Rachel Crisp is currently writing her masters thesis on dominance interactions in female vampire bats. Males have a clear dominance hierarchy in competition over roost territories, but do the female vampires have a dominance rank? If so, does it strongly correlate with cooperative interactions? Her work should come out next year!
Despite all the work on cooperation, not much is known or published about competitive interactions in female vampires. Interestingly, female vampire bats are larger than males, but there is no evidence for a strong female reproductive skew as in cooperative breeding societies. The little bit on competitive interactions that is available is in German (work in the 1970s supervised by Uwe Schmidt) or Korean (by Shi-Ryoung Park). Rachel Moon graciously translated this 1988 paper by Park from Korean to English.
For easy accessibility, here it is below.
Dominance relationships in a colony of vampire bat, Desmodus rotundus
Park, S.R.
Korea National Univ. of Education, Chongwon (Korea R.). Dept. of Biology
Translated by Rachel Moon, Harvard University
Originally published as Park, S. R. (1988). Dominance relationship in a colony of vampire bat, Desmodus rotundus. The Korean Journal of Zoology. 31 (4): 243-250.
ABSTRACT
Dominance relationship was investigated in a captive of Desmodus rotundus, a neotropical sangivorous bat, under seminaturalistic conditions. The hierarchy was determined from four different behaviors (flee, fly-out, avoid, wait) by the encounter of two adult bats on the feeding site. The aggressive action “flee after fighting” was relatively low (16%) compared to the other three observed behaviors. A hierarchy of the females was reflected sometimes in the feeding order. The harem male dominated the non-harem males and exhibited his territorial behavior. However, to his female partners he didn’t show aggression.
INTRODUCTION
Except for a few species, most bat species (Chiroptera) live socially (Gopalakrishna, 1955; Eisentraut, 1957; Kulzer, 1958; Goodwin and Greenhall, 1961; Barbour and Davis, 1969). Bats exhibit complex social structures and diverse kinds of social behavior (Bradbury, 1977). However, the functional significance of bat social structure and social behavior is still not well studied; therefore, this study aims to understand the significance of complex social behavior of bats by studying dominance relationship in a group of South American neotropical vampire bats (Desmodus rotundus).
Vampire bats (Desmodus rotundus) have developed and adopted unique behaviors and physiological structures that enable them to feed on the blood of vertebrate animals. Vampire bats form long-term small colonies with highly developed social structures (Wimsatt, 1969; Schmidt et a., 1978; Wilkinson, 1985). Until now it has been nearly impossible to study dominance relationship structure of vampire bats in natural settings; therefore this study aims to investigate dominance relationship in a group of vampire bats in experimental settings that resemble naturalistic conditions.
MATERIALS AND METHODS
This study was conducted with 9 vampire bats (Desmodus rotundus; three males, six females). Only one male and one female were captured in the wild (Colombia, 1975), and others were born and raised in captivity. The bats were kept in a thermostatic chamber (with 12h/12h of light and dark) at a temperature of 25C and 70% humidity. They were provided cow or pig blood (with removed fibrin) on a bird water feeder. In order to distinguish each individual from another, I marked each bat by attaching aluminum loop of different colors on its forearm (Table 1).
The observation cage had a size of 250 x 180 x 100 cm, and its left side, right side, back side and ceiling were made with thin plastic surface with small holes so that the bats could hang easily. The front center part of the room was made with transparent glass (100 * 50 cm) so that the experimenter can observe easily.
In order to observe the bats’ behaviors, an infrared night vision scope (metascope 9902E) was used, during early hours (17:30-20:30) of the 12 dark hours. This study emphasized an understanding the quantitative aspects of behavior observed in a previous study of vampire bat social relationship (Schmidt and Manske, 1973). In other words, I recorded and analyzed frequency and duration of observed behaviors, distribution of behaviors, and subsequent behaviors.
Table 1
RESULTS
The social behavior of bats takes place at a feeding site, where they often encounter one another. During the initial period of feeding time, aggressive physical fights were often observed. This behavior usually begins with two bats pushing and shoving each other. If the opponent does not back off immediately, this aggressive physical fight occasionally turns into a fierce combat. To first determine the feeding dominance relationship of bats in the colony, we investigated the feeding times of individual bats, as seen in Figure 1.
Figure 1
D (female) always feeds first; this female kept her place until she was full, even though other younger bats who were feeding at the same time often obstructed her by physical fight of pushing and shoving aside (Figure 2A). H (female) always showed up at the feeding site after the first feeding activity period, when other bats were mostly not feeding. During this period, H often encountered her 15-month-old daughter J at the feeding site. J would often push H to the side, although J had several unoccupied feeders nearby. Then J would wait right behind her mother H until H finishes feeding and returns (Figure 2B). As soon as H left the feeding site, J started to feed at the same spot H was feeding.
Figure 2 (sadly unclear) and Table 2
However, not all of the other colony members ate their meals following such straightforward feeding order. Depending on each feeding site situations (whether bats are at the feeding site or not, and if so which bats are present), the bats visited the feeding site at irregular intervals. Therefore, it was difficult to determine group dominance relationship solely based on feeding order. Because the bats frequently encountered different individuals at the feeding site, it was possible to observe several types of social behavior. I chose four different types of social behavior exhibited by two encountering bats as the main parameter to determine bats’ dominance hierarchy.
Fleeing is exhibited after aggressive behavior, whereas fly-out, avoid, and wait behaviors are “direct-flight” behaviors performed by inferior bats themselves in order to avoid potential conflicts; therefore, these three types of behavior are characterized as unaggressive or submissive behavior.
A total of 294 encounters were observed at the feeding site, and the frequency of each behavior type is shown in Table 2. Aggressive behavior accounted for 15.6% of all observed behaviors, which shows that it happened relatively less frequently than unaggressive behavior (Figure 3). Aggressive behaviors between male bats at the feeding site rarely took place; the most common behavior between two encountering male bats was “fly-out” behavior, which accounted for half of all behaviors exhibited.
In order to determine dominance relationship, I used a point system in which the superior (winner) bat earns 1 point when superior bat and inferior (loser) bat are distinguished. The score difference between two bats is shown in Table 3 by comparing the scores of each bat. Using this result to build a sociogram of dominance hierarchy at the feeding site, the following phenomena in each group could be explained.
Dominance relationship among harem females (Figure 4)
When encounters took place between two females from five harem females, the most common social behaviors were “wait” and “avoid.” D was the most superior dominant bat among five harem females. B, who had the lowest dominance hierarchy ranking, exhibited “wait” and “avoid” behavior as a response to D’s behaviors. E had a middle dominance hierarchy ranking, which was higher than inferior bats C and B and lower than superior bats D and H. E responded by “fly-out” behavior all three times when she encountered H. Although I never observed direct encounters of H and D at a feeding site (their feeding period almost never overlapped), I concluded that D had a higher dominance hierarchy ranking than H depending on feeding ranking.
Table 3, Figure 3, and Figure 4
Figure 5
Dominance relationship among males (Figure 5)
When two out of three male bats (G, A, F) encounter at the feeding site, the inferior bat usually flees away. Thus a clear dominance hierarchy was revealed among these three males. The most superior bat was G; whenever A or F appeared at the feeding site, G forced them to leave the site. When G approached, the inferior bats rushed their feeding. The most inferior bat was F; whenever F was feeding, I often observed him looking around his surroundings and rushing his feeding. Similarly, A also exhibited typical feeding behavior of inferior bats, which was carefully approaching feeding sites, quickly feeding non-stop, and leaving in a hurry.
Out of 31 encounters between G and A at the feeding site, A showed “fly-out” response 26 times; of 42 encounters between G and F, F responded by flying out 32 times. Out of 12 encounters between A and F, F exhibited “fly-out” behavior in all encounters. Therefore it was determined that the most superior bat was G, the most inferior bat was F, and A was in the middle.
Dominance relationship among male bats and harem females (Figure 6)
At the feeding site, G (male) always showed passive behavior towards old harem females who have previously given birth to pups. When these females were feeding at the feeding site, G responded by exhibiting “wait” behavior 30-40 cm away from the site until the females finished feeding. I observed six encounters between G and B (female who hasn’t yet given birth), and four out of six times B showed submissive behavior (“fly-out”) towards G.
A (male) showed dominance towards B and C (females); however, the number of encounter between A and D or H (females) was too small to clearly determine their dominance hierarchy.
F (male) was certainly superior than B and C (females), who had low dominance hierarchy rankings within harem females. However, he ended up getting an inferior status after frequent pecking-order disputes with other harem females. His dominance hierarchy ranking was determined by his fights (“fleeing”) with other females, which were 19 times (73%) out of 26 encounters.
Figure 6
DISCUSSION
Vampire bats (Desmodus rotundus) form small groups when they go out to feed in the wild. Greenhall et al. (1969) observed behaviors such as combats, waiting, and co-feeding when vampire bats were feeding in groups in the wild. Furthermore, even in captivity the vampire bats often engage in pecking order disputes at feeding sites; therefore, the social structure based on dominance hierarchy seems to be a prominent characteristic of social behavior of vampire bats (Schmidt and Van de Flierdt, 1973). Vampire bats maintain close relationships through various social interactions at feeding sites, such as combats and submissive behaviors. According to the results of this study on a captive group of vampire bats, aggressive behavior (16%) took place less frequently than unaggressive behavior (submissive behavior), and most of the bats showed defensive or submissive behaviors (wait, fly-out, avoid) at the feeding site.
Park (1986) reported that aggressive behaviors are usually triggered by subadult bats, showing a strong tendency to claim high dominance status. Park observed that bats who are 14-16 months old often engaged more in dominance ranking fights compared to adult bats. The results of this study also revealed that group members abide by dominance hierarchy through a single consistent order when feeding and that aggressive behaviors between adult bats at feeding sites did not occur as often. Thus, it can be thought that vampire bats have especially well-developed mechanism of group formation, which serves to restrain mutual aggression by strengthening the cohesiveness among group members.
Vampire bats form a typical harem social structure (Load, 1976). Such social structure has been observed in other bat species such as Pipistrellus nanus (O’Shea, 1980), Phylolostomus hastatus (MaCreacken and Bradbury, 1981), Carollia perspicillata (Porter, 1979), and Artibeus jamaicensis (Morrison, 1978); the male bats in these species also form a single distinct dominance hierarchy, which is observed by ritualized combats. Park (1986) found out that alpha male (harem male) vampire bats stayed with females for a long period of time, whereas beta males stayed at a place where females use as their temporary shelter. On the contrary, gamma males stayed far away from female groups and did not exhibit any territorial behavior. Connecting to the results of this study, it seems that hierarchy system of male vampire bats is associated with territoriality. In the context of dominance behavior, Wicker and Uhrig (1969) observed Lavia frons engaging in a territorial fight with neighboring bats, and Bradbury and Emmons (1974) witnessed Saccopteryx leptura driving out outsider bats from its hunting territory. Several other bat species (Vespertilionidae: Dwyer, 1970; Brosset, 1976; Phyllostomatidae: Fenton and Kunz, 1977; Porter, 1979) are known to defend their harems and exhibit territorial behavior towards intruders and competitors.
Sex and age of bats are significant factors in formation of dominance hierarchy. Usually, older animals show dominance over younger animals, and males show dominance over females (Immelmann, 1983). This study reveals that alpha males (harem males) did not exhibit absolute dominance over females; on the other hand, harem males exhibited inferior behaviors toward their female partners. It is not easy to declare dominance relationship based on age only with the results of this study. Whether juvenile bats depend on dominance hierarchy rankings of their mother bats require further investigation.
References
New timeline
Recent and relevant papers
With my new lab starting in Fall 2018, I am now interested in prospective graduate students and postdocs. More information on how to apply here. Below are some of my thoughts and advice on applying to graduate schools and being a graduate student.
Check out this advice written by wiser people than me:
On choosing a graduate program
Rather than basing your decision on the prestige of the school, choose a good lab (research group led by a PI). The best schools tend to have better labs but not always, and the most prestigious schools might have a more competitive atmosphere, which may or may not be your thing. Schools can specialize by hiring several excellent faculty in a specific area, such as animal behavior. For example, University of Texas Austin and University of California Davis have two of the best animal behavior programs in the world, despite not being as famous as Harvard or Oxford. The name of the school does matters and so do the other labs in your department, but for a research career in our field, what matters most is the quality of your papers not the prestige of the school. So the question should be: which lab will help me do my best possible work?
A good place to see a bunch of labs at once is to go to a scientific conference. Don’t be afraid to ask a senior grad student or postdoc: If you were me, what lab would you join?
Don’t apply to the school until you’ve talked with the PI. Also, talk to at least three people in the lab and ask them what the PI is like. Are they hands-off or demanding? What are lab meetings like? How quickly do they respond to emails? Ask them in a way and in a setting where they can be totally honest. Expect to hear different things, but look for common themes.
The PI matters a lot, but so do the other lab members. You’ll probably spend more time with them than the PI. So try and evaluate about the culture of the lab. If the PI has a very large lab, see if there’s a postdoc that could be your direct mentor.
On doing a masters before a PhD
In some countries and at some schools, getting a masters before a doctorate is mandatory, and I think there’s actually some sense in this. But many undergraduates in the USA who want to do a PhD in biology think getting a masters in biology does not make sense and is a waste of time. I’d like to present the counter-argument. There are two good reasons to get a masters before a PhD.
First, doing a masters puts you one step ahead when you start your PhD. Becoming a good scientist typically takes a long time. Many students think that a masters degree puts you two years “behind” but it actually puts you two years ahead, because a masters is like a “practice PhD”. You’ll get better at critical reading, writing, and statistical analysis. If all goes well, you publish a paper, maybe even two. When you start your PhD, you’ll be a better researcher than you would have been coming straight from your undergrad. A 2-year MSc degree can even put you on track to get your PhD two years earlier, or get you a faculty interviews as postdoc two years earlier.
One secret to success in academia is trying to be one step ahead of where you need to be at each stage of your career. As an undergrad, that means publishing a paper. As a starting PhD student, it means having a compelling proposal to apply for fellowships. As a finishing PhD student, it means establishing yourself as an international expert on the topic of your dissertation. As a postdoc, it means laying the foundations for a fundable long-term research program. At each stage, you will not be compared to others based on your age. So while impressive, there’s no real long-term advantage of being a 24-year-old with a PhD. Instead, you’ll be competing for funds with others at the same career stage, based on what you’ve done so far. My point is that what you know, and what you’ve done, are more important than how quickly you get various degrees.
Second, doing a masters gives you time to decide if academia is right for you. Being a research scientist in a field like behavioral ecology is one of the most creative and intellectually stimulating jobs one can imagine. If I had a million dollars, almost nothing about my work life would change. But science is truly a “labor of love”, and academia is neither the fastest nor easiest path to securing a permanent, stable job. For instance, 12% of college baseball players go on to play in the major leagues, whereas only 10% of incoming biology PhD students become biology professors. As an undergrad, you can get a pretty rosy picture of academia talking with professors. There’s survivorship bias: the people who tell you about academia as a career are the few people who succeeded in it through some combination of talent, perseverance, and luck. Professors are not a random sample of grad students; whereas many grad students suffer through graduate school, many professors look back at their grad school years with sweet nostalgic memories of having the time to focus solely on their research. It’s easy for professors (especially older professors) to think, “I simply did X, Y, and Z and that’s how I became a professor”, but today, the statistics for becoming a professor are actually a bit grim. Each year in the USA, there are 16,000 new biology PhD students. Of those successful recruits, 63% get their PhD, and the average time to that degree is 7 years. Of those graduates, 70% get a postdoc and of those postdocs, 30% get a second one. Only 15% of postdocs get a tenure-track job within 6 years (~13 years after receiving a PhD). Most starting PhD students in biology in the USA want to be a tenure-track professor. But only about 7% of them actually get that job.
If you’re unsure about doing a PhD, just ask yourself this question: if you knew you had a zero chance of getting a faculty job, would you still want to spend 7 years doing a PhD just for the experience itself? If the answer (as it would be for many of us) is: “Yes! I love doing research“, then of course do a PhD! You cannot lose. If you’re unsure, then perhaps consider a masters instead. Then, you’ll be in a better position to know whether to commit to the longer academic journey, complete with greater expectations, fewer deadlines to structure your time, and an extra dose of imposter syndrome. Some starting grad students realize that they don’t want to be in academia in the middle of their PhD, but it’s difficult psychologically to quit and do something else that makes you happier. That transition can feel like failure. In contrast, you can always turn a MSc into a PhD, and if you start with the goal of getting a masters, you can leave with a masters and that is a great success. It’s a way to test the waters.
On writing research proposals
Brainstorm a list of topics and questions that are truly interesting to you. Study the most fascinating topic you can. Read the literature, but don’t let the literature tell you what questions are interesting. That is, don’t get brainwashed by other people’s research agendas: it’s good to think outside the box.
Start with a compelling question, then think about how someone could get the answer, then look to see if anyone has done exactly that.
Many big interesting questions are addressed by one or more general theories and every theory makes key assumptions and predictions. Have these actually been tested yet? That’s a good place to start. For example, biological market theory assumes that a shift in supply or demand will lead to changes in the value of services exchanged by individuals in a mutualism. Has this been tested? Reciprocity theory predicts that individuals will reduce cooperative investments towards individuals that don’t reciprocate. What’s the evidence for that?
Not every interesting phenomenon is directly addressed by a scientific theory, but often there is a theory, perhaps from another discipline, that could be applied to the problem. That’s another good starting place. For example, what theories from biology could be explain the psychology of human friendship? If your research doesn’t address a theory, it should address a big question that is of interest to many people.
Your proposal should start with the big picture. This should be something that everyone will find interesting. Answer these questions:
After you write the draft, get lots of feedback. Get input from as many minds as possible. The most likely scenario is that inexperienced researchers will propose to do ambitious things X, Y, and Z in their first year, and more experienced people will tell them to start off by focusing just on part 1 of X. Just doing that might take 2 years.
On managing your PI
Scientists don’t receive any training in how to be a good mentor. Your PI will be committed to your success but they won’t necessarily know what you want or need unless you tell them. Nobody wants to be “needy” but it’s a good idea to be proactive. If the PI doesn’t check up on you, send them monthly updates. When you write outlines and drafts, ask for feedback. If you want to discuss things, ask them when is good to meet. Professors have packed schedules, so it’s usually better to set a meeting, then to just drop in and expect to have a long discussion.
On being a good scientist
Being a successful academic is not always the same thing as being a good scientist. There are academics who are terrible scientists, and there are great scientists who are not very successful in academia. Being a successful academic means being a good teacher, getting large grants, and publishing in prestigious journals. In sum, it means that you have lots of influence in your field. Being a successful scientist, however, means that your influence is actually moving your field towards a more accurate view of the world, because your work is careful and rigorous, you encourage other people to critique it, and you are honest about the limits of your conclusions. In sum, you say things that are actually true. Science is a job for people who value intellectual honesty, skepticism, logic, and evidence. Science is inherently open and transparent. If you try to succeed in academia at the expense of the quality of your science by overselling your work or making straw man arguments, you may do well in the short-term, but you will eventually gain a bad reputation as a sloppy scientist among the leading researchers in your field. And those are the people you should care the most about impressing.
Ideally, we are both good scientists and good academics. The ideal lab has a culture that encourages being a good scientist first and foremost, by trying to create an environment where everyone feels safe to be ignorant and ask really naïve questions; where undergraduates feel comfortable arguing with the PIs, postdocs, and grad students; and where nobody criticizes people, but we all feel comfortable criticizing ideas (constructively). Not taking criticism of ideas personally or defensively is one of the one most difficult, yet important, skills for scientists. We must remember that the goal is to make the final product as good as possible, not to be the most expert or clever person in the room. Likewise, our goal should be to produce work that is transparently valuable, not to “get it past the reviewers”. Even if criticism is not constructive or just plain wrong, it still tells you what parts of your argument you may need to communicate more clearly. Expertise only comes from failing, a lot.
The whole point of academia is meeting and talking with talented, interesting, and passionate people who know a lot about something, so do not be afraid to seek out, talk to, and listen to more experienced people who can think more clearly than you about topics with which you’re struggling. Yes, more senior scientists always seem too busy, but there is nothing they love more than to use their arcane knowledge to really help out a scientist in training. Looking back, I realize I wasted so many opportunities to talk science with really smart and knowledgeable people. Yes it can be embarrassing to reveal just how little you really understand about a topic, but everyone expects that from a student, so now is the best time!
Katharina Eggert is from Germany and visited STRI from March until May 2017. She helped with a broad variety of projects including scoring cooperation in vampire bats, maintaining a system of monitoring bat roosts, and measuring exploration of novel objects by young and old vampire bats.
I have always had an interest in the ecology and conservation of the flora and fauna of the tropical rainforests. Before interning at the Smithsonian Tropical Research Institute with Dr. Gerald Carter, I had worked at field stations in Ecuador and Peru. My interest in bats started in spring 1994 when a small colony of Pipistrellus pipistrellus moved into a crevice above my window, and decided to return every year thereafter. I have spent many summers watching “my” bats and they motivated me to join and volunteer for our local conservation organisation. During my internship at STRI I had a unique opportunity to study cooperative behaviour and social bonds in the common vampire bat. I learned about designing and evaluating research projects that focus on social interactions. In addition, I assisted with a range of different bat-related projects in Gamboa and Barro Colorado Island. This enabled me to gain a wide range of valuable bat-relevant field skills.
Hugo Narizano is from France and visited STRI from February to May. He is currently a MSc student at Edinburgh Napier University with Jason Gilchrist, and is studying the relationships between self-grooming and social grooming in vampire bats.
My interest in biology, especially ethology and wildlife, started as a child when I was living on a former farm in a small village. Growing up surrounded by a wide range of different animals, including some mysterious bats, triggered my desire to devote my life to animals. I started to be particularly interested in the similarities between humans and non-human animal sociality. This project was my first opportunity to work with bats, and with the common vampire bat, which I consider to be one of the most interesting bat species. I am learning more about designing and running experiments. Also, this project has enabled me to meet intelligent and inspiring people from STRI studying different topics and species. I have learned more about science as a whole. This project has taught me about what it takes to become a competent scientist.
After I graduate from Edinburgh Napier University, I am willing to conduct another research project with vampire bats, or on a different topic with bats, such as the interaction between Nepenthes hemsleyana, a pitcher plant, and Kerivoula hardwickii, the Hardwicke’s woolly bats [see past blogpost]. In the near future, I also wish to follow on with a PhD focusing on bat behaviour or ecology preferably, or possibly on a eusocial species.
Jineth Berrío-Martínez (MSc in Biology) is a researcher from Colombia who arrived in April has been travelling around Panama to find additional wild vampire bat colonies. She is working on development of biting ability in young vampire bats.
My research interests include tropical biology, population ecology, reproductive biology, evolution, and conservation. Early in my career as a biologist, bats caught my attention, leading me to work with them for more than eight years now. Desmodus rotundus is one of my favorite bat species because of the astonishing morphological and behavioral adaptations related to their diet. Despite the fact that vampires are a common species in my home country, there are many aspects of their ecology that are unknown or poorly understood.
Without a doubt, this internship has been an extraordinary opportunity to gain experience in behavioral ecology. Gerry is teaching me about experimental design and statistical analysis. Additionally, I hope to provide valuable support to a variety of different projects from filming and measuring behavior to fieldwork. I intend to make sure that my research projects are completed with diligence.
Many of the most remarkable scientific papers I have read on tropical ecology, behavior, and evolution have been written by researchers associated with Smithsonian Tropical Research Institute (STRI). Here I am exposed to other researchers’ experiences studying ecological and evolutionary problems. I strongly believe the skills I will learn and the collaborations I will establish during this internship will be an important platform for achieving my future academic goals. I plan to improve my research skills and pursue a PhD in Ecology and Conservation abroad.
Samuel Kaiser (MSc in Biology) arrived in June from Germany and is currently conducting a thermal preference experiment in vampire bats. The goal is to see if captive-born vampire bats without any past experience have an innate preference for warm blood.
It is hard to pinpoint my interests. I like animal behaviour – how animals communicate, interact and socialise. I’m also interested in how animals are affected by the environment and humans. Previously, I studied microplastic pollution and its effect on Daphnia magna. Then, starting an internship at the Max-Planck-Institute for Ornithology (Seewiesen, Germany), I discovered my fascination for bats and their use of echolocation to orient and hunt. After conducting experiments on passive-listening in the greater horseshoe bat (Rhinolophus ferrumequinum), I switched my focus to studying thermoperception in the tropical bat Phyllostomus discolor. This ultimately lead me to the internship at Smithsonian Tropical Research Institute in Gamboa, Panama with Dr. Gerald Carter and Dr. Rachel Page to learn more about the common vampire and its preferences for warm blood. My fascination with the common vampire is based in its ability to sense infrared radiation. This internship is a great opportunity for me to study tropical bats, and I have always wanted to do fieldwork in the tropics. In the future, I plan to travel around Central America and later start a PhD in animal behaviour.
Sebastian Stockmaier is a PhD student at the University of Texas at Austin in Dan Bolnick`s lab. This is Basti’s fifth field season in Panama and his second season working on vampire bats. He is studying the influence of sickness on cooperative behaviors in vampire bats. 
Despite my passion for being outside and for all the wildlife out there, I chose to spend most of my undergraduate research in laboratories working on virus-cell interactions (Institute Pasteur in Paris) and phylogenetic classification of some mysterious African bat viruses (Robert Koch Institute in Berlin). I then started a Masters program in organismal and evolutionary biology at the University of Konstanz, where I worked with Dina Dechmann and Teague O`Mara on several bat and bird species, as well as on tiny European shrews.
My masters at the University of Konstanz taught me–besides the fundamentals of evolution, ecology, and behavior–about the beauty of getting out into the field. Some formative influences included several research projects at STRI in Panama, and a spontaneous research trip to Kasanka National Park in Zambia, a spot known among bat researchers for a massive seasonal gathering of flying foxes. Having experienced biology in both the field and lab, I am trying to bridge the gap in pursuing some of my research questions. For my doctoral degree, I joined Dan Bolnick’s lab at the University of Texas. One of the main questions in our lab revolves around how pathogens interact with their hosts , a topic which involves ecology, behavior, and evolutionary genetics. I am generally interested in how transmissible pathogens shape group-living, and how they influence the evolution of social traits. I am also interested in how social behaviors of hosts can shape the evolutionary trajectories of a pathogen. I am trying to tackle some questions using vampire bats, and for other questions, I plan to establish experiments in Austin using aggregating C. elegans genotypes and a nematode pathogen. Since I enjoy teaching as well as research, I would like to further pursue a career in academia.
Along with Basti, Rachel Crisp has also worked in both 2016 and 2017. She is studying social dominance in female vampire bats.
“Team Vampire” is part of the Rachel Page Bat Lab at STRI.
Adam Cole from NPR visited our lab to shoot this great video short on human-vampire bat conflict.
So “should we wipe out vampire bats?” No, even if we could, we shouldn’t try, and frankly, nobody is actually suggesting exterminating vampire bats as a long-term solution. More on this topic in a previous post:
Is killing vampire bats good for public health? No. It might increase rabies risks.
The best work on this topic is being done now by Daniel Streicker’s lab.
Our latest paper here. Also some early press here. There are actually three recent papers on social networks and the benefits of network size in primates (by Laurent Brent and co-authors), songbirds (by Josh Firth and co-authors), and bats (by me and co-authors):
Family network size and survival across the lifespan of female macaques
by L. J. N. Brent, A. Ruiz-Lambides, M. L. Platt
Abstract: Two decades of research suggest social relationships have a common evolutionary basis in humans and other gregarious mammals. Critical to the support of this idea is growing evidence that mortality is influenced by social integration, but when these effects emerge and how long they last is mostly unknown. Here, we report in adult female macaques that the impact of number of close adult female relatives, a proxy for social integration, on survival is not experienced uniformly across the life course; prime-aged females with a greater number of relatives had better survival outcomes compared with prime-aged females with fewer relatives, whereas no such effect was found in older females. Group size and dominance rank did not influence this result. Older females were less frequent targets of aggression, suggesting enhanced experience navigating the social landscape may obviate the need for social relationships in old age. Only one study of humans has found age-based dependency in the association between social integration and survival. Using the largest dataset for any non-human animal to date, our study extends support for the idea that sociality promotes survival and suggests strategies employed across the life course change along with experience of the social world.
From the world’s longest-running field study of birds at Oxford…
Wild birds respond to flockmate loss by increasing their social network associations to others
by Josh A. Firth, Bernhard Voelkl, Ross A. Crates, Lucy M. Aplin, Dora Biro, Darren P. Croft, Ben C. Sheldon
Abstract: Understanding the consequences of losing individuals from wild populations is a current and pressing issue, yet how such loss influences the social behaviour of the remaining animals is largely unexplored. Through combining the automated tracking of winter flocks of over 500 wild great tits (Parus major) with removal experiments, we assessed how individuals’ social network positions responded to the loss of their social associates. We found that the extent of flockmate loss that individuals experienced correlated positively with subsequent increases in the number of their social associations, the average strength of their bonds and their overall connectedness within the social network (defined as summed edge weights). Increased social connectivity was not driven by general disturbance or changes in foraging behaviour, but by modifications to fine-scale social network connections in response to losing their associates. Therefore, the reduction in social connectedness expected by individual loss may be mitigated by increases in social associations between remaining individuals. Given that these findings demonstrate rapid adjustment of social network associations in response to the loss of previous social ties, future research should examine the generality of the compensatory adjustment of social relations in ways that maintain the structure of social organization.
Given their relevance, if these papers had come out earlier, I would have cited them!
Social bet-hedging in vampire bats
by Gerald G. Carter, Damien R. Farine, Gerald S. Wilkinson
Abstract: Helping kin or nonkin can provide direct fitness benefits, but helping kin also benefits indirect fitness. Why then should organisms invest in cooperative partnerships with nonkin, if kin relationships are available and more beneficial? One explanation is that a kin-limited support network is too small and risky. Even if additional weaker partnerships reduce immediate net cooperative returns, individuals extending cooperation to nonkin can maintain a larger social network which reduces the potential costs associated with losing a primary cooperation partner. Just as financial or evolutionary bet-hedging strategies can reduce risk, investing in quantity of social relationships at the expense of relationship quality (‘social bet-hedging’) can reduce the risks posed by unpredictable social environments. Here, we provide evidence for social bet-hedging in food-sharing vampire bats. When we experimentally removed a key food-sharing partner, females that previously fed a greater number of unrelated females suffered a smaller reduction in food received. Females that invested in more nonkin bonds did not do better under normal conditions, but they coped better with partner loss. Hence, loss of a key partner revealed the importance of weaker nonkin bonds. Social bet-hedging can have important implications for social network structure by influencing how individuals form relationships.
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1. Introduction
When cooperative relationships require an investment of time or energy, individuals should invest preferentially in the partner yielding the greatest cooperative returns [1–3]. However, if cooperative relationships take time to develop and partners are not always available, then a strategy that focuses investments in the single most-profitable partnership is risky. When partner availability is unpredictable, a better strategy would diversify cooperative investments across more partners to reduce the potential costs of losing a key partnership. We call this strategy social bet-hedging. Like other forms of bet-hedging [4], this strategy can be advantageous even if it reduces average short-term returns.
Bet-hedging strategies avoid risk. Social bet-hedging is analogous to evolutionary bet-hedging, where phenotypes with less temporally variable reproductive success outbreed phenotypes yielding reproductive success that is higher on average but more temporally variable [4]. This occurs because optimizing growth rates (or returns on investment) requires increasing the geometric, rather than arithmetic, mean. An evolutionary bet-hedging strategy can maximize geometric mean fitness, even at the expense of a lower arithmetic mean fitness, by coping better with rare stressful conditions [4].
By spreading cooperative investments to more partners, social bet-hedging strategies can reduce the temporal variance in cooperative returns caused by changes in partner availability. Investing in new relationships can be beneficial even if this requires diverting time and energy away from the most-profitable cooperative relationship which yields the greatest inclusive fitness return rate (e.g. the strongest reciprocator or closest kin).
Social bet-hedging might explain why female common vampire bats (Desmodus rotundus) that have strong reciprocal food-sharing relationships with close kin still regurgitate food to other nonkin [5–7]. Vampire bats are susceptible to starvation and depend on a network of food-sharing partners to feed them after unsuccessful foraging nights. The strongest, most reliable, and most balanced food-sharing bonds develop between mothers and daughters, but even for these close kin, the direct fitness benefits of food sharing might exceed the indirect fitness benefits [5–10]. The best known predictor of sharing rates within familiar pairs is not kinship, but the reciprocal rate of sharing [5,8]. If feeding close kin yields reciprocal sharing benefits that are equal or greater to feeding nonkin, why invest in nonkin bonds?
Sharing only with kin could be risky because relatives can be lost for various reasons. A starved female with only one or a few close maternal kin in her food-sharing network might not find her primary close kin donor, for example, if this partner also failed to feed or switched to a different roost on that night—which happens frequently [10]. To compensate for this risk, a social bet-hedging female would foster new bonds by diverting some of her social time and energy away from mothers and daughters and towards other females. Even if each of these additional partners is less related and reciprocates less, this strategy could dramatically increase long-term survival by reducing the risk of failing to find a primary donor when in dire need.
To test this idea, we quantify the impact, in terms of total food received, of removing a past key food donor for individual bats in need. Previously, Carter & Wilkinson [6] demonstrated that females that fed more nonkin females in previous years subsequently received more food in the absence of this key donor (see Methods), but this finding could simply mean that better-connected bats always receive more food. Here, we extend our analysis of this experiment to show that, as predicted by social bet-hedging, helping more nonkin did not increase food received when key donors were available, but it reduced the negative impact on food received when a key donor was removed.
2. Methods
We used data from a previous experiment [6], where a female subject was isolated and fasted for 24 h, then reintroduced to a captive colony of 27–34 individually marked conspecifics to measure food donated by each groupmate. Mean dyadic donation rates were calculated from 1337 dyadic regurgitation observations among 14 captive females using 91 fasting trials over a 4-year period (see electronic supplementary material, [6]). Relatedness was estimated using maternal pedigree and 19 microsatellite markers (see [6]). For each female, a unique key donor with a strong history of food sharing was selected for temporary removal; key donors were either the subject’s highest-ranking donor (nine cases), second-highest ranking donor (four cases), or a lower-ranking donor but the highest-ranking recipient (one case) (see electronic supplementary material, [6]). During two control trials, a female that had never fed the subject was excluded by either removing it or fasting it on the same night. During three subsequent test trials, the subject’s key donor was similarly excluded [6]. A previous analysis showed that bats that fed more nonkin females in past years received more food during test trials [6], but the social bet-hedging hypothesis predicts that this relationship should be most important when key donors are removed, not when they are present.
Here, we fitted linear models to predict the amount of food received with and without key donors present as well as the change in total food received (difference in food received per trial) when key donors were removed. We included the number of nonkin females fed in the past 4 years to represent investment in the size of a social support network. We did not include the number of kin fed because this depended on the number of kin available. We also did not include the number of males fed because stable bonds in the wild are female–female. To control for sampling bias, we included the control variable opportunity to donate, which is the number of trials where the subject could have fed another bat (see electronic supplementary material). The distribution of residuals did not deviate from normal (Shapiro Wilk’s test: W = 0.98, p = 0.95). To visualize results, we plotted mean food received against residual past sharing to nonkin females—the residuals from a regression of the number of unrelated females fed on number of opportunities to donate (to control for the latter).
3. Results
Under typical conditions, when key donors were present, the number of female nonkin fed in previous years did not predict the amount of food received; instead the trend was negative (figure 1a;R2= 0.43, β = −52.4, t = −1.81, p = 0.155). However, feeding more female nonkin did predict receiving more food later when a female’s key donor was absent (figure 1b;R2 = 0.56, β = 56.0, t = 3.68, p = 0.004). A bat’s proclivity to invest in female nonkin therefore predicted the change in total food she received when key donors were removed (R2 = 0.58, F2,11 = 7.54; β = 108.4, t = 3.48, p = 0.005; figure 1c). Females that fed more female nonkin coped better with partner removal. This result was robust to several variations in the analysis (see electronic supplementary material).
4. Discussion
Our results support the social bet-hedging hypothesis. By helping nonkin, individuals appear to maintain a wider support network than would be possible through only helping close kin. This suggests that female vampire bats can reduce the costs of losing a key donor by ‘not putting all their eggs in one basket’.
The social bet-hedging hypothesis makes three key assumptions. First, it assumes that individuals shift cooperative investments to and from individuals based on their relative cooperative returns, as predicted by reciprocity and biological market theory (e.g. models of partner control and partner choice) [1–3].
Second, it assumes not only that there are fitness benefits to having both more cooperative partners and stronger relationships [11–17], but also that individuals often face a trade-off between investing in relationship quantity versus quality (strength). If cooperative relationships require continuous investment, then merely increasing the number of weak connections can reduce overall cooperative returns, just as increasing offspring production at the expense of offspring quality does not reliably increase fitness [18]. On the other hand, strengthening each relationship can come at the expense of relationship quantity, so individuals might therefore divert investments towards partners that yield lower indirect fitness or reciprocal returns simply to create more relationships.
Third, social bet-hedging only makes sense if lost cooperative partnerships cannot be replaced instantly and effortlessly (as evidenced by figure 1a). Backup partners must already be in place. Social bet-hedging therefore assumes that new relationships require time and energy to develop. This seems true for food-sharing vampire bats [5–10].
Social bet-hedging may also exist for other cooperative behaviours. For example, female baboons increase their social grooming rates and groom more partners after the death of a close female relative [19], suggesting that investments in more relationships can help to compensate for the loss of a key social partner. In humans, although relationship quality is better than relationship quantity at predicting received social support [20], people appear to benefit from a greater number of weaker friendships in environments where friends are more likely to leave [21].
Many models of cooperation focus on pairwise interactions (e.g. [2]), but cooperative ‘exchange rates’ are determined by the supply and demand of cooperative services and partners—properties of the larger social network [22]. Many cooperative species might allocate cooperative investments across several partners and compare the varying return rates from each [3,22]. It remains unclear, however, if or how different social animals balance the quality and quantity of social ties. By influencing the number and strength of connections in a social network, strategies like social bet-hedging can both shape, and be shaped by, social network structure.
Ethics: All procedures were approved by the University of Maryland Institutional Animal Care and Use Committee (Protocol R-10-63).
Data accessibility: The data supporting this article have been uploaded as part of the electronic supplementary material.
Authors’ contributions: G.G.C. and D.R.F. conceived the analysis, G.G.C. carried out the analysis, and D.R.F. and G.S.W. advised the analysis. G.G.C. drafted the manuscript; D.R.F. and G.S.W. revised it critically for important intellectual content. All authors gave final approval of the version to be published, and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Funding: Work by G.G.C. was supported by a Ford Predoctoral Fellowship, a Dissertation Improvement Grant from the National Science Foundation (IOS-1311336), and grants from the American Society of Mammalogists and Animal Behavior Society.
Acknowledgements: We thank the Organization for Bat Conservation for their extraordinary support. Ronald Noë, Rachel Crisp, Julia Vrtilek and two anonymous reviewers provided comments that improved the manuscript.
References
Text Supplement
Supplement to methods
For each female test subject, we selected a unique key donor. All targeted key donor pairs were symmetrical such that if bat A was the key donor for bat B, then B was the targeted key donor for A. This was possible because if bat A was one of the most frequent donors for B, then B was typically one of the most frequent donors for A. The key donor was the subject’s highest-ranking donor, i.e. the bat that gave it the most food, in nine cases (including three mothers, four daughters, another relative, and one nonrelative). The key donor was the subject’s the second-highest-ranking donor in four cases (including one mother, another relative, and two nonrelatives). However, in one case (one nonrelative), the key donor was the highest-ranking recipient for the subject, but only the ninth-highest-ranking donor. In each trial, a possible donor was excluded by either removing it or fasting it on the same night, and this occurred on five occasions separated by at least 7 days.
The control variable opportunity to donate explained 79% of the variation in the observed number of partners fed (F(1,13)=48, p<0.0001), and it also predicted the number of nonkin females fed (R2=0.31, F(1,13)=5.5, p=0.038). Opportunity to donate was determined by a bat’s presence or absence in the home cage during past fasting trials, which was influenced by age (Spearman’s correlation with age: 0.58; p=0.03) and the bat being haphazardly excluded from some past fasting trials based on sickness, injury, or recent birth of a pup.
Supplement to results
When controlling for opportunity to donate, the effect of the number of nonkin females fed on the change in food received remained the same after excluding three cases where key donors failed to donate (R2=0.64, n=11, F(2,8)=7.1, nonkin females fed: beta=115.5, t=3.16, p=0.0134). The effect was also detected when using nonkin females fed per opportunity to donate as the predictor (R2=0.29, n=14, F=4.79, p=0.0490). When we added key donor kinship as a factor (kin or nonkin) and the interaction between kinship and nonkin females fed as predictors in the model, we found no interaction effect (p=0.73). When this interaction term was removed, we found that nonkin females fed (beta=108.2, t=3.30, p=0.008), but not kinship (p=0.95), predicted the change in food received.
Supplement to discussion
Social bet-hedging can be seen as a strategy for balancing two potentially contradicting strategies: group augmentation, defined as investing in group members to increase group size, i.e. partner quantity (Kokko et al. 2001, Kingma et al. 2014), and reciprocity, defined as investing preferentially in specific partners that provide the best reciprocal returns, i.e. partner quality (Trivers 1971, Carter 2014). Imagine you are the ideal Darwinian primate, deciding how much to groom each member of your group to maximize cooperative returns and hence inclusive fitness. For simplicity in this case, assume all kinship is equal. Each groupmate will later provide you with food, if you have groomed them sufficiently, and each group member might differ in the amount of food they would feed you per unit of grooming received. Assume that return rates are tracked by some form of emotional scorekeeping, and that you therefore have full knowledge of which relationships provide the greatest return rates, assuming those individuals are present. There are countless ways to divide your time and energy. You could spend 100% of your grooming effort on your best food provider. You could allocate 85% to her and 10% to the next best and 5% to the third best. You could split your grooming effort equally among all group members. It’s easy to see the analogy with betting or financial investing. The optimal strategy will depend on the distribution of food-sharing probabilities and amounts (Kelly 1956). If one partner provides the highest return rate, then you should simply invest everything in that partner, i.e. a partner choice strategy. On the other hand, if all groupmates are equally likely to provide food and to provide equal amounts of food, then you should simply maximize the number of partners that are alive or available to you, i.e. group augmentation. However, if partner return rates or availability vary over time, then “social bet-hedging” becomes relevant.
The need for social bet-hedging also depends on the timescale of reciprocal relationship formation: how much grooming does it take to create a relationship that starts benefiting you with food sharing? If social grooming can immediately lead to food sharing in the next minute, then social bet-hedging is not necessary, because when food is needed, you can immediately divert social grooming to the current best partner. If, however, a food-sharing relationship requires several days of previous grooming investment, then you should already be grooming many different partners, in case they can become future food providers in a time of need. This form of social bet-hedging requires long-term contingency embedded within complex, stable, multi-benefit relationships, so it is most likely to be found in primate or primate-like societies composed of stable individualized cooperative relationships. It would be particularly interesting to test the extent to which subconscious decisions to invest in relationship quantity or quality influence human social networks of collaboration or friendship.
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