social bat .org

“Paying it forward” can help promote cooperation but not enforce it, because it does not prevent freeloading by itself.

“Direct reciprocity” occurs when individuals are more likely to help individuals that helped them previously, while “generalized reciprocity” (also called “upstream reciprocity“) occurs when individuals are more likely to help after they have been helped by any individual. So direct reciprocity is like “I’ll scratch your back if you scratch mine” and generalized reciprocity is like “pay it forward“. Although generalized reciprocity could be adaptive, this behavior could also be simply a nonadaptive byproduct of direct reciprocity. For example, a predisposition to caring about baby animals could be seen as a maladaptive byproduct of selection for caring about one’s own baby, and similarly, generalized reciprocity may result completely from selection for direct reciprocity. But others think generalized reciprocity may be very important in some animal societies because it poses fewer cognitive demands.

Unlike direct reciprocity, generalized reciprocity cannot stabilize cooperation all by itself, because there’s no way to prevent cheating in a well-mixed population.

I recently received an email asking how I distinguished between evidence of direct and generalized reciprocity in vampire bat food sharing. The email also pointed out that a minor error (when stating that I found no evidence of generalized reciprocity, I mistakenly referred to the supplementary materials even though supporting evidence was in the next few lines).

My reply was very long and spread across two emails, so I’m copying it below. I’ve added links to references where appropriate.

Hi Dr. Taborsky,

Thanks for your interest in our paper. I’m a big fan. I have been following your lab’s work on cooperative breeding in cichlids and generalized reciprocity in rats.

I’ll answer your second question first: “food received” in Fig. S4 refers to food received from a particular partner (not in general).

For your first point, I’m sorry for the confusion. The results supporting that statement are actually the sentences directly following and not in the supplement. I’m a bit embarrassed to say that I believe it’s a mistake. This text was moved to the supplementary materials at some point to ensure meeting the page limits, then they were moved back to the main text (so the reference to the supplement is mostly unnecessary). Here’s that text again:

Donation sizes could sometimes be compared both before and after the donor was fed within a round of trials. In these 28 cases, we failed to find a difference in presence of food sharing (paired t=0.98, df=27, p=0.34), total food donated (paired t=-1.3, df=27, p=0.20), or food donated per recipient (paired t=0.16, df=27, p=0.87). When the donor was fed on the previous day, we found no difference between the amount donated on that day compared to the donor’s average on other days (n=9 donors and 9 trials, paired t=-0.013, df=8, p=0.99).

However, there are some additional relevant things that you can get from the food sharing matrix in the supplement. For example, one can easily test if — among bats that both gave and received– overall food received predicts overall food given, which is consistent with generalized reciprocity. After log-transforming the data, there is a weak but NS trend between total help given and total help received by bats that did both (R-squared = 0.19, p=0.09). See correlation pictured below.

Correlation between overall food given and overall food received among bats that both gave and received

Some thoughts on evidence for generalized reciprocity in the study
I’m certainly interested in looking further at the role of generalized reciprocity in the vampire bats. Although I failed to find evidence that bats donated more often after they had recently received, my sample size was very small, so the effect of generalized reciprocity would have had to be substantial to be detected. Bats can certainly act as donors after being fasted and fed the previous night. My expectation was that the bats would be more likely to feed others after being a recipient in a trial. There’s actually two reasons for this. The first is the possibility of generalized reciprocity (bats might be more likely to share with others after having just received recently). The second reason is that the fasted bats always fed immediately after the food sharing trial (after all the other bats had already fed), and so of all potential donors for the next night, the previous day’s recipient had fed most recently, usually a large amount. However, I did not find any support for that prediction as I explained in the paper. I will expound on this in case it was unclear.

After a bat was fed by others, I found no subsequent change in the amount or probability of their subsequent food donations. There were 28 cases where a bat had opportunities to feed others before and after it served as a subject within a fasting round. When I compared food sharing before and after the donor was fasted, I found no significant difference for the total amount of food given by the donor, the amount of food given per recipient, or the probability of giving food during a trial. There were also 9 bats that donated to others the day after they were fed. In these 9 cases, the mean sharing on days immediately after being fed (327.6 s) did not exceed the mean sharing on other days (328.4 s). Of course, these sample sizes are also very small (and yes, I did just now see your editorial Ethology paper on sample sizes!). Basically, our data do not make a strong case for or against generalized reciprocity as a factor in food sharing, and of course we did not test the effect of anonymity and compare it with trials showing reciprocity (as you did with the rats). We did not find strong evidence of it.

Our data do not actually provide conclusive evidence for or against direct reciprocity either in my opinion. We are in the process of organizing more controlled tests in a lab setting to address this. A major advantage of working with vampire bats is that no training is required for the bats to share food, but the huge difficulty has been getting them into our lab. I have spent the majority of my PhD trying to do this, with limited success. I just brought my first group of 7 bats here 10 days ago.

Some thoughts on generalized reciprocity as an evolutionary explanation for food sharing
I think my results disprove the harassment idea and the idea that non-kin sharing only occurred due to a lack of kin presence. However, distinguishing between direct reciprocity and kin discrimination based on familiarity is far more difficult. Unlike these alternatives, I don’t consider generalized reciprocity to be a stand-alone alternative explanation, but rather as a probable supplementary mechanism, i.e. an additional source of information for decision-making as outlined by your “hierarchical information hypothesis” (Rutte and Taborsky 2008).

I don’t think generalized reciprocity can by itself explain food sharing in vampire bats because of the instability of roosting group membership. The vampire bat social network involves a lot of roost switching. As your lab showed previously, generalized reciprocity works well in stable groups of 3 where the actions and outcomes of generalized reciprocity are the same as direct reciprocity 50% of the time. (i.e. if you return anonymous help in a group of 3, there’s a 50% chance you are directly reciprocating).

However, generalized reciprocity strategies are self-promoting via passive positive assortment (or spatial selection, population viscosity, limited dispersal, or whatever you want to call it), so generalized reciprocity starts to breakdown with more social mixing. You showed this mathematically, but I think its also logically intuitive. Hence, indiscriminate helping towards with groupmates (whether interpreted as kin selection or equivalently multi-level selection) and indiscriminate helping based on past anonymous help both make the same assumptions and predictions when considered as a stand-alone explanation for cooperation. The assumption is that enforcement is not required due to population viscosity. And the prediction is that the animals should not be basing helping acts on individual discrimination of any kind.

Conclusion

Generalized reciprocity would be neither necessary nor sufficient to stabilize cooperative food sharing in vampire bats. In contrast, the other alternative mechanisms I discussed (e.g. enforcement via direct reciprocity or kin selection via limited dispersal or via nepotism) could in theory explain food sharing by themselves. That’s why I looked for observational evidence of generalized reciprocity, but dismissed it as an alternative explanation.

I think multiple factors and their interactions are at work, and I suspect generalized reciprocity probably helps promote cooperation alongside the other more key drivers. Indeed, before I started in his lab, I emailed Jerry Wikinson and noted that in his original 1984 small captive trials, there were 2 cases where starved bats were not fed by reciprocators and in both cases, the donors were the bats that had just been fed (by another bat) in the last trial. So generalized reciprocity has been on my mind since the beginning, but I have not find any real evidence for it yet.

Best
Gerry

Finally!

The bad news is that there are only 7 bats, rather than the 15 for which I was waiting, or the 30 for which I was hoping. Still, after 4 years of persistent effort, it feels nice to have any sort of success at getting bats into our lab. The population of vampires at Organization for Bat Conservation (OBC) has been booming with 9 new young of the year, but Chicago Brookfield Zoo had lost about the same number of bats this year before they gave me the 7 remaining females. So that worries me a bit.

After leaving Michigan, I drove the bats from Chicago to University of Maryland on March 7, arriving around 1 am on March 8. The car was 75 degrees inside and full of soaked rags to keep the humidity high. I’m hoping to genotype them and estimate their relatedness to the OBC bats in the next few days.

Cooperative behaviors, such as food sharing, can be studied under a spectrum of conditions from completely natural to very artificial. For example, a careful observer in the field can measure the extent to which male chimpanzees will share meat in the wild after a hunt, or an experimenter in the lab can test the extent to which two chimpanzees in separate cages will pass food to each other by operating a simple mechanical device (like pulling a tray that delivers food to another individual).

There are clear pros and cons to each of these approaches, and each will give you different sorts of information about the animals. For example, field observations of cooperation, albeit natural, won’t allow you to manipulate the situation very much, and often cannot show you what enforces cooperation (i.e. what protects it from freeloading). On the other hand, controlled studies in captive settings won’t necessarily elicit the natural evolved behaviors in which we are all interested. So, for a given helping behavior in a given species, it would be interesting to see what happens when natural forms of cooperation are tested under artificial conditions.

I asked this question in vampire bats by testing if vampire bats would still share food if they had to pass it through a barrier– the metal bars of a cage. This is, of course, a completely unnatural situation. Normally, the bats groom each other awhile before regurgitating food. But if the bats are motivated to feed another individual and not just responding, perhaps they will adapt their food sharing behavior to the novel situation.

After first observing that wild vampire bats will feed unfed individuals inside their roosts, Wilkinson began inducing food sharing by keeping a bat from feeding overnight, first in the wild and then in captivity. For the past couple of years, I have been doing similar trials many times with captive vampire bats at the Bat Zone in Bloomfield Hills, Michigan. This has allowed me to map out the food-sharing network in a group of common vampire bats with varying relatedness but that all know each other equally. One of the things that surprised me is that the majority of the donors approach the hungry bats, not vice versa. This led me to believe that food sharing could not be explained as merely a response to harassment, something which you sometimes see in primates.

In the last couple of weeks, I’ve been placing the hungry bat first inside a small cage in the corner of the larger walk-in colony flight cage, before releasing it into the colony cage. Not only is having to feed a trapped bat across a barrier a novel situation, but the donor and recipient would not be able to groom each other beforehand. This is relevant because Wilkinson speculated that social grooming might allow the bats to detect cheaters by feeling the fullness of a partner’s belly. Also, a trapped hungry bat would not be able to beg or solicit a food donor. Any donating bat would have to willingly fly across the flight cage in order to feed the hungry trapped individual. For all these reasons, I was highly skeptical that this would work, but I thought it was worth testing (my main goal here was to record social calls and get fresh DNA).

Much to my surprise however, when an unfed bat was trapped in a wire cage, other individuals would sometimes come down and regurgitate food to this hungry bat by pressing their face against the metal bars. It was not so surprising that mothers sometimes did this for their grown offspring, but I was more surprised that the adult offspring would also sometimes pass their food across the cage wall to their mothers. Also noteworthy was that the food sharing across the cage wall barrier was much less common than the more natural form of food sharing– hanging belly to belly with copious social grooming before and after. Whereas the natural form occurred for almost every subject, only a few bats regurgitated small amounts of food across the metal bars of a cage.

To me, this demonstrates that even though a given species might often share food in nature, if you make the sharing behavior more difficult or artificial in a lab environment, they might not cooperate as much or even at all. It may also be true that animals that normally would not share food under natural circumstances, might then actually do so under certain lab conditions, for example, if they learned how to obtain a food reward by cooperating during the course of the experiment. This would be simply operant conditioning, not a reflection of whether this species was particularly social or predisposed to cooperation. So caution must be used when interpreting the results of such experiments.

New paper available here

Key points

• We re-examined the well-known but controversial case of reciprocal food sharing in vampire bats. What factors predict the decisions of vampire bats to donate food to hungry roost-mates?
• In collaboration with the Organization for Bat Conservation, we collected a larger sample of food sharing data than ever before under controlled settings. We show that this extreme but natural form of cooperation cannot easily be explained by nepotism or harassment– as argued by some recent high-profile review articles and books.
• For vampire bats that are equally and highly familiar, reciprocal sharing and social grooming were both better predictors than genetic kinship for the amount and likelihood of food sharing.
• Surprisingly, donors “voluntarily” initiated the majority of food sharing events, even with non-relatives. Persistent begging was not required.
• Food sharing appears mutually beneficial for donors and recipients. If so, additional controlled experiments are needed to confirm exactly how the bats’ individual behaviors collectively prevent “cheating” and an evolutionary “tragedy of the commons“.

Yep, that’s a corny Christmas reference in the title… A recent paper compared the hearing sensitivity of common vampires with other bats. We humans can hear from about 20 Hz to just under 20,000 Hz (20 kHz). Here, listen:

Vampires like other bats have excellent high frequency hearing. Anything above about 17 kHz starts to sound like weirdly uncomfortable silence to us, but  a vampire bat can hear well up to 113 kHz. They need this ultrasonic hearing of course to analyze the echoes of their biosonar calls. As you would expect, vampire bats have excellent hearing in the range in which they echolocate (about 70 kHz).

The echolocation ability of vampire bats is comparable with other bats. If you strung wires throughout a room without light, vampires would be able to avoid wires as thin as 0.5 mm, albeit they might need several trials of practice before they can maneuver adeptly around 0.25 mm wires (source). This performance is on par with larger bats, but exceeded by smaller aerial insectivores*.

What’s particularly unique about vampires, though, is not their high frequency hearing, but rather their low frequency hearing. The authors of this study confirmed that- as far as we know- common vampires can hear the lowest frequencies of any bat, including the big Paleotropical fruit bats that don’t echolocate at all. At 60 dB, a common vampire bat can hear sounds as low as 716 Hz. Now, to us that doesn’t sound very low. See (er, hear):

The vast majority of bats could not hear that tone. In fact, no other echolocating bat can hear well below 1,500 Hz. Next, consider what 250 Hz sounds like to us humans:

For a bat, that is infrasonic, way too low even for a vampire bat. They can’t hear that sound even when it is broadcast at 80 dB SPL (think really loud vacuum cleaner). That means that when I’m holding a struggling vampire bat and talking to it in a quiet, soothing, and re-assuring voice, they hear none of that. Oh well.

Still, a vampire’s hearing limit is more than an octave lower than other Neotropical leaf-nosed bats. In fact, common vampires have better low-frequency hearing than the Virginia opposum. While bats can’t hear bass, they could feel vibrations of intense low sounds with their bodies.

Vampire bat sensitivity for low frequencies seems to be a special adaptation. One piece of evidence for this is the fact that the hearing sensitivity of the common vampire at decreasing frequencies looks somewhat normal until it hits 5 kHz. Below that point, the sensitivity suddenly jumps up, beyond other bats. So, interestingly, vampires can hear 4 kHz better than 5 kHz. Then with even lower frequencies, the bat continues to lose sensitivity… until 2.4 kHz where, again, the sensitivity of the vampire ear jumps up again to another high point at about 2 kHz. These strange peaks indicate that vampire bats might have some kind of yet-undescribed mechanism that gives them improved low-frequency hearing.

Why do vampire bats have such good low frequency hearing? Check out this paper entitled “Classification of human breathing sounds by the common vampire bat, Desmodus rotundus“

To summarize, in the authors’ words:

a common vampire bat’s ear

The current behavioral study shows that the common vampire bat, Desmodus rotundus, is very sensitive to breathing sounds. In the three-alternative, forced-choice setup, it spontaneously associates unknown breathing sounds with the subject who emitted them. This exceptional performance is underlined by the inability of human listeners to match the vampire bats’ accomplishment under the most difficult experimental condition where the sounds had been recorded under physical strain. Numerical simulations show that while the human listeners relied on breathing-frequency information, the vampire bats appeared to recruit different acoustic parameters and to choose amongst these parameters depending on which provided the highest discriminative power. On the basis of these findings, it is suggested that vampire bats can memorize and classify complex acoustic features of prey-generated breathing sounds to facilitate the identification of prey animals that they have successfully fed on before.

Most bat ears are tuned to hear their prey, and in this case, vampire bats prey on large animals that make low pitch breathing sounds. To us, breathing might seem too low pitch, but  it actually produces faint sounds at high frequencies:

human breathing extends into frequencies that we cannot hear

Not only can the bats learn what their prey sound like, but they can even learn particular host individuals. This might be why a vampire bat will sometimes bite the same individual in a group night after night regardless of where they are sleeping amongst others. Perhaps the bats can identify their favorite host by their breathing pattern alone.

In general, bat ears are not only tuned for hunting and echolocation, but also for communication. Like other bat species, vampires have a number of social calls. All bats locate  and recognize their pups  using isolation calls**. Adult vampires also produce contact calls that sweep from  about 36 kHz down to 19 kHz, with most of the sonic energy at 20-25 kHz. Vampire pup isolation calls are even lower, perhaps so that they travel farther at lower intensities. The frequency that vampire bats hear best at is 20 kHz, right beyond our limit, and the same pitch as the isolation calls of their pups:

Footnotes:

* Rhinolophus ferremequinum can detect wires as thin as 8/100th of a mm.

**These low frequency pup calls were first described in detail by Ed Gould, whom I’ve had the pleasure of getting to know in person because he volunteers at Our House center for youth. He now crafts amazing pottery and keeps himself quite happily busy. Ed’s student Dennis Turner did some of the earlier foundational field studies on vampire bats in the early 70s.

The poster below was the winner for the University of Maryland Bioscience Day 2012 Poster Competition for the category Biodiversity, Conservation, Ecology & Evolution, and Environmental Science. More importantly, it summarizes the findings in a recent manuscript we submitted.

Click to see full size

Micah Miles

Third year, Banneker-Key Scholar, concentration in Wildlife Ecology and Management

I fell in love with animals at a very young age though dozens of wildlife documentaries, volumes of nature books, and copious visits to the National Zoo. As an Environmental Science and Policy major I seek to better understand the ways in which animals rely on their surroundings and use this ecological understanding to minimize anthropogenic biodiversity decline and habitat fragmentation. In the last few years I have read books about bats and visited a bat museum in Costa Rica so when the opportunity to study social behaviors in vampire bats presented itself, I flew at the chance. Working as an undergraduate research assistant also provides a comfortable setting for my first attempts at my own individual research. Since I plan on attending graduate school, developing research experience is a top priority. After receiving a master’s degree I want to work in wildlife management, functioning as an intermediate between the science of animal interactions and the policy that shapes our influences on their survival. In my free time, I enjoy books, classic movies, and questing through D.C. in search of the perfect bakery.

Lauren Leffer

First year, Banneker-Key Scholar, specialization in Ecology and Evolution

What are your main interests? Outside of eating, breathing, and sleeping I enjoy studying evolutionary biology and animal behavior (specifically animal cognitive ability, and social structure). I am also interested in environmental conservation, creative writing, and entomology.

Why did you choose to apply for this position as an undergraduate research assistant? As an incoming undergraduate freshman, I knew I wanted to start making research connections right away, and to get some idea of what I’d actually be in for, pursuing a career in biology research/academia. I was already very familiar with (and interested in) the existing research on vampire bat social behavior (because like any normal teenager, I spend significant amounts of my free time reading biology publications), and as soon as I saw the want-ad on the daily list-serve, I had to apply. It’s still pretty hard to wrap my head around the fact that I’m working on the type of research I’ve been reading about for years, and I couldn’t be more excited to have this chance.

What do you plan to do after college? I plan to enter the cycle of never-ending graduate programs, with aims of performing evolutionary biology and animal behavior research. I’d also like to travel a decent amount.

What do you do for fun? Science, cook, run, hike, go outside, read, write, draw, and talk to people.