The intricate lives of bottlenose dolphins
Janet Mann, Professor of Biology and Psychology at Georgetown University, earned her PhD at the University of Michigan in 1991. For 25 years her work has focused on dolphin female reproduction, calf development, life history and tool-use in Shark Bay, Australia. She has published over 70 scientific papers in journals such as PNAS, Proceedings of the Royal Society, and Nature Communications. Her edited volume, Cetacean Societies (University of Chicago Press, 2000) received several awards. Twice she was a fellow at the Center for Advanced Study in the Behavioral Sciences at Stanford University and in 2012 she spoke at the Royal Society. Her research has received considerable media attention, including a 2011 BBC documentary focusing on her work. Professor Mann is recognized as one of the world’s authorities on dolphin behavioral biology. In 2011 she received two mentoring awards (Outstanding Mentor Award by the Council of Undergraduate Research and the Allan Angerio Award for Excellence in Faculty Mentorship) in recognition of her deep commitment to undergraduate education. Author website.
Although we have barely skimmed the water surface, in 25 years of studying wild bottlenose dolphins (Tursiops sp.) in Shark Bay, Australia, we have discovered a considerable piece of what their individual lives are like. Studying a marine mammal that leaves no traces, has no dens, travels far and wide and spends most of its life out of our view is not so easy, but worth the effort. With brains three times the size of the common chimpanzee, an understanding of wild bottlenose dolphins offers immense insight into mammalian cognitive and social evolution. To be more specific, the social, life-history and cognitive features of bottlenose dolphins show remarkable convergence with primates and other large brained mammals, offering a powerful method for examining selection pressures that favored cognitive evolution, tool-use, elaborate social network structure, extensive maternal care, behavioral plasticity and prolonged development in distantly related taxa.
Figure 1. Janet Mann with dolphins at the bow of her boat. Photo by Scott Tuason
The Dolphins of Shark Bay Research Project has been going strong for nearly three decades and involves scientists and students from four continents, a dozen countries and universities. My own work focuses on female life histories, reproduction and calf behavior and development. I also manage the large longitudinal database (which has tracked over 1500 dolphins) with my collaborator, Professor Lisa Singh (Computer Science, Georgetown University). The structure of data collection was heavily influenced by primatology. My mentors, Professor Jeanne Altmann (Princeton University) and Professor Barbara Smuts (University of Michigan), both studied savannah baboons for decades, but I was trained in Developmental and Biological Psychology at Brown University (Sc.B) and the University of Michigan (Ph.D.). I was attracted to bottlenose dolphin research by the parallels with primates and the methodological challenges in sampling their behavior.
Fortunately, Shark Bay (Figure 2) has shallow (mostly <6m), clear water with low human activity and the dolphins are residential, making it easy to find the same individuals day after day. It is also a UNESCO World Heritage Site with very low human activity and industry. We collect data in several ways, including surveys (for basic behavioral, reproductive, demographic, ecological and association data population-wide), focal follows (for comprehensive quantitative behavioral and ecological data on individuals), substrate transects (for detailed ecological data including habitat and prey). Focal follows involve searching for a specific individual (or mother-calf pair) and collecting systematic data for several hours on their behavior, associates, location and other details. Substrate transects involved diving and filming and collecting samples from the substrate in nearly 100 randomized deep-water locations to quantify habitat in areas too deep to see from the surface. The combination of methods allows us to examine dolphin life from the smallest minutiae of social interactions to population-wide patterns.
Figure 2. Map of Shark Bay and the main study area for the Shark Bay Dolphin Research Project.
Bottlenose dolphin society
The first thing to know about bottlenose dolphin society is that the dolphins are not in stable groups like a pod of killer whales or a troop of savanna baboons. Rather, their society has a dynamic fission-fusion nature, much like humans, with group composition being temporally and spatially variable over minutes, days or years. Although there are cliques or clusters containing individuals that preferentially associate, there is no community boundary and the society is best characterized as a continuous overlapping mosaic of relationships. Some dolphins have hundreds of associates over a few years, while others have only a few dozen (Gibson & Mann 2008a). The average group size is four, and rarely do groups get larger than 30 dolphins. We believe the challenges of forming and maintaining bonds in such a fluid and complex society is one reason dolphin brains are so large – with a large component likely dedicated to social cognition. The closest bonds in dolphin society are between a mother and her nursing calf, which extends for three years and occasionally up to nine years (Mann et al. 2000). Dolphins have some of the latest and most variable weaning ages for any mammal. Most weaning takes place half way (six months) into the mother’s next pregnancy. But after weaning, sons and daughters are really on their own (Mann et al. 2000). Daughters occasionally associate with their mothers post-weaning, but sons rarely do (Tsai & Mann 2012). Although both sexes remain in their natal area (termed bisexual locational philopatry), males spend much of their time with other males, eventually forming long-term alliances.
The second most closely bonded relationship is between adult males, which have been studied extensively by Richard Connor (University of Massachussetts-Dartmouth). By the time they are in their late teens, most males have formed tight alliances with one or two other males. These first-order alliances also form bonds with other pairs and triplets, known as second-order alliances, and there are additional layers of complexity beyond that (Connor et al. 2011). Alliance size, stability and complexity varies – and some males are not successful at establishing alliances at all. Alliances cooperate to gain access to females and keep other males away from an individual female. This is the context in which aggression is most often seen – either fights between or even within alliances and occasionally attacks on females who try to escape. Sometimes females assist other females in escaping this unwanted attention, and risk being attacked by males for doing so, but female association patterns are more variable, so they aren’t always around when they are needed.
Figure 3. Alliance of seven males called the “Prima Donnas”. They have been together for over 20 years. Photo by Janet Mann
But most of the time, females don’t have to worry too much about male aggression, they are raising calves on their own, and males show little interest in females with nursing calves—except in the year she is likely to wean. Females begin to calve around age 11 or 12, but to be successful, females need enough resources to support a large, growing calf. As such, females tend to be the impressive hunters of Shark Bay, and the diversity of foraging tactics is renowned. Five females literally hydroplane onto sandy beaches to trap mullet, and risk being stranded in the process (Figure 4, Sargeant et al. 2005). Some of you may have seen this behavior in the BBC’s Planet Earth Shallow Seas episode or the BBC’s 2011 film “The Dolphins of Shark Bay.”
Figure 4. Female beaches herself to catch a mullet, which she appears to have missed. Photo by Janet Mann
One female named Wedges catches giant golden trevally -- fish a meter long -- in deep water, and brings them to shallow (1-2 m) water to break the fish up so she can swallow it bit by bit. It often takes her an hour to break up the fish, but she catches one every 2.6 hours (Mann & Sargeant 2003, Figure 5). During this process, tiger sharks, smaller sharks, and curious dolphins are attracted to the event, causing her to interupt her feeding to chase them away. Another female named Sequel has been seen swimming at top speed, slamming into a comorant (a bird) that has just caught a fish, causing the cormorant to drop the fish so she can grab it. This is kleptoparasitism reversed since it is usually the birds stealing from dolphins.
Figure 5. Wedges with golden trevally fish as she carries it to shallow water to break up. Photo by Janet Mann.
But most curious are the spongers. About 55 dolphins (~5 percent of the population) in the eastern gulf of Shark Bay use basket shaped marine sponges to ferret prey from the seafloor (Figure 6, Mann et al. 2008). Basket sponges are worn on the rostrum (beak) and they change sponges every hour or so. They are mostly female, but eight males do sponge. It is a fairly solitary existence, spongers spend most of their time alone, sponging. As the only well-documented tool-using dolphins or whales, this behavior has attracted our intense scrutiny.
Figure 6. A) Basket sponge (Echinodyctium mesenterium) growing on the seafloor. B) Dolphin carrying sponge on her beak. C) Cluttered seafloor in channels where dolphins sponge. D) Hidden barred sandperch. The arrow on the right points to the eye of the fish. Photos by Eric Patterson. Figure from Patterson & Mann 2011.
Why do some dolphins become spongers while others do not? First and foremost, no dolphin becomes a sponger unless his or her mother was also a sponger. Nearly all daughters of spongers become spongers but only half of the sons do. This suggests that there is sex-biased copying. Based on our observations of sponging and other foraging tactics, daughers are more likely to develop similar social and hunting behaviors as their mothers (Mann et al. 2008; Sargeant et al. 2005; Gibson & Mann 2008a). Although sons clearly learn hunting tactics from their mothers (Sargeant & Mann 2009), the cost of becoming a sponger might be too great for males. Because sponging is a lifetime commitment—all spongers that were discovered in the mid-1980s are still sponging—and sponging dolphins spend more time using tools than any other non-human animal (Mann et al. 2008), we suggest that a sponging lifestyle would infringe on the male’s ability to establish and maintain an alliance, and to be able to range widely to access cycling females. Sponging is restricted to deep channels where there are plenty of basket sponges (Sargeant et al. 2007).
It is curious that some males adopt sponging while others do not. We are currently examining whether mothers change their behavior and/or associates with some male calves and that this influences the likelihood of sponging. Since all those who begin to sponge adopt the behavior by age 3, a male calf seems to decide quite early in life whether or not he will become a sponger. We hypothesize that male calves who are exposed to many non-sponging males will be less likely to adopt sponging than males that have little exposure to non-sponging males pre-weaning. Thus, mothers might be able to manipulate her son’s trajectory by who she joins up with when he is young. Mothers might also adjust their behavior with sons more than daughters. To date, our results are suggestive that both maternal behavior and associates change with sons that do not become spongers.
But there is more to the story. We have always wondered why dolphins need the sponge in the first place! There are many dolphins in the same habitat that do not use sponges. What advantage or disadvantage do spongers have? Female calving success does not differ from non-spongers. My graduate student, Eric Patterson, came into my office one day with a great idea. Since most of the echo received when dolphins use sonar comes from the swim bladder (a gas filled organ that fish use to maintain buoyancy), he proposed that dolphins were targeting prey that didn’t have swim bladders and were likely hidden by the cluttered substrate in the channels. I thought this was a brilliant insight and naturally wondered why I hadn’t come up with it myself!
To explore his idea, Eric established dive transects in and out of channels. He sampled the substrate, got detailed data on prey and sponge distribution and importantly, became a sponger himself by attaching a sponge to the end of a pole. This was something I tried back in 1994 and really wanted someone to ‘sponge’ to see what we’d scare up, but in a systematic way. Eric did an extensive study of habitat, sponges, and prey types in the channels and other deep water habitats. While sponging he kept scaring up the same fish, Parapercis nebulosa, the barred sandperch. This fish is plentiful in channels, virtually absent in other deep water habitats, and is only visible after being scared up with a sponge. They move only a few meters away and then are an easy catch. So Eric caught lots of these fish. Lo and behold, no swim bladder. These fish are invisible to the eye and inaudible to the ear of a dolphin (Patterson & Mann 2011). We also had a scat sample of a sponger and P. nebulosa was there. We have some photos of spongers with barred sandperch in their jaws and other bits and pieces that help confirm the picture. Spongers are hunting barred sandperch and no one else can. You need a sponge to find them. Thus the spongers are exploiting a niche that is otherwise unavailable.
So, the spongers have figured out a way to access prey that others cannot—or at least not easily. One wouldn’t normally expect dolphins to use tools, given their extraordinary echolocation ability, but in some environments and with some prey, echolocation may be of less use. By contrast, dolphins in the Bahamas dive into sand up to their eyeballs, after conger eels, which have swim bladders. Also the Bahamian substrate is soft sand where they do it. The cluttered substrate of Shark Bay channels doesn’t make this kind of behavior practical.
Dolphin social life is hard to keep up with. Fortunately we have the tools of social network analysis to help us unravel the complexity and provide insights into social cognition. Even a calf’s social life is difficult to keep up with because they often separate from their mothers — up to a kilometer away — and establish their own network (Stanton et al. 2011). While their mothers have a network of adult and juvenile female associates, calves seem to ‘sample’ more widely. Both mothers and calves associate with adult males less than expected, but male calves have a particularly strong bond with other male calves. We are investigating how these early bonds affect survivorship post-weaning, in addition to how stable these bonds are through their lifetimes. Some male alliances established strong bonds in infancy and are still together, 25 years later! Males and females do not differ in the number of social relationships, but males have higher tie strength and cliquishness, which is expected given the male alliance structure (Mann et al. 2012). Female networks are more fluid, but appear to be equally important. Female social bonds are linked to fitness (Frère et al. 2010), although the precise way these factors influence fitness are not known. Females form cliques based on a range of factors including kinship, behavior, and shared habitat (Mann et al. 2012). Female bonds are more fluid because context, such as reproductive status (cycling, lactating or pregnant), and energetic needs will partly dictate when and where to associate and for how long.
Bottlenose dolphins appear to spend years learning to navigate a demanding social and ecological seascape, with changing relationships and context and complex hunting tactics. Individual dolphins vary on a wide range of features: sociability, network structure, alliance formation, life history traits, habitat use and foraging tactics. It is these challenges that have likely shaped the evolution of individual variation, innovation, cognition and plasticity in dolphin populations, all of which contribute to the evolution of brain size and social complexity.
Connor, R.C., Watson-Capps, J.J., Sherwin, W.B., & Krützen, M. (2011). A new level of complexity in the male alliance networks of Indian Ocean bottlenose dolphins (Tursiops sp.) Biology Letters, 7:623-626. doi: 10.1098/rsbl.2010.0852
Frère, C.H., Krützen, M., Mann, J., Connor, R., Bejder, L., Sherwin, W.B. (2010). Social and genetic interactions drive fitness variation in a wild population of bottlenose dolphins. Proceedings of the National Academy of Sciences. 107: 19949-19954
Gibson, Q.A. & Mann, J. (2008a). Early social development in wild bottlenose dolphins: sex differences, individual variation and maternal influence. Animal Behaviour. 76: 375-387.
Gibson, Q.A. & Mann, J. (2008b). The size, composition, and function of wild bottlenose dolphin (Tursiops sp.) mother-calf groups in Shark Bay, Australia. Animal Behaviour. 76: 389-405.
Mann, J., Connor, R., & Tyack, P., and Whitehead, H. (Eds.) 2000. Cetacean Societies: Field studies of dolphins and whales. Chicago: The University of Chicago Press.
Mann, J. & Sargeant, B. (2003). Like mother, like calf: The ontogeny of foraging traditions in wild Indian Ocean bottlenose dolphins (Tursiops sp.). In D. Fragaszy and S. Perry (Eds.) The Biology of Traditions: Models and Evidence. Cambridge University Press. pp. 236-266
Mann, J., Sargeant, B.L., Watson-Capps, J., Gibson, Q., Heithaus, M.R., Connor, R.C., & Patterson, E. (2008). Why do dolphins carry sponges?PLoS One. 3(12) e3868.
Mann, J., Stanton, M.A., Patterson, E.M., Bienenstock, E.J., & Singh, L.O. (2012). Social networks reveal a culture club in tool using dolphins. Nature Communications
Mann, J., Connor, R. C., Barre, L.M. & Heithaus, M.R. 2000. Female reproductive success in bottlenose dolphins (Tursiops sp.): Life history, habitat, provisioning, and group size effects. Behavioral Ecology, 11: 210-219
Patterson E.M. & Mann, J. 2011. The ecological conditions that favour tool use and innovation in wild bottlenose dolphins (Tursiops sp.). PLoS One. 6(7)e22243. doi:10.1371/journal.pone.0022243
Sargeant, B.L & Mann, J. (2009). Developmental evidence for foraging traditions in wild bottlenose dolphins. Animal Behaviour, 78:715-721.
Sargeant, B.L., Mann, J., Berggren, P. & Krützen M. (2005). Specialization and development of beach hunting, a rare foraging behavior, by wild Indian Ocean bottlenose dolphins (Tursiops sp.) Canadian Journal of Zoology. 83(11), 1400-1410. doi:10.1139/Z05-136
Sargeant, B.L., Wirsing, A.J., Heithaus, M.R., & Mann, J. (2007). Can environmental heterogeneity explain individual foraging variation in wild bottlenose dolphins (Tursiops sp.)? Behavioral Ecology and Sociobiology. 61:679-688. doi:10.1007/s00265-006-0296-8
Stanton, M.A., Gibson, Q.A., Mann, J.( 2011). When mum’s away: A study of mother and calf ego networks during separations in wild bottlenose dolphins (Tursiops sp.) Animal Behaviour. 82, 405-412
Tsai, Y.J. & Mann, J. (2012). Dispersal, philopatry and the role of fission-fusion dynamics in bottlenose dolphins. Marine Mammal Science. 28(3). doi :10.1111/j.1748-7692.2011.00559