that in the interview below. Basically, I consider that result a ‘failure’ because it needs further examination, and I can only speculate as to what it means. So I still don’t know if you can get evidence for partner switching among close kin. You need a better, longer experiment.

The other neat result came out exactly as predicted. When I took away a primary donor, the bats that had fed more non-kin females in previous years coped better: they had more donors and hence were fed more. This is what you would expect if bats feed non-kin because it increases their social safety net of reciprocal benefits. Both these results are shown visually in my previous post with slides from a conference talk.

There’s also a Nat Geo article about it here. The original unedited email interview by the journal article is below:

Hi Michael,

1. How did you first get involved with studying bats? And of all bats, why vampire bats?

I have been a bat fanatic since I was two or three years old. One of my earliest memories was seeing a large flying fox up close in the Philippines (my mother is from there) when I was just a toddler. Ironically, this is because the bats were being eaten!

I have been fascinated by bats from grade school to college to grad school. I discovered vampires during my undergraduate at Cornell. I took on a project to sequence prey DNA in vampire bat feces. When I started working with vampires, I immediately became enamored with their intelligence and their unique biology. Just about everything about vampire bats is interesting.

2. Prior to you and Jerry Wilkinson doing the work described in this study, what did we know about vampire bats’ feeding behavior?

I assume you mean food sharing behavior–
Jerry Wilkinson (my doctoral advisor) did this now-classic multiple-year field study on vampire bat food sharing, which was popularized in many textbooks and popular books such as the The Selfish Gene (Second Edition) by Richard Dawkins. He did this study for his PhD around the year I was born. I came to University of Maryland specifically to work with him and follow up on his work.

Basically, what Wilkinson found is two key things. First, vampires regurgitate blood to feed other adults (just like mother birds feed chicks). These blood “donations” are predicted by co-roosting association and by genetic kinship. Each of these factors was predictive, even when you controlled for the other. Second, he put created a captive group of non-relatives and simulated a situation where each failed at getting blood; he fasted one bat per night. The bats reciprocated donations more than expected by chance. From these findings, he suggested that bats help others, not only because of genetic kinship, but also because it would encourage reciprocal donations. This was of the first studies suggesting that reciprocity could be occurring even among related individuals. The idea that genetic relatedness can lead to altruism is one of the most well-supported findings in evolutionary biology. So when biologists see cooperation between animals that are genetic kin, it’s simple to say, “they cooperate because they are related” but of course it might be more complex.

Over time, Wilkinson’s conclusion that vampires share food because of reciprocity has drawn a lot of attention and also controversy. That’s why I wanted to look at it in more detail.

In a previous study we published in 2013 (in this same journal), we fasted a lot more vampire bats on a lot more nights. These were related and unrelated adult bats that were all familiar with each other. Under these circumstances, the bats’ decisions to help were based on their past social experience (things like receiving food or grooming in the past) not genetic relatedness. The best predictor of sharing from bat A to B was the sharing rate from B to A. To me this suggested that kin selection could not be the whole story for vampire bat food sharing.

3. Walk me through how you raise vampire bats in captivity. How do you keep them? Where do you get the blood? Give me a sense of what it’s like to stand in the enclosures and do your work.

I have worked with captive-born bats from zoos and with wild bats captured in Mexico, Belize, and Trinidad. The bats in this study are cared for by the Organization for Bat Conservation in Bloomfield Hills, Michigan. This is a great organization that supports conservation and research on bats. The advantage of these captive bats is that we know their maternal pedigree and their social history (every other vampire bat they have ever interacted with). The blood they drink is donated from an organic hormone-free slaughterhouse.

[NOTE: The article (and perhaps my response here) makes it seem like I started this colony, but I didn’t; I came to work at OBC’s vampire bats because I was invited by Rob Mies who saw me talk at a conference.]

When you walk into the enclosures, the older vampires all open their mouths wide to echolocate, so they can “see” you with their biosonar. A few of the younger bats will actually fly over, land on me, and run all over my body. That’s only because they were used to me being in there. This is something vampire bats will do to a large prey animal like a cow or horse. I really like it when they do that. They have never bitten me to get blood, but if I stayed still long enough in the cage or fell asleep, I think they would try to feed on me, even though these guys drink cow blood out of little spouts.

Most of my time is spent crouching on the floor outside the cage and watching them socialize using an infrared-sensitive camcorder. But I have it easy. Jerry Wilkinson spent hundreds of hours laying on his back amidst cockroaches and bat guano, directly below a wild vampire bat colony.

4. If I read your paper right, females that fed more bats who weren’t her kin received more food in turn, and they had more donors — but this doesn’t hold for males, or related bats of either sex. Why do you think that the non-kin female relationship is special?

It’s not that the non-kin female relationship is special, it’s just that if you want to have a wide social network, those are the relationships you need. If you’re a female vampire bat, you have a pretty limited number of maternal relatives, but many other non-relatives or distant relatives that you can form bonds with.

In the wild, male bats don’t form long-term social bonds. They leave their natal social group once they reach reproductive age. Food sharing is really more of a female behavior in vampire bats. Males sometimes feed females and vice versa, but males almost never feed males.

5. Figure 4 struck me for the starkness of the bimodal response: donor bats either dramatically upping or decreasing their donations once they were able to donate blood once again. What’s going on there?

I’m not 100% sure yet. I would like to repeat this experiment for a longer period and with more bats. One possibility is that only some of the bats are starting to shift their investments over to alternative partners, as we expected if the bats are basing their cooperative investments on their returns (gradual “partner switching”). And perhaps the other bats are actually sharing more with each other because they could not before, just like how you might be especially generous to a friend if you were unable to help them for a long time. I think we called this “relationship repair”. At this point, it’s still very speculative. I would need to see more data before I drew any strong conclusions.

6. Outside of feeding behavior, how else do vampire bats display sociality?

They groom each other. They cluster for warmth. They produced vocalizations (‘contact calls’) when they are isolated from the group. They might also follow each other to feeding sites. I have seen two vampire bats feed from the same wound. In fact, I have even seen one vampire bat crawl unto the back of another to reach a high wound on the leg of a chicken.

7. At the risk of oversimplifying your paper, it strikes me that socially speaking, female non-kin bats seem to play a long game, with feeding events affecting reciprocal behaviors weeks after the fact. How does that change our understanding of bat sociality — and influence our understanding of sociality as a whole?

Yes, I do think vampire bats are playing “the long game”. They can live to be more than 30 years old, and even in the wild, we have seen the same female vampire bats roosting together after more than a decade. Vampire bats were often the textbook example of reciprocity as “tit-for-tat” in the prisoner’s dilemma (an important game theory scenario where cooperation is difficult). The idea is that two animals might take turns helping each other, even though they suffer a risk at being exploited if the other doesn’t reciprocate. Reciprocity across repeated interactions is a good, stable strategy for cooperation (even in the prisoner’s dilemma). But in nature, It’s hard to find any scenarios in nature that really match all the assumptions of a prisoner’s dilemma. Cooperation rarely occurs in discrete rounds, and animals often have more than one social partner. Most importantly, they might have a foundation of past social experience– a social relationship.

When researchers studying cooperation have wanted to test the hypothesis of reciprocity in some animal species, we typically test whether two individuals will take turns pulling a lever to deliver a food gift to a partner (or something like that). If you and I are playing a cooperation game, the expectation is that I will reply to what you did to me in the last round. If you cooperate, I cooperate. If you defect, I defect, etc.

But what if you and I have been friends a long time? Well, it might take much longer for you to see me begin to stop cooperating with you.

I think we will find that many long-lived social animals, like cetaceans, elephants, vampire bats, ravens, and of course nonhuman primates, have cooperative social relationships that are functionally analogous to human friendships. I think we will find that they are reciprocal in the long-term but not strictly alternating. And the cooperative services are varied and diverse, like a human friendship. Friends are, in many ways, the family you choose. And as Aristotle said “A friend to all is a friend to none.” Human friendship is not a equal group-level behavior, you invest in certain relationships to the exclusion of others. These are important properties for when thinking about how cooperation might work in other species.

[Two more general questions]

Yikes, I have run out of time and I’m late for something. So I’m going to skip this question and the next one for now. I will write more later if I have time.


Thanks for your interest in my article.

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Why vampire bats network

This gallery contains 88 photos.

Here are slides from the longer version (about 2x as long) of the talk I gave at the annual meeting of the North American Society for Bat Research. There was a contest at the conference for shortest title, hence the … Continue reading

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New paper on giving intranasal oxytocin to vampire bats

Intranasal oxytocin increases social grooming and food sharing in the common vampire bat Desmodus rotundus I gave two groups of highly familiar captive vampire bats intranasal oxytocin. In the first group intranasal oxytocin led to larger regurgitated food donations. In the second group, I gave a larger dose and found that oxytocin also increased allogrooming between adult females. I did not detect effects on donation probability or number of grooming partners. The peak effect of intranasal oxytocin occurred 30-50 minutes after inhalation, matching the time that intranasal oxytocin causes a spike in brains of rats and mice. This suggests that intranasal oxytocin does not enter the brain directly. This paper also shows that oxytocin can be used as a tool in future manipulations of vampire bat cooperation.

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Vampires 101: An interview about vampire bats

I just spoke with a geologist who was fed on by a vampire bat while she slept outside just down the street from where I live. She found the small but bloody bite on her toe in the morning. In many years, vampire bats were almost never caught near Gamboa, Panama (where I live now) but since I’ve been here, people have caught 4 of them not too far away. Perhaps they are moving nearby because of some new large animals at the nearby zoo. (Or maybe they know I’m here!)

If you are bit by a bat, get a rabies post-exposure vaccination.

—-in other news—

I recently answered a bunch of questions from a journalist writing an article about blood-feeding. I thought my answers might also be of some interest to readers here, so I’m posting them below. I’m not posting his questions, because that might be some kind of copyright violation. (I did check to see if I own my own answers in an interview, and I think I’m in the clear). In the past, I’ve given interviews where journalists just use a tiny segment or quote (or misquote) which can completely distort what I was saying. So here’s the whole thing…(Sorry in advance for typos. It was an interview, not an article.)

On the public’s fear of vampire bats

Bats are perhaps the most misunderstood and maligned group of mammals. And of those more than 1300 species of bats, the three blood-feeding vampires are the most feared and hated, especially in Latin America where they live. Vampire bats are named after the mythical vampire legend, which actually pre-dates the discovery of the bat by European naturalists. As the name suggests, vampire bats drink nothing but blood, and throughout Central and South America, they most often feed on the blood of livestock. They only take about a tablespoon of blood, so they don’t kill the animal, but they can spread diseases like rabies. For this reason, they are considered a serious nuisance and a concern of animal and public health, and their populations are actively reduced in many areas by poisoning.

What most people don’t know about vampire bats is that they are actually incredibly intelligence and socially complex. Like primates, they form long-term social relationships and perform extensive social grooming. They possess a form of cooperative food sharing. If a bat comes back to a roost without getting a meal, other bats in her social network will regurgitate food for her, just like a mother bird does for her chicks. The difference is that the bats don’t just feed their offspring; they feed adults, both kin and non-kin that have helped them before. Bats that are more generous are fed more when they fail to feed. They rely on a social support network, and in that way, the bats have something analogous to human friendship. They also have very large brains and very large neocortex; they are outliers among bats in this regard.

I would say that the public’s relationship to vampire bats in Latin America is similar to North America’s relationship to the wolf in the last century. Both of these animals can be severe nuisance to farmers and ranchers. Teddy Roosevelt called wolves “the beast of waste and destruction” and the government policy was to kill them all until they were extirpated from an area. That’s essentially the policy towards vampire bats in Latin America. Now people in North America have a much more respectful and even reverential attitude towards wolves. We respect them for their intelligence, mystery, and their primal beauty. Maybe the same will happen with vampire bats.

On how vampires feed

Vampire bats have been observed feeding on many different kinds of wild and domestic animals, including horses, cows, goats, pigs, chickens, tapirs, peccaries, sea lions, even eagles and penguins. People can also be fed on by vampire bats, especially in the Amazon region of Peru and Brazil where humans might be even more accessible than livestock. The most common vampire bat (actually called “the common vampire bat”) prefers mammals. Another species prefers birds but will feed on mammals if available, and another rare vampire bat feeds exclusively on birds.

A vampire bat will usually feed on sleeping “host”. They walk or climb stealthily to an area where blood is close to the skin. They find this area using infrared heat receptors on their nose. They make a quick bite that removes a tiny divot of skin. Then they lick the blood that flows out. They have an anticoagulant in their saliva that prevents the wound from clotting too quickly. Often, the “host” does not even wake up.

These bats are quite stealthy and maneuverable on the ground. Unlike other bats, they can walk, jump, and even run on the ground. There is a slow-motion video online filmed by my friend Dan Riskin, check it out online. I think of them as “super bats” because they are super fast, super strong, super smart, etc.

About VampCam

Vamp cam was set up by Organization for Bat Conservation in Bloomfield Hills, Michigan. They have a great educational facility where the public can visit and see many species of bats from all over the world and learn about their ecological importance. The director Rob Mies had the great idea to put up a web cam last year so anyone in the world can watch the vampire bats. I piggybacked off this by creating a website where people could volunteer to score social behaviors for me (like grooming). It was a kind of social experiment to see if people would actually do it. It also allowed me to go back and watch video footage of anything especially interesting. So far, people from as far away as Australia have recorded about 70 observations. And a few people have emailed me about something they see. I have also heard that people have used it in the classroom. I still enjoy checking in on the bats now and then. Over the next 2 years, if I get this NSF funding, I’m hoping to develop it more into a citizen science project in collaboration with Organization for Bat Conservation.

About vampire bat infrared perception

The bats can detect subtle heat with their nose at a distance of about 16 cm or 6 inches. The only other animals that can do this are some snakes, like pit vipers. Vampire bats have evolved their own way of doing it, which is different than the snakes. There’s a protein that all vertebrates appear to have for detecting heat. The protein is called TRPV1; it is “tuned” to temperatures above 43 deg C. In vampire bat noses, the bats have a special version of the same protein that can detect temperatures as low as 30 deg C. In the rest of their body, they created the normal version. This is the typical way that new abilities evolve. You take an old adaptation and you tweak it to serve a new function.

No, the heat sensing has nothing to do with echolocation or biosonar, which is another special sensing ability used by vampires and most other bats to navigate in darkness. In addition to biosonar, and the “normal” senses, sight, smell, touch, hearing– vampire bats also have specialized low frequency hearing. One idea is that they use this ability to learn the breathing sounds of their prey, but this has yet to be confirmed.

On how bats use their wings

Bat biologists have identified more than 60 ways bats use their wings (besides flying). These including fanning themselves, defending themselves, hiding, courtship displays, holding objects, grooming, crawling, swimming, and capturing prey. For instance, most people don’t realize that bats that catch insects in the air use their wings as nets.

On bat parasites and parasitism

Vampire bats have more parasites than the average bat. In the neotropics, many of the bats have small bat flies called “streblids”. And there are mites and other things too, but I don’t know much about it. Bruce Patterson, an expert on bat flies, led a study where they counted bat flies on 53 bats in Venezuela and the vampire bats were ranked 5th and 6th in terms of how many bat flies they had.

These streblid flies can get around. I was in Belize with a colleague who was marking both bats and flies. She put a tiny drop of paint on each fly. She released one bat with a marked fly, and soon thereafter caught a different bat with the same fly! Apparently, the released bat went back to the roost and the fly switched hosts.

But yes, vampire bats are parasites, and they have parasites. And I would not be surprised if someone has studied the parasites on the bat flies. There are many microscopic protozoa like Trypansoma that are parasites on blood-feeding insects.

It also seems to me that being a parasite is the easiest way to make a living as a non-plant. You exploit a host, but without killing it. Parasitism is actually not too far from symbiosis, and it’s easy to make an evolutionary transition between the two relationships. If you extract resources from another organism (a parasite), it would benefit you even more to keep that organism alive and even help it reproduce (no longer a parasite), as long as you can still benefit yourself. That way, there’s less evolutionary pressure for your partner to evolve defenses. That’s essentially what humans do with domestic plants and animals when we take their fruits, seeds, and milk; we also help them reproduce more than non-domestic lineages.

I would argue that parasites (if you include pathogens) are the most important force in evolution. For example, it seems that parasites are the reason that sex exists, but that’s another story…”the red queen hypothesis”

But I wouldn’t call the bats bloodsuckers, since they don’t suck blood. When they feed, I think they look rather more like a cute cat lapping up milk (maybe that’s a stretch).

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Vampire bats are exceptional social groomers

Undergraduate Lauren Leffer and I just published a paper in PLOS One entitled Social Grooming in Bats: Are Vampire Bats Exceptional? The answer, I think, is yes. Here’s the story behind the paper.

Grooming monkeys

When you think of social grooming, you think of primates. Social grooming in primates has been viewed as a social glue that helps maintain social bonds, and as a social currency that can be exchanged for favors. In fact, I would wager that there are more data on social grooming in primates than almost any other mammalian cooperative behavior (outside humans). But many other animals groom each other too, including some bats. In 1986, Jerry Wilkinson published a great observational study on social grooming in vampire bats, and he showed that it correlated with both food sharing and differed between ages and sexes. My impression has always been that vampire bats are pretty unique among bats in their propensity for social grooming. But we know that at least some other group-living bats also groom each other, and some people have told me that, in captivity, other bat species groom each other maybe even just as much as the vampires. So how special are vampire bats? Are they really more like primates than other bats?
ARKive video - Common vampire bats allogrooming and territorial males fightingDoing a comparative study on social grooming across species is a bit tricky in the field, because other factors, like the number of ectoparasites, or the nature of the relationships between the individual bats, might predict grooming rates even more than the species differences. For example, vampire bats have lots of ectoparasites, and they also form long-term social bonds, and maybe that’s why they social groom each other more.

At the Bat Zone, run by the Organization for Bat Conservation (OBC), there are several species of group-living bats living in captivity. None of them have bat flies or other ectoparasites, and since all the bats are stuck in captivity, there are not species differences in proximity or association, like you would normally have in the wild. In other words, the environments are pretty similar for all the bats there. So, in my mind, it’s a great opportunity to compare social grooming rates.

Undergraduate student Lauren Leffer, with help from volunteers at OBC, sampled social grooming by watching a single random individual, and then going from cage to cage, species to species, and recording what the bats were doing. Social grooming was of course, pretty rare overall; but I was surprised to find that observers witnessed it in many of the captive bats, even in species, like Carollia perspicillata, where it has never, to my knowledge, been observed in the wild. But the rates were very low compared to the vampire bats. You can read the paper for more details on that.

To me, this all suggests that there’s a real species difference in social grooming, and it’s not just an artifact of some particular vampire bats being more familiar with each other than members of other species.

Here in Panama, graduate student Victoria Flores has been watching many videos of social interactions between roosting frog-eating bats (Trachops cirrhosus).  Like all bats, they spend some time grooming themselves. But Victoria has never seen Trachops grooming others either.

I also did a study where I put several completely unfamiliar vampire bats together for several weeks. At first, there was no social grooming, but gradually the bats began to groom each other. You could see bonds forming in real time; it was fascinating. I’m replicating that study in a couple of months here in Panama. We are in search of roosts and places to catch vampires. A couple of days ago, Thomas Sattler sent me these pictures of a (very) large roost of common vampire bats in a hollow tree in Panama.

IMG_2936 IMG_0100

That’s a lot of vampire bats!

Here at the Smithsonian Tropical Research Institute, I’m starting a project on the sensory ecology of vampires with Rachel Page and John Ratcliffe (starting in January 2016). I’m also applying for NSF fellowship money to work on social behavior, oxytocin, and oxytocin receptors with Alex Ophir. If successful, this work would start January 2017 at the latest, but the competition is quite stiff and seems unlikely. The sensory ecology work is guaranteed, and should be quite fun, because it will involve experiments with single subjects that one can watch in real time. In contrast, the social behavior experiments take much more time, the data require weeks to accumulate, and one has to analyze interactions between multiple subjects (social networks). We are currently planning and preparing for the arrival of our vampire bat colony, while waiting for our permits to be approved.

Finally, this short note paper also just came out, from my visit to Thailand.

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Names of farmers and ranchers in Panama

I need names and addresses of farmers and ranchers in Panama that have seen vampire bat bites on their animals! If you or anyone you know has information, please email me or call me at 68293025 (Panama).

Fresh vampire bat by Uwe Schmidt

Fresh vampire bat bite by Uwe Schmidt

The urgency is that I need a this list as soon as possible to meet a permit deadline. I need authorization from all landowners >50 days before I catch any bats!

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A suggested reading list

I just gave a talk on vampire bat cooperation, and someone asked me for a reading list to introduce them to the topics I talked about (cooperation, reciprocity, social bonds, etc). So here it is (real quick, no time to put links). I chose review papers wherever possible and only picked empirical studies with results that make important points (marked with ***). Some of the empirical results are just a single paper that’s part of a larger story with more papers. In this case, I picked my favorite one. My suggested reading list of papers on cooperation (just my opinion, don’t get mad if your favorite is missing):

Evolution of cooperation

  • West, S. A., Griffin, A. S., & Gardner, A. (2007). Evolutionary explanations for cooperation. Current Biology—This paper is the best short introduction to the field.
  • ***Griffin, A.S., West, S.A. & Buckling, A. (2004) Cooperation and competition in pathogenic bacteria. Nature—An experimental evolution study that demonstrates empirically how the scale of competition interacts with genetic relatedness: cooperating with kin is less advantageous when you compete with those same kin for resources.

Human cooperation

  • West, S. A., El Mouden, C., & Gardner, A. (2011). Sixteen common misconceptions about the evolution of cooperation in humans. Evolution and Human Behavior. —Great review paper that helps clear up the huge amount of confusion in evolutionary studies of human cooperation.
  • ***Burton-Chellew, M.N. & West, S.A. (2013). Pro-social preferences do not explain human cooperation in public-goods games. Proceedings of the National Academy of Science. — Great paper. Explains the problem with an entire faulty approach to studying human cooperation.
  • DeScioli, P., & Kurzban, R. (2013). A solution to the mysteries of morality. Psychological Bulletin. — A very innovative solution to a very good puzzle.

Direct fitness benefits

  • Trivers, R. L. (1971). The evolution of reciprocal altruism. Quarterly Review of Biology. —People should read this paper again. There’s a lot of great ideas packed into it.
  • Carter, G. G. (2014). The reciprocity controversy. Animal Behavior and Cognition. —Please ignore the fact that you’ve never heard of this journal! I argue that most of the reciprocity controversy is semantic (much like the “kin selection” vs “group selection” confusion).
  • ***Wilkinson, G. S. (1984). Reciprocal food sharing in the vampire bat. Nature. —Argues that reciprocity can occur between relatives, but that point was, and still is, largely overlooked.
  • Bshary, R., Grutter, A. S., Willener, A. S., & Leimar, O. (2008). Pairs of cooperating cleaner fish provide better service quality than singletons. Nature, 455(7215), 964-966.
  • ***Zöttl, M., Heg, D., Chervet, N., & Taborsky, M. (2013). Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay. Nature communications, 4, 1341. —This study shows an interesting interaction between kinship and enforcement.
  • Ratnieks, F. L., & Wenseleers, T. (2008). Altruism in insect societies and beyond: voluntary or enforced? TREE. —A good review of the same topic.

Partner choice and biological markets

  • Noë, R., & Hammerstein, P. (1994). Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology and Sociobiology. — The best new ideas for understanding more complex cooperation since Trivers (1971).
  • Noë, R. (2006). Cooperation experiments: coordination through communication versus acting apart together. Animal Behaviour. — The best review of cooperation/reciprocity experiments and what’s wrong with so many of them.
  • ***Fruteau, C., Voelkl, B., Van Damme, E., & Noë, R. (2009). Supply and demand determine the market value of food providers in wild vervet monkeys. Proceedings of the National Academy of Sciences. — This is maybe my favorite study of cooperation. It demonstrates so many things: not only partner choice and market effects like supple and demand, but also that food is easily exchanged for other services like grooming.
  • ***Kiers, E. T., Duhamel, M., Beesetty, Y., Mensah, J. A., Franken, O., Verbruggen, E., … & Bücking, H. (2011). Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science. I love it!! Very clean result. Amazing experiment.

Cooperative social bonds

  • Seyfarth, R. M., & Cheney, D. L. (2012). The evolutionary origins of friendship. Annual Review of Psychology. The best review on this growing literature.
  • Dunbar, R. I., & Shultz, S. (2007). Evolution in the social brain. Science, 317(5843), 1344-1347.—a good argument for why social bonds are not simple emergent byproducts (like psuedoreciprocity).

Oxytocin and cooperation

  • ***Madden, J. R., & Clutton-Brock, T. H. (2011). Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal. Proceedings B. — Shows the power of peripheral OT for manipulating behavior, and that one mechanism underlies several cooperative behaviors.
  • Crockford, C., Deschner, T., Ziegler, T. E., & Wittig, R. M. (2014). Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review. Frontiers in Behavioral Neuroscience.— A great review of an exploding field.

Others, maybe unrelated, but personal favorites of mine

  • Karban, R., Shiojiri, K., Ishizaki, S., Wetzel, W. C., & Evans, R. Y. (2013). Kin recognition affects plant communication and defence. Proceedings B. —Incredible.
  • Page, R. A., & Ryan, M. J. (2006). Social transmission of novel foraging behavior in bats: frog calls and their referents. Current Biology. — One of the best behavioral studies on bats and paved the way for many other great studies.
  • Gould, E. (1988). Wing-clapping sounds of Eonycteris spelaea (Pteropodidae) in Malaysia. Journal of Mammalogy. A hidden gem. Ed Gould was right: they do echolocate with their wings: See the confirmation experiments by Yossi Yovel.
  • von Helversen, D., & von Helversen, O. (1999). Acoustic guide in bat-pollinated flower. Nature. — What a great discovery.
  • Killingsworth, M. A., & Gilbert, D. T. (2010). A wandering mind is an unhappy mind. Science. — Fun quick read.
  • Dudley, S. A., & File, A. L. (2007). Kin recognition in an annual plant. Biology Letters. — What a joy!
  • Ratcliffe, J. M., Fenton, M. B., & Galef, B. G. (2003). An exception to the rule: common vampire bats do not learn taste aversions. Animal Behaviour. — This is a nice example of a great prediction leading to a great experiment and a great result. A great little story.
  • Gould, E., Woolf, N. K., & Turner, D. C. (1973). Double-note communication calls in bats: occurrence in three families. Journal of Mammalogy, 998-1001. — I like this study because it introduced the idea of really studying bats for communication rather than just echolocation. Also, it kick-started and inspired my masters work when I notice these same call types made by adult vampires.
  • Boughman, J. W., & Wilkinson, G. S. (1998). Greater spear-nosed bats discriminate group mates by vocalizations. Animal Behaviour, 55(6), 1717-1732. — Such a great story and fits together so well with other work.

I’m sorry if your own paper does not show up in this list. There are a lot of great papers and I can’t think of them all off the top of my head. These are the ones that came to me just now.

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