A new field site in Panama

I am hoping to develop some new long-term field sites for future work on vampire bats.

On March 27, I traveled with Austin Garrido, Rob Mies (director of the Organization for Bat Conservation), his daughter Georgia Mies, and labmates May Dixon, Rachel Crisp, Katharina Eggert, Hugo Narizano, and Julia Vrtilek to Lake Bayano, a two-hour drive from our lab in Gamboa, Panama. This is closer than our other field site which is five hours away. On a previous trip, I had seen several stable roosting groups of vampire bats (Desmodus rotundus) in Pueblo Nuevo Cave along with other bats including Natalus mexicanus roosting individually, Carollia perspicillata roosting in small groups, and large mixed aggregations of Pteronotus gymnonotus and, I think, Pteronotus parnelli.

We saw the same species on this trip. At least 3-4 female groups of vampire bats were located in the first part of the cave that is easily accessible from the entrance. These are groups I hope to track in the future using proximity loggers. See the video below with high-definition infrared footage shot by Rob Mies, which allowed me to count the bats.

There are apparently about five cattle pastures in the surrounding area. That night, during the new moon, we set mist-nets around corralled cattle at the closest pasture hoping to catch and band a sample of vampire bats and perhaps even see some of those same marked individuals back in the cave. A large mark-recapture study could even help us estimate the vampire bat population size.

That night, we caught only 25 vampires bats in our nets. Three escaped from the hand or net being before being processed (a female and two bats of unknown sex). Interestingly, only 5 of 24 vampire bats we netted at the cattle pasture were female. One of these female vampires was a yearling, not fully grown. The captures were spread pretty evenly throughout the night, but the highest density of captures seemed to be between 1:45 and 4:00 am. We recaptured two of the bats we banded. The last bat we caught was around 4:30 am and we took down nets around 5 am.

The next day, I saw one of the banded males back in the cave. The three original female groups were still there. Hopefully, this will be a second site that Simon Ripperger and I will study social foraging in vampire bats. I had valuable discussions with the cattle farmers. They agreed to gather the farmers together at some point when we return in order to discuss what work we would like to do there in the future.

A big special thanks to Austin Garrido for organizing logistics, to May Dixon for help with all-night mist-netting, and to Rob Mies for footage.

Posted in About vampire bats, News | Leave a comment

Update: three golden opportunities

Now – October 2017, the Smithsonian Institute has awarded me with a fellowship to finish collecting data from lab and field experiments on vampire bat social behavior with Rachel Page at the Smithsonian Tropical Research Institute in Panama.

November 2017 – August 2018, the Humboldt Foundation has awarded me a fellowship to learn more about social network analysis, resampling methods, and simulations in collaboration with Damien Farine at the Department of Collective Behavior, Max Planck Institute for Ornithology, in Germany.

August 2018, I will be back in the USA working in the Department of Evolution, Ecology and Organismal Biology at The Ohio State University as a tenure-track assistant professor of biology. I will also continue my collaborations with the Organization for Bat Conservation.

This is an exciting time, and the challenge for me is to make the very most of it! I find myself in the unbelievably fortunate and privileged position of being gifted the freedom to do what I love, and given the resources to do it as well as I can. For this, I owe a tremendous debt of gratitude to my recent mentors, Jerry Wilkinson, John Ratcliffe, and Rachel Page. Most of all, I thank everyone on Team Vampire.

Work as hard as much as you want to on the things you like to do the best. Don’t think about what you want to be, but what you want to do!Richard Feynman

 

 

 

 

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Reciprocity before Trivers

“New” ideas are rarely new. In science we stand on the shoulders of giants and whenever I read the works of the giants, I often find that many ideas or discoveries– that I thought were “mine” or belonged to some more recent author– were actually first described by Darwin or some other author from long ago.

I hope to soon publish a paper on a hypothesis I call “social bet-hedging” which is the idea that individuals might face a trade-off between investing in the quantity versus quality (strength) of cooperative relationships, and that, in unpredictable social environments having more friendships might be better than  investing in fewer stronger friendships (even if the opposite is true normally). More on this in a future blogpost.

Before publishing it, I looked through the cooperation literature and emailed people who have most influenced me on the topic of cooperative relationships: Ronald Noe, Dorothy Cheney, and Robert Seyfarth. I wanted to make sure that I had not accidentally stolen the idea from someone else.

If you read the scientific literature on a given topic in backwards chronological order, you find that authors with new ideas tend to overemphasize their originality. This is probably also true for novel technology. In science, most “new ideas” are really incremental developments or novel applications of older ideas. Work that is labeled “transformative” and “revolutionary” often involves taking something that’s been around awhile (but never fully appreciated) and showing its general importance in a convincing manner.

Even when new ideas are truly new, they often are built on a foundation that allows contemporary thinks to converge of the same new idea. For example, before Darwin famously discovered natural selection, some forester you probably never heard of named Patrick Matthew discovered it three decades earlier. He compared artificial selection on trees with what normally happens in a forest: the healthiest most fecund trees survive and reproduce (kinda obvious really). He wrote,

“There is a law universal in nature, tending to render every reproductive being the best possibly suited to its condition that its kind, or that organized matter, is susceptible of, which appears intended to model the physical and mental or instinctive powers, to their highest perfection, and to continue them so. This law sustains the lion in his strength, the hare in her swiftness, and the fox in his wiles. As Nature, in all her modifications of life, has a power of increase far beyond what is needed to supply the place of what falls by Time’s decay, those individuals who possess not the requisite strength, swiftness, hardihood, or cunning, fall prematurely without reproducing—either a prey to their natural devourers, or sinking under disease, generally induced by want of nourishment, their place being occupied by the more perfect of their own kind, who are pressing on the means of subsistence.”

That first sentence is not the best example of clear writing, but that was the style back then in ye olde days. Even more unfortunate is that he published this in an appendix to a book entitled Naval Timber and Arboriculture (1831) where it remained mostly unread.

As Ernst Mayr summarized:

Patrick Matthew undoubtedly had the right idea, just like Darwin did on September 28, 1838, but he did not devote the next twenty years to converting it into a cogent theory of evolution. As a result it had no impact whatsoever.

Not everyone thinks this is fair. Yep, there’s a full conspiracy theory regarding this “greatest cover-up in the history of science”.

The double invention of calculus is another example of new ideas coming about independently but simultaneously, giving the impression that the time was ripe and the stage was set.

New ideas never jump into existence fully formed by single people. They are memes that persist by being passed along (like natural selection), and they evolve by branching off from previous forms (like speciation). For this reason, most discoveries come into focus gradually. True “Eureka” moments in science are rare. Profound new idea are always built on foundation of less appreciated past work.

I was reminded of this recently while reading a section of the classic work Adaptation and Natural Selection by GC Williams (1966). So many of the ideas I attributed to Trivers’s notion of “reciprocal altruism” (1971) and its application to human friendship could be traced back to older works, even well-read classics like this one.

Before I present the key text, I’ll recap a bit of brief background. The concept of reciprocal altruism or reciprocity was formulated by Trivers 1971 (Quarterly Review of Biology) with the suggestion that each individual’s need to enforce mutual benefit could help explain many behaviors that underlie enduring cooperative relationships, including human friendship. The idea was extremely influential.

Trivers’ paper also touched upon on almost every related topic, such that for every subsequent extension of Trivers’ idea, one can find a mention of it in his original paper. For instance, biological market theory (Noe and Hammerstein 1994, 1995) later added the role of market effects and the emphasized a distinction between models of partner choice and partner control (i.e. reciprocal altruism). But in his paper, Trivers’ mentioned the role partner choice in friendship. He also described cases where cooperation was enforced by ecological circumstance rather than by behavior (now called “pseudoreciprocity” or “byproduct benefits”). He described applications to cleaner-client fish, which later became an important model system. Trivers also mentioned the iterated prisoner’s dilemma as a model for the evolution of reciprocity, which was later formalized by Axelrod & Hamilton ten years later (1981 Science). He even mentioned interactions between reciprocity and kinship which have only been experimentally explored recently. Although Trivers never actually worked on reciprocity himself, he at least mentioned almost all the new ideas and directions that would be developed from his theory.

As a term, “reciprocal altruism” is competing with other terms and concepts in the struggle for existence. In biology, the popularity of this term (and the breadth of its definition) rose to a peak in the 1990s, where it became mired in confusion and controversy, eventually falling in popularity until today it is defined very specifically and often considered unimportant outside of humans. I wrote a review explaining how and why this happened.

But I digress. My point here is that the foundations for the concept of reciprocity had already been floating around in the collective scientific consciousness before Trivers (1971). For example, the “tit-for-tat” demonstration built upon the ‘folk theorem’ of game theory–that repeating interactions which influence fitness can stabilize the evolution of almost any behavioral trait through social reward/punishment–an observation that has been understood since the 1950s.

A second example: here is the text from GC Williams Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought (1966) discussing contingency in cooperative relationships (bold emphasis mine).

…I wish to consider an apparent exception to the rule that the natural selection of individuals cannot produce group-related adaptations. This exception may be found in animals that live in stable social groups and have the intelligence and other mental qualities necessary to form a system of personal friendships and animosities that transcend the limits of family relationship. Human society would be impossible without the ability of each of us to know, individually, a variety of neighbors. We learn that Mr. X is a noble gentleman and that Mr. Y is a scoundrel. A moment of reflection should convince anyone that these relationships may have much to do with evolutionary success. Primitive man lived in a world in which stable interactions of personalities were very much a part of his ecological environment. He had to adjust to this set of ecological factors as well as to any other. If he was socially acceptable, some of his neighbors might bring food to himself and his family when he was temporarily incapacitated by disease or injury. In time of dearth, a stronger neighbor might rob our primitive man of food, but the neighbor would be more likely to rob a detestable primitive Mr. Y and his troublesome family. Conversely, when a poor Mr. X is sick our primitive man will, if he can, provide for him. Mr. X’s warm heart will know the emotion of gratitude and, since he recognizes his benefactor and remembers the help provided, will probably reciprocate some day. A number of people, including Darwin (1896, Chap. 5), have recognized the importance of this factor in human evolution. Darwin speaks of it as the “lowly motive” of helping others in the hope of future repayment. I see no reason why a conscious motive need be involved. It is necessary that help provided to others be occasionally reciprocated if it is to be favored by natural selection. It is not necessary that either the giver or the receiver be aware of this.

Simply stated, an individual who maximizes his friendships and minimizes his antagonisms will have an evolutionary advantage, and selection should favor those characters that promote the optimization of personal relationships. I imagine that this evolutionary factor has increased man’s capacity for altruism and compassion and has tempered his ethically less acceptable heritage of sexual and predatory aggressiveness. There is theoretically no limit to the extent and complexity of group-related behavior that this factor could produce, and the immediate goal of such behavior would always be the well-being of some other individual, often genetically unrelated. Ultimately, however, this would not be an adaptation for group benefit. It would be developed by the differential survival of individuals and would be designed for the perpetuation of the genes of the individual providing the benefit to another. It would involve only such immediate self-sacrifice for which the probability of later repayment would be sufficient justification. The natural selection of alternative alleles can foster the production of individuals willing to sacrifice their lives for their offspring, but never for mere friends.

The prerequisites for the operation of this evolutionary factor are such as to confine it to a minor fraction of the Earth’s biota. Many animals form dominance hierarchies, but these are not sufficient to produce an evolutionary advantage in mutual aid. A consistent interaction pattern between hens in a barnyard is adequately explained without postulating emotional bonds between individuals. One hen reacts to another on the basis of the social releasers that are displayed, and if individual recognition is operative, it merely adjusts the behavior towards another individual according to the immediate results of past interactions. There is no reason to believe that a hen can harbor grudges against or feel friendship toward another hen. Certainly the repayment of favors would be out of the question.

A competition for social goodwill cannot fail to have been a factor in human evolution, and I would expect that it would operate in many of the other primates. Altman (1962) described the formation of semipermanent coalitions between individuals within bands of wild rhesus monkeys and cited similar examples from other primates. Members of such coalitions helped each other in conflicts and indulged in other kinds of mutual aid. Surely an individual that had a better than average ability to form such coalitions would have an evolutionary advantage over its competitors. Perhaps this evolutionary factor might operate in the evolution of porpoises. This seems to be the most likely explanation for the very solicitous behavior that they sometimes show toward each other (Slijper, 1962, pp. 193-197). I would be reluctant, however, to recognize this factor in any group but the mammalia, and I would imagine it to be confined to a minority of this group. For the overwhelming mass of the Earth’s biota, friendship and hate are not parts of the ecological environment, and the only way for socially beneficial self-sacrifice to evolve is through the biased survival and extinction of populations, not by selective gene substitution within populations.


The observation that great new ideas often have precedents can also be made about Hamilton’s inclusive fitness theory, the best contender for most important and influential theory in social evolution. This idea, which Maynard Smith later renamed “kin selection”, was supposedly discussed informally by JBS Haldane in the 1950s.

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Maynard Smith’s apology letter in the magazine New Scientist for taking credit away from WD Hamilton and assigning it to JBS Haldane

Most people agree that the credit for the idea of kin selection must go to Hamilton. But some people attribute it to Haldane or Maynard-Smith, and much worse, I have seen many lay authors and social scientists credit the famous author Richard Dawkins with these ideas, because he popularized it in his classic 1976 book “The Selfish Gene”. For better or worse, the evolutionary success of a new idea will depend not only on its accuracy, but its ability to be understood and to thereby influence others. This is why Dawkins did more for spreading Hamilton’s ideas than Hamilton did. Credit typically goes to those who do the best job of developing and explaining the ideas’ importance to others and making it available for them to use. And sometimes the jobs of innovation, development, and popularization are best done by different people.

Scientists are motivated by getting recognition for their work, but perhaps we scientists should be explicit that we should (and do) give less credit to whoever had the idea first. If you have a good idea, there’s a good chance someone else had it first. What matters more is what you do with your ideas. The most important reason to know everything relevant that came before is to advance knowledge or develop it further without wasting time reinventing the wheel.

Posted in About cooperation, About science as an activity | Leave a comment

Field notes on weekend trip to Costa Rica (with disc-winged bats!)

Spix’s disc-winged bat Thyroptera tricolor has suction cups (yes, suction cups) on its thumbs, and it uses these to cling to the smooth surface of young, furled Heliconia leaves.

I’ve wanted to see a disc-winged bat since I was about ten years old, and I finally got to see them this week while visiting Gloriana Chaverri, and Caroline and Michael Schöner at their field site in Costa Rica over the weekend.

Gloriana is a leading expert on social lives of Neotropical leaf-dwelling bats. This includes bats that chew leaves to make them into “tents” as well as disc-winged bats (Thyroptera). Over the last seven years, Gloriana has shown that Thyroptera live in small groups with multiple matrilines that often switch between their very temporary roosts, the furled leaves [1-3]. Both sons and daughters often remain at their natal site, and inbreeding is avoided because the bats mate with members of other populations. Each population includes several groups that switch among several roosts.

Despite moving daily between their tubular leaf roosts, the bats maintain very cohesive social networks. To coordinate their roost-switching, the bats use a system of contact calling [4-7]. Bats flying in search of their group make one contact call type called an “inquiry call” and groupmates within furled leaves make another call type in response. The calls have both individual and group-level signatures. The calls are also amplified by the funnel-like shape of the leaf roost.

Here’s a video of one flying into a leaf roost:

 

Most recently, Gloriana has been working with Caroline and Michael Schöner. The Schöners have pioneered work on an astonishing mutualism in another leaf-dwelling bat [8-10]. There is a pitcher plant in the paleotropics (Nepenthes) that has coevolved with a small insectivorous bat of the genus Kerivoula. The bat lives inside the pitcher and defecates into the fluid-filled “pitcher”. Most pitcher plants are carnivorous. They trap, drown, and digest insects inside the tiny pool of their pitcher, but this pitcher plant is modified to be a tiny little one-bat house. The level of the digestive fluid is lower to accommodate the bat’s roosting position. The plant lets the bat do the capturing, chewing, and pre-digesting of the insect prey. Some pitcher plants also attract shrews with a nectar reward and get them to poop into the pitcher [11]. For lack of a more polite term, the Schöners call the plants “coprophagous”.

In exchange for nutrients, the plant benefits the bat by providing it with a literal “roof over it’s head” and it’s distinctive shape is acoustically attractive to the bats. This is yet another example of bat-plant acoustic communication. There are also bat-pollinated flowers and leaves that reflect and enhance the echolocation calls of bats when they are ready to be pollinated [12-13].

What’s especially intriguing is that Kerivoula will also live in a different pitcher plant species that is not coevolved for the bats, and the bats can only fit inside the pitcher because it has been emptied. How? Something chews a small hole at the base of the pitcher to drain the liquid out. Could it be the bat? Nobody knows for sure. The Schöners suspect this is the case, but they have not yet caught the bat in the act. The bat might be a mutualist for the first species, but a parasite for the other. Or perhaps there’s a three-way interaction: the bat, the pitcher plant, and a third mystery organism that makes the hole, perhaps to drinks the pitcher plant liquid. It’s an unsolved mystery.

See also this blogpost by Merlin Tuttle and photos.

The Schöners are surprised by the physical similarities of Thyroptera and Kerivoula, although the personalities of the two bats are quite distinct. Kerivoula will eat larger insects and has the bite to match. Thyroptera it seems are a bit easier to work with. After your experiments are done, you can release Thyroptera into a furled leaf and they will just crawl inside and stay. As Caroline puts it, “Thyroptera is more well-behaved.”

The Schöners are tracking the bats’ movements among different leaves in the wild. Do the same bats consistently find new leaves and others follow? Or do all the bats do a search on their own? They are also looking at the bats use of spatial memory when relocating roosts. For this experiment, they work in a flight tent with an array of artificial leaves. The work is fascinating and I’m excited to see the results.

The Schöners take turns tromping around in the forest looking for bats and staying at the field station looking after their 9-month-old, Sophia, who loves fried platanos and has inherited the Schöners’ love of smiling. One similarity between Gloriana and the Schöners is their friendliness and propensity for hearty laughing. The atmosphere at the field station is one of joyful cheer, with everyone trying their best to make Sophie smile. It’s been a great place for a holiday.

Before coming to the Baru field station where I am now, I visited two caves with my wife Michelle, my labmate Nia Toshkova, and our guide: Gloriana’s graduate student Stanimira Deleva, who is studying the variation in use of caves by all different Costa Rican bats. The larger caves was two kilometers long and full of Pteronotus gymnonotus or Pternotus davyi. The smaller cave had Saccopteryx bilineata and Peropteryx kappleri. Nia and Stanimira are old friends, both cavers from Bulgaria. Michelle and I met Stanimira on a caving trip in Panama where I found a new potential site to work with vampire bats.

Here is a video of the Thyroptera being very cute:

References:

  1. Chaverri, G., & Kunz, T. H. (2011). All-offspring natal philopatry in a neotropical bat. Animal behaviour, 82(5), 1127-1133.
  2. Buchalski M, Chaverri G, and Vonhof M. 2014. When genes move farther than offspring: gene flow by male gamete dispersal in the highly philopatric bat species Thyroptera tricolor. Molecular Ecology 23:464-480.
  3. Chaverri G. 2010. Comparative social network analysis in a leaf-roosting bat. Behavioral Ecology and Sociobiology 64:1619-1630.
  4. Chaverri G, Gillam EH, and Vonhof MJ. 2010. Social calls used by a leaf-roosting bat to signal location. Biology Letters 6:441-444.
  5. Gillam EH, and Chaverri G. 2012. Strong individual signatures and weaker group signatures in contact calls of Spix’s disc-winged bat, Thyroptera tricolor. Animal Behaviour 83:269-276.
  6. Chaverri G, Gillam EH, and Kunz TH. 2012. A call-and-response system facilitates group cohesion among disc-winged bats. Behavioral Ecology 24:481-487.
  7. Chaverri G, and Gillam EH. 2013. Sound amplification by means of a horn-like roosting structure in Spix’s disc-winged bat. Proceedings of the Royal Society B 280:20132362.
  8. Grafe TU, Schöner CR, Kerth G, Junaidi A, and Schöner MG. 2011. A novel resource–service mutualism between bats and pitcher plants. Biology Letters 7:436-439.
  9. Schöner CR, Schöner MG, Kerth G, and Grafe TU. 2013. Supply determines demand: influence of partner quality and quantity on the interactions between bats and pitcher plants. Oecologia 173:191-202.
  10. Schöner MG, Schöner CR, Simon R, Grafe TU, Puechmaille SJ, Ji LL, and Kerth G. 2015. Bats are acoustically attracted to mutualistic carnivorous plants. Current Biology 25:1911-1916.
  11. Clarke, C. M., Bauer, U., Ch’ien, C. L., Tuen, A. A., Rembold, K., & Moran, J. A. (2009). Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters, 5(5), 632-635.
  12. von Helversen, D., & von Helversen, O. (1999). Acoustic guide in bat-pollinated flower. Nature, 398(6730), 759-760.
  13. Simon, R., Holderied, M. W., Koch, C. U., & von Helversen, O. (2011). Floral acoustics: conspicuous echoes of a dish-shaped leaf attract bat pollinators. Science, 333(6042), 631-633.
Posted in About cooperation, Other topics | 1 Comment

New paper: risk exaggerates nepotism in vampire bats

Here’s the paper.

In evolutionary biology, we often draw a line between “altruism” and other cooperative traits. Altruistic traits are special in that they lead to a net cost to one’s survival and reproduction. Some traits are clear cases: when a bee stings you it dies, so the suicidal bee sting is an altruistic trait.

But nature abhors clear categories. Most seemingly “altruistic” behaviors are ambiguous in whether they pose net average fitness benefits or costs. This leads to some confusion for several reasons. First, most acts that most people call altruistic are not altruism in the evolutionary sense. Any form of “reciprocal altruism” is not really altruism as defined above. This is why people who study animal cognition invented the term “prosocial” behavior to avoid the word “altruism” and all the inevitable semantic arguments with evolutionary biologists. Second, the kinds of costs we can easily measure (like time and energy) are not the same as fitness costs which can only be measured after whole lifetimes have gone by, so this means we can’t categorize most of the cooperative behaviors that we are studying. Third, many people equate helping kin with “altruism” but much helping between kin might actually be mutually beneficial. For example, natural selection might have shaped me to care about the survival of my family, not just because that helps them survive, but also because it helps my own survival.

For traits like this that pose both costs and benefits to the helper (food sharing in vampire bats is an example), it’s better to think of there being a spectrum where the exact cost/benefit ratios of a cooperative trait can slide around from positive to negative depending on the circumstances. It’s not a completely different behavior just because you move from -0.1 to +0.1 direct fitness effects.

Thankfully, to better understand a cooperative trait, we don’t always need to try to unambiguously classify traits or exactly measure the change in lifetime reproductive success that comes from performing the behavior. Instead, we can just change the factor we think is important and see if the animal’s helping decisions also changes as one would expect from theory. Rather than measuring lifetime fitness consequences, we can test the design of the trait. In this case, what information is involved the decision-making process?

For example, many animal parents will go to extreme lengths to protect their babies (e.g. below is footage of a mother moose attacking a truck) and various theories (inclusive fitness and parent-offspring conflict) makes predictions about the design of this behavior.

A mother’s brain should be designed by natural selection to put herself at some degree of risk to save her offspring, but not too much risk. Unlike the sterile worker bee, she is not a genetic dead-end, so she should not carelessly cast away her own life for any potential benefit to her genetic kin. Theory predicts that at some risk to her own survival and reproduction, she should give up on trying to save her offspring. There’s a risk factor that can be tuned up and down that should have an effect on the probability of A helping B, and this factor should interact with genetic relatedness. One could also tune up the kinship factor. As the famous quote by Haldane goes: I would give up my life to save 2 brothers or 8 cousins.

Risk should decrease my willingness to help and increase the degree to which I care about someone’s relatedness to me. As you dial down the risk, I am more willing to help: I would not run into a burning building, suffering certain third degree burns, to help a total stranger, but I would do it if I had protective gear. As you dial up the risk to me, the circle of people I would be willing to help in that situation should shrink: I would jump in the ocean to save a stranger, but I would only jump in shark-infested waters to save my child.

Like other animals, we don’t weigh the costs and benefits consciously, but the emotional urgency we feel to help or not help depends on situation-based cues that have, in our evolutionary past, acted as reliable indicators of inclusive fitness benefits of helping in situations similar to the one we are facing. 

So how can we test this in food-sharing vampire bats?

A few years ago, I was trying to record contact calls from hungry vampire bats. So put a caged hungry bat in a larger flight room with the other bats and put a microphone on it. I discovered to my surprise that other bats would feed these trapped individuals through the cage bars. At some point, this gave me the idea to do a small side experiment to test the idea that idea that risk increases nepotism.

To manipulate the perceived risks of helping, I created a novel “rescue” condition, where any donor vampire bat had to leave her warm, safe, dark, and comfy roosting location alongside her groupmates, then descend to an illuminated spot (vampire bats are very light phobic) where the trapped bat was stuck, and then to feed the trapped bat, she has to press her face to the cage bars (which sometimes makes her surroundings invisible) and regurgitate across cage bars. Compared to normal food-sharing, they don’t seem to like doing this. But they do it.

Sixteen of 29 bats were fed by others when trapped. They were fed by both kin and nonkin, but the degree of nonkin sharing declined quite obviously. All 15 starved bats that were tested in both trapped and free conditions received less food when trapped, and they received a consistently greater proportion of this food from closer relatives when trapped than when free. The vampires were more willing to feed mothers, daughters, and sons in the rescue condition. This is what we should expect if the bats’ nepotistic biases are exaggerated under dangerous conditions.

This paper was published in the journal Behavioral Ecology. Or if you lack institutional access you can get it from me here.

 

 

Posted in About cooperation, About vampire bats | Leave a comment

‘Team Vampire’ Fall 2016

Julia Vrtilek (Biology, Amherst College, 2015) is studying the development of grooming and food-sharing networks in young-of-the-year vampire bats.

What are your interests?
I find it fascinating and awe-inspiring that “from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved.” I’m interested in evolutionary biology, ecology, and animal behavior, as well as the latest thing I’ve read about in a recent cool article.

What do you hope to gain from working on the vampire bat project?
Primarily I hope to learn: about the bats, about research as a career, about myself. I’ve never worked with such a complex model organism before, and I know Gerry can teach me a lot about experimental design and statistics that I can use in my future work. I have mostly worked in microbiology, and the time has come to decide where I want to focus my future research. STRI is the perfect place for that; I am surrounded by smart, dedicated people who study all the things I’m interested in, and I hope to absorb enough about their work to help me concentrate my future efforts on my most enduring interests. I also hope to contribute to our understanding of reciprocity and cooperation!

What are your plans for the future?
This coming year, I expect to be working towards my Master’s degree in Zurich, and then I plan to proceed toward a doctoral degree.

Ellen Jacobs ( Ecology, Behavior, and Evolution, UC San Diego, 2016) is studying preference of young vampire bats for contact calls of mothers and other females.

What are your interests?
My primary interest is in animal social dynamics. I’m fascinated by the way that animals relate to each other, either in similar or totally different ways to humans. I’ve started focusing on acoustic communication, and I am very interested in the way that we can gain insight into the behaviors of different species based on their vocalizations. I am curious about the evolutionary and ecological causes and consequences of the ways that animals communicate. Ultimately, my interests are in understanding how different animals perceive and interact with the world and each other.

ellenjulia

Julia and Ellen

What do you hope to gain from working on the vampire bat project?
The vampire bat project is a great way for me to explore my interests in communication and social dynamics, because vampire bats have such complex social interactions. I’m learning a lot about how researchers study social interactions, which I know will be useful in my future studies. I hope to gain experience in designing and running research projects, as well as statistical analysis that I haven’t had a lot of opportunities to do before. I’ve also never worked with terrestrial animals before, as much of my background is in marine biology, so I am finding the differences between terrestrial and marine animal research very interesting. STRI and the vampire bat project are a great introduction into the world of biological research, so I’m trying to soak up as much as I can.

What are your plans for the future?
I’m hoping to begin a Masters in the next school year, then a doctoral degree with the intention of pursuing a career in bioacoustics.


Rachel Crisp (currently MSc student at Exeter with Lauren Brent) is studying female social rank in vampire bats.

What are your interests?
From molluscs to mammals, sociality has arisen multiple times with varying degrees of complexity throughout the animal kingdom, and we observe social strategies that are both divergent or convergent. I’m interested in what influences the formation and structure of animal social networks, and what it can tell us about sociality in general. In addition, I’m interested in the influence of parasites, mating systems, and dispersal on social networks, and how sociality can influence cognitive abilities.

What do you hope to gain from working on the vampire bat project?
Vampire bats are interesting because they share some convergent social traits with primates despite diverging 66.5 million years ago. In primates, social rank is well described and is an important way that individuals balance the social benefits of group living against the social costs of escalating aggression. Currently we know very little about intra-sexual competition among female vampire bats and whether they resolve this social conflict in the same way as primates: by forming a dominance hierarchy. I’m hoping to gain insight into whether female vampire bats form a social rank and if rank is associated with grooming and food-sharing social networks. I hope this will elucidate some unexplained variation in vampire bat cooperation and give some insight into how vampire bat social networks compare to those of other socially complex vertebrates.

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Rachel

What are your plans for the future?
I’m particularly intrigued by convergent evolution in social systems and behavior across taxa. The social behavior of squid is a neglected area of study that I think could provide us with an interesting comparative study for social evolution. I’m also interested in using the variation in sociality among cephalopod orders to study social evolution. Ideally I would like to combine these (still rather vague) questions in some way.

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“Prepared learning” in bats

I had a brief discussion with someone at the International Behavioral Ecology meetings about evidence in bats for prepared learning–the phenomenon that animals learn some associations faster than others. More importantly, the notion here is that animals learn things faster when those lessons would be most common and necessary in the environments in which they evolved.

The classic example is that a rat quickly associates feeling sick with a novel flavor of food, but it’s slower to associate feeling sick with a novel sound or sight [1]. Conversely, the rat learns faster to associate an electric shock with a novel sound or sight than with eating a novel flavor.

Most psychologists consider this quite special and call it an “adaptive specialization for learning” and even find it quite controversial or unbelievable [2]. I, on the other end of the spectrum, think most learning probably works this way. We just haven’t done enough studies on this topic which make that clear, because it’s difficult to show.

What’s truly impressive is that one form of prepared learning has been experimentally evolved in fruit flies  [3].

Two years ago, Dunlap and Stephens did a great experiment [3]. They created artificial worlds where flies were selected to learn to avoid an egg-laying site that was previously paired with quinine (which had been done before); and in addition to this, they created selection that favored learning some associations more readily than others.

To do this, they created two egg-laying sites that differed in both smell and color. In some worlds, the association of quinine with color was the best predictor of which type to avoid; in others the association of quinine with odor was most adaptive. That is, their experiment made one type of cue (odor or color) a more reliable indicator of flavor of quinine, which indicated that your eggs would not survive. In world 1, quinine was always indicated by the color of the food dish and odor was only half as reliable. In world 2, quinine was always indicated by an odor and color was only half as reliable. In worlds 3 and 4, both were either reliable or unreliable.  For 40 generations of evolutions, they allowed 10 populations of flies to evolve in each world. And yes, they found that when only odor associations were 100% reliable, the flies evolved increased sensitivity to learning the quinine–odor experience and reduced sensitivity to learning quinine–color. And the same was true for the other three worlds. In other words, these flies were born prepared to learn some things faster than others.

So there’s another reason to throw “nature vs nurture” out the window. In my opinion, natural selection doesn’t just give you the ability to learn, it gives you adaptively biased learning. Nature determines how you respond to nurture.

I really don’t think it could be any other way. You can’t build a general associative learning machine that pairs any information with any outcome based on repeated pairings. You can only build a machine that takes certain selection of sensory inputs and pairs those with other selected inputs to produce outputs. If A + B, then do C. But an animal has countless number of sensory inputs during every second of it’s life. Learning is always based on rules (about how to learn and what to learn) that are not themselves learned. So in some sense, it can be argued that all learning is in some degree prepared; it’s just a question of how much.

We can also see evidence for prepared learning in how animals learn today. Evidence for this comes from the niche-specific cognitive strategies hypothesis, put forth by York Winter, which predicts that animals feeding on stationary food like flowers (or that cache food in different locations [4-5]) will be faster to learn rewarded locations, whereas animals that feed on very mobile food (like insects) will be faster to learn rewarded sensory cues (like a visual cue for a predatory bird or an echo-acoustic shape cue for a predatory bat).

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The neotropical bat, Glossophaga soricina (shown left) feeds on both insects, fruits, and floral nectar, but it possesses morphological and cognitive adaptations for flower-feeding. These bats will revisit the same flower as many as 30 times in a single night [7]. As expected from the niche-specific cognition hypothesis, Glossophaga has an excellent spatial memory that can overshadow sensory cues [8-9]. The bats can learn a rewarded location instantly, but they cannot ignore location and learn only using shapes. Even when spatial cues to the location of food become unreliable, Glossophaga has great difficulty in learning to ignore location and use shape cues instead [8]. In a study by Stich and Winter [9], bats were presented with choice between two very different shapes, one rewarded and one unrewarded, and the arrangement of shapes were swapped from left to right (see image below).

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All you have to do is figure out that the sphere (left) always gives you food and the other shape never does. How long will this take you? 5000 trials and you still get it wrong 1 out of 10 times? WTF.

So all the bats had to do was learn to associate a shape with food. According to associative learning theory, this should be pretty trivial.

But here’s the shocker: In this simple task, Glossophaga required more than 5000 trials before reaching a criterion of 85% correct responses [9], because they could not ignore which side it was presented on. And when they were tested in a new experimental room, they forgot what they learned about shape in the old room [9].

This is astounding because we know that flower bats use shapes a lot to identify flowers and find flower openings. In fact, the shapes of some bat-pollinated flowers evolved to signal bats.

Learned spatial cues can even be more powerful than cues that are instinctually attractive. Many neotropical flowers that are pollinated by bats produce a compound called dimethyl disulfide, which is powerfully and innately attractive to these bats [10]. If you take a test tube of dimethyl disulfide into a cage of captive Glossophaga that have never smelled it before in their life, they will fly over and stick their head into the test tube. They love it even without any previous experience.

But once Glossophaga learns a rewarded location, their spatial memory will still overshadow their use of dimethyl disulfide. I did this experiment myself [11]. I was surprised. If you move a feeder over a few feet, they will fly  and hover at the blank spot on the wall where the feeder used to hang, before going over to the feeder clearly marked with rewarded smells and shapes.

The niche-specific cognitive strategy suggests that animal-eating bats should learn in a completely different way because prey don’t stay still. So sensory cues should be salient and learning food rewards based on sensory cues should be very easy for predatory bats. They should learn food-rewarded shapes or sounds faster than rewarded locations. And this seems to be true. Siemers [12] reported supportive evidence from a single insectivorous bat Myotis nattereri that quickly and easily learned to ignore location and associate shapes with food. They are the opposite of Glossophaga.

I  copied and pasted the relevant part below because this paper is hard to get online. I just love how Bjorn Siemers turned a possible mere anecdote into a nice little study using careful observation and on-the-spot experimentation. People who say you can’t really learn anything from a sample size of one, take note. He reports [12]:

…a female M. nattereri lost its balance and slid into a white round bowl next to the cage. The bowl contained about 250 mealworms. The bat grabbed a mealworm and flew off. The bat returned in a few seconds and approached the bowl, striking its uropatagium [tail membrane] against the rim of the bowl. The bat repeated the approach flight three times, retrieving one or two more mealworms. I then moved the bowl in the flight tent and started videotaping the bat’’s behavior. When the bat flew by the bowl at the new position, it hovered around it for 240 s without touching it. Over the next 60 min, the bat spent 650 s in eight 30 to 150 s long hover-and-attack- bouts above and around the bowl. The bat ‘attacked’ the bowl 101 times by touching the inner or outer side of the rim with its uropatagium. When the bat touched the inner side of the bowl, it sometimes successfully caught a mealworm in the uropatagium…

screen-shot-2016-09-11-at-7-52-00-pm…I then removed the bowl and put three alive and moving mealworms onto the smooth cardboard surface where the bowl had been. The bat inspected the site for 100 s without landing or touching the surface or catching any mealworms. When I placed the round bowl (now without mealworms) back onto the cardboard, the bat ‘attacked’ the empty bowl (13 times in 120 s). I filled the bowl again with mealworms and the bat ‘attacked’ the bowl another 28 times (three hover-and-attack- bouts with total duration of 180 s). Subsequently I initiated a choice experiment whereby at the opposite edges of the cardboard surface, the round bowl (empty) was presented simultaneously with the square one, new to the bat but filled with about 250 live mealworms. The rustling mealworms were clearly audible at least to my human ear from where the bat hovered over the experimental set up. The bat was tested during two hover-and-attack-bouts in this choice experiment (duration of bouts 110 s and 130 s, respectively). The position of the bowls was exchanged between the two bouts. While 20 ‘attacks’ were directed at the round, empty bowl, only two (unsuccessful) ‘attacks’ occurred at the quadratic one with mealworms (Fig. 1). The bat significantly preferred the empty [round] bowl as a target over the square one (χ2 = 14.7, d.f. = 1, P < 0.001). In the next night, I again presented the round, empty bowl on the cardboard. The bat ‘attacked’ three times in one 20 s hover-and-attack-bout and then lost interest

…After one accidental experience, an experimental bat learned to associate the round bowl with prey. The bat never attacked mealworms on the cardboard where the round bowl had been, and rarely did it look for mealworms in the square bowl that was unfamiliar to it as a feeding site. But the bat readily and repeatedly tried to retrieve prey from the round bowl, making attempts to take prey even when the bowl was empty. The evidence suggests that the bat was not perceiving the meal worms themselves but was operantly conditioned to the bowl as an indication of prey.

This finding was replicated and extended by Hulgard and Ratcliffe [13] who trained four additional bats of this species using rewarded styrofoam shapes hung from the ceiling.  All the bats learned to associate a specific shape with nearby food rewards and their shape training even seemed to overshadow their use of spatial memory.

So we have a flower-visiting bat that takes just one trial to learn a location and 5000+ trials to learn a rewarded shape, because spatial cues overshadow shape cues. By contrast, we have an insect-eating bat that takes just one trial to learn a shape, and once learned, this interferes with later spatial learning.

In the lab I’m currently in, Rachel Page has done a decade of research on how frog-eating bats use different cues and combinations of cues under varying contexts for finding their prey. But what we still need is one large comparative study using the same design across more species, as has been done with this massive comparison of cognitive self-control in primates [14].

Even better than just testing use of different cues (spatial, visual, echo-acoustic shape, smell, etc) would be testing the association rates between different cues and their natural outcomes. For example, a flower bat should readily match a location with either a food reward or an “escape-from-danger” reward (i.e. learn a hiding spot). In contrast, an insect-eating bat might more quickly learn to associate a location as a hiding spot than as a place to get food. Experiments like this would test that associative learning is influenced not only by the cue salience of the learner (determined by the ecological challenges it faced during its evolutionary history) but also on the ecological validity of the association itself (certain associations, like taste-sickness, simply make more ecological sense).

References

1. Garcia, John, and Robert A. Koelling. “Relation of cue to consequence in avoidance learning.” Psychonomic Science 4.1 (1966): 123-124.

2. Macphail, Euan M., and Johan J. Bolhuis. “The evolution of intelligence: adaptive specializations versus general process.” Biological Reviews of the Cambridge Philosophical Society 76.03 (2001): 341-364.

3. Dunlap, Aimee S., and David W. Stephens. “Experimental evolution of prepared learning.” Proceedings of the National Academy of Sciences 111.32 (2014): 11750-11755.

4. Clayton, Nicola S., and John R. Krebs. “Memory for spatial and object-specific cues in food-storing and non-storing birds.” Journal of Comparative Physiology A 174.3 (1994): 371-379.

5. Brodbeck, David R. “Memory for spatial and local cues: A comparison of a storing and a nonstoring species.” Animal Learning & Behavior 22.2 (1994): 119-133.

6. Clare, Elizabeth L., et al. “Trophic niche flexibility in Glossophaga soricina: how a nectar seeker sneaks an insect snack.” Functional ecology 28.3 (2014): 632-641.

7. Winter Y, von Helversen O (2001) Bats as pollinators: foraging energetics and floral adaptations. In: Chittka L, Thomson J, editors. Cognitive ecology of pollination. Oxford: Oxford University Press.. 360 p.

8. Thiele J, Winter Y (2005) Hierarchical strategy for relocating food targets in flower bats: spatial memory versus cue-directed search. Anim Behav 69: 315–327.

9. Stich KP, Winter Y (2006) Lack of generalization of object discrimination between spatial contexts by a bat. J Exp Biol 209: 4802–4808.

10. Von Helversen, Otto, L. Winkler, and H. J. Bestmann. “Sulphur-containing “perfumes” attract flower-visiting bats.” Journal of Comparative Physiology A 186.2 (2000): 143-153.

11. Carter, Gerald G., John M. Ratcliffe, and Bennett G. Galef. “Flower bats (Glossophaga soricina) and fruit bats (Carollia perspicillata) rely on spatial cues over shapes and scents when relocating food.” PloS one 5.5 (2010): e10808.

12. Siemers, Björn M. “Finding prey by associative learning in gleaning bats: experiments with a Natterer’s bat Myotis nattereri.” Acta Chiropterologica 3.2 (2001): 211-215.

13. Hulgard, Katrine, and John M. Ratcliffe. “Niche-specific cognitive strategies: object memory interferes with spatial memory in the predatory bat Myotis nattereri.” Journal of Experimental Biology 217.18 (2014): 3293-3300.

14. MacLean, Evan L., et al. “The evolution of self-control.” Proceedings of the National Academy of Sciences 111.20 (2014): E2140-E2148.

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