Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies

Male bottlenose dolphins (Tursiops sp.) in Shark Bay have one of the most complex male societies outside humans. Two broad mating strategies have been identified in males. In the first strategy, there are two types of alliances: stable 'first-order' pairs and trios that herd individual females in reproductive condition, and 'second-order' teams of two first-order alliances (five or six individuals) that join forces against rivals in contests for females. In the alternative strategy, a 'super-alliance' of ca. 14 individuals, males form pairs or trios to herd females, but in contrast to the stable alliances, these pairs and trios are highly labile. Here, we show that males in stable first-order alliances and the derived second-order alliances are often strongly related, so that they may gain inclusive fitness benefits from alliance membership. By contrast, members of the super-alliance are no more closely related than expected by chance. Further, the strength of the association of alliance partners within the super-alliance, as measured by an index of joint participation in consorting a female, was not correlated with their genetic relatedness. Thus, within one population and one sex, it appears that there may be simultaneous operation of more than one mode of group formation.     

‘O father: where art thou?’— Paternity assessment in an open fission–fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay,Western Australia

Sexually mature male bottlenose dolphins in Shark Bay cooperate by pursuing distinct alliance strategies to monopolize females in reproductive condition. We present the results of a comprehensive study in a wild cetacean population to test whether male alliance membership is a prerequisite for reproductive success. We compared two methods for inferring paternity: both calculate a likelihood ratio, called the paternity index, between two opposing hypotheses, but they differ in the way that significance is applied to the data. The first method, a Bayesian approach commonly used in human paternity testing, appeared to be overly conservative for our data set, but would be less susceptible to assumptions if a larger number of microsatellite loci had been used. Using the second approach, the computer program cervus 2.0, we successfully assigned 11 paternities to nine males, and 17 paternities to 14 out of 139 sexually mature males at 95% and 80% confidence levels, respectively. It appears that being a member of a bottlenose dolphin alliance is not a prerequisite for paternity: two paternities were obtained by juvenile males (one at the 95%, the other at the 80% confidence level), suggesting that young males without alliance partners pursue different mating tactics to adults. Likelihood analyses showed that these two juvenile males were significantly more likely to be the true father of the offspring than to be their half-sibling (P < 0.05). Using paternity data at an 80% confidence level, we could show that reproductive success was significantly skewed within at least some stable first-order alliances (P < 0.01). Interestingly, there is powerful evidence that one mating was incestuous, with one calf apparently fathered by its mother's father (P < 0.01). Our study suggests that the reproductive success of both allied males, and of nonallied juveniles, needs to be incorporated into an adaptive framework that seeks to explain alliance formation in male bottlenose dolphins.     

Synchrony,leadership, and association in male Indo-pacific bottlenose dolphins (Tursiops aduncus)

Male Indo-pacific bottlenose dolphins in Shark Bay, Western Australia, have converged with humans in the formation of nested male alliances and the use of synchrony in alliance behavior. Further, the strength of association among allied male dolphins varies and the stability of alliances correlates with the rate that males consort with estrus females (and is thus a possible indicator of dominance). To examine the possibility that synchrony reflects alliance association strength and dominance relationships, we analyzed videotapes from focal follows of two groups of males that reflect the range of alliance size and the strength of association between individuals in the population. We examined two variables: leadership during synchronous behaviors, based on which animal in a synchronously surfacing pair surfaced first, and the degree of synchrony, based on temporal differences in synchronous surfacing. We predicted that closer associates would exhibit a greater degree of synchrony and that one dolphin in a dyad would consistently lead. Contrary to our predictions, the degree of synchrony was inversely related to strength of association within alliances. This surprising result suggests that individuals with less secure bonds may strive more to achieve synchrony. We found no evidence of leadership during synchronous surfacing or between synchrony and other behavioral variables. Proximate mechanisms for synchronous behavior, such as entrainment and mutual motor imitation (“the mirror game” paradigm), may inhibit leadership in this context. Our results show that synchrony during surfacing is not a useful behavior to examine for dominance relationships in wild dolphins but it may be a useful tool to examine variation in alliance relationships.     

SHARK ATTACKS ON BOTTLENOSE DOLPHINS (TURSIOPS ADUNCUS) IN SHARK BAY, WESTERN AUSTRALIA: ATTACK RATE, BITE SCAR FREQUENCIES, AND ATTACK SEASONALITY

Shark predation may have been a central factor influencing the evolution of sociality in dolphins, as well as a determinant of dolphin habitat use and behavior. To understand the role of predation in driving interpopulation differences in behavior and sociality, it is important to quantify differences in predation risk among populations. This study describes the frequency of shark-inflicted scars and estimates the shark attack rate on bottlenose dolphins ( Tursiops aduncus ) in Shark Bay, Western Australia. Shark bite scars were found on 74.2% (95 of 128) of non-calves, and most of these scars were inflicted by tiger sharks ( Galeocerdo cuvier ). Although there were no differences among age/sex classes in the frequency of scarring, significantly more adult males than adult females bore multiple scars. The rate of unsuccessful shark attack was estimated to be between 11% and 13% of dolphins attacked each year. Large sharks (>3 m) were responsible for a disproportionate number of attacks. However, bites from small carcharhinid sharks on 6.2% of dolphins suggest that some of these small sharks may be dolphin ectoparasites. Both the scar frequencies and attack rate suggest that Shark Bay dolphins face a greater risk of predation than bottlenose dolphins in other locations.     

Complex social structure, alliance stability and mating access in a bottlenose dolphin 'super-alliance'

Large brain size in mammals has been related to the number and complexity of social relationships, particularly social alliances within groups. The largest within-group male alliance known outside of humans is found in a social network (> 400) of Indian Ocean bottlenose dolphins (Tursiops aduncus) in Shark Bay Western Australia. Members of this dolphin 'super-alliance' cooperate against other alliances over access to females. Males within the super-alliance form temporary trios and occasionally pairs in order to consort with individual females. The frequent switching of alliance partners suggests that social relationships among males within the super-alliance might be relatively simple and based on an equivalence rule', thereby allowing dolphins to form large alliances without taxing their 'social intelligence'. The equivalence model predicts that the 14 males in the super-alliance should not exhibit differences in alliance stability or partner preferences. However, data from 100 consortships do not support the equivalence hypothesis. The 14 males exhibited striking differences in alliance stability and partner preferences suggesting that the super-alliance has a complex internal structure. Further, within the super-alliance, alliance stability correlates with consortship rate, suggesting that differentiated relationships within the super-alliance are based on competition for access to females.     

A novel mammalian social structure in Indo-Pacific bottlenose dolphins (Tursiops sp.): complex male alliances in an open social network

Terrestrial mammals with differentiated social relationships live in 'semi-closed groups' that occasionally accept new members emigrating from other groups. Bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia, exhibit a fission-fusion grouping pattern with strongly differentiated relationships, including nested male alliances. Previous studies failed to detect a group membership 'boundary', suggesting that the dolphins live in an open social network. However, two alternative hypotheses have not been excluded. The community defence model posits that the dolphins live in a large semi-closed 'chimpanzee-like' community defended by males and predicts that a dominant alliance(s) will range over the entire community range. The mating season defence model predicts that alliances will defend mating-season territories or sets of females. Here, both models are tested and rejected: no alliances ranged over the entire community range and alliances showed extensive overlap in mating season ranges and consorted females. The Shark Bay dolphins, therefore, present a combination of traits that is unique among mammals: complex male alliances in an open social network. The open social network of dolphins is linked to their relatively low costs of locomotion. This reveals a surprising and previously unrecognized convergence between adaptations reducing travel costs and complex intergroup-alliance relationships in dolphins, elephants and humans.     

Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia

Bottlenose dolphins are one of only a few mammalian taxa where the males are known to cooperate within their social group in order to maintain mating access to single females against other males. Male bonds in bottlenose dolphins have been hypothesized as evolving through kinship and associated inclusive fitness effects. In this study we tested whether individually identified male bottlenose dolphins preferentially associate and form alliances with kin in a small coastal resident population of southeastern Australia using a combination of behavioural data, genetic sexing, sequences of the mitochondrial DNA control region and nuclear microsatellite markers. Males generally associated significantly more often than expected with one to three other males, with whom they jointly herded females for mating. Associations and alliance membership were not associated with either maternal kinship or genetic relatedness. The majority of male pairs within alliances were randomly related, although high relatedness values were found between males of different alliances in the resident population. These findings indicate that mechanisms other than kin selection may be foremost in the development and maintenance of cooperation between male bottlenose dolphins.     

A Sex-Specific Affiliative Contact Behavior in Indian Ocean Bottlenose Dolphins, Tursiops sp.

A variety of signals are employed by animals to establish, mediate and advertise social bonds. Gentle contact behaviors, such as grooming in primates, are an important class of affiliative signals that may provide direct benefits (e.g. stress reduction, parasite removal) in addition to their signal information. Unlike other kinds of signals (e.g. male displays) examples of affiliative contact behaviors restricted to one sex are rare. Here we describe a strongly sex‐biased affiliative behavior ‘contact swimming’, in female bottlenose dolphins in Shark Bay, Western Australia. Females were more likely to be observed contact swimming than males and the presence of males likely influenced this behavior. This is surprising given that female relationships have been characterized as weak. Female dolphins are sometimes herded and harassed by males and contact swimming occurs most often between females in male‐biased groups. Contact swimming may serve as a signal of cooperation between females. Possible direct benefits include stress reduction and assisted locomotion.     

Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus)

In most mammals males usually disperse before breeding, while females remain in their natal group or area. However, in odontocete cetaceans behavioural and/or genetic evidence from populations of four species indicate that both males and females remain in their natal group or site. For coastal resident bottlenose dolphins field data suggest that both sexes are philopatric to their natal site. Assignment tests and analyses of relatedness based on microsatellite markers were used to investigate this hypothesis in resident bottlenose dolphins, Tursiops aduncus, from two small coastal populations of southeastern Australia. Mean corrected assignment and mean relatedness were higher for resident females than for resident males. Only 8% of resident females had a lower probability than average of being born locally compared to 33% of resident males. Our genetic data contradict the hypothesis of bisexual philopatry to natal site and suggest that these bottlenose dolphins are not unusual amongst mammals, with females being the more philopatric and males the more dispersing sex.     

Cultural transmission of tool use combined with habitat specializations leads to fine-scale genetic structure in bottlenose dolphins

Socially learned behaviours leading to genetic population structure have rarely been described outside humans. Here, we provide evidence of fine-scale genetic structure that has probably arisen based on socially transmitted behaviours in bottlenose dolphins (Tursiops sp.) in western Shark Bay, Western Australia. We argue that vertical social transmission in different habitats has led to significant geographical genetic structure of mitochondrial DNA (mtDNA) haplotypes. Dolphins with mtDNA haplotypes E or F are found predominantly in deep (more than 10 m) channel habitat, while dolphins with a third haplotype (H) are found predominantly in shallow habitat (less than 10 m), indicating a strong haplotype–habitat correlation. Some dolphins in the deep habitat engage in a foraging strategy using tools. These ‘sponging’ dolphins are members of one matriline, carrying haplotype E. This pattern is consistent with what had been demonstrated previously at another research site in Shark Bay, where vertical social transmission of sponging had been shown using multiple lines of evidence. Using an individual-based model, we found support that in western Shark Bay, socially transmitted specializations may have led to the observed genetic structure. The reported genetic structure appears to present an example of cultural hitchhiking of mtDNA haplotypes on socially transmitted foraging strategies, suggesting that, as in humans, genetic structure can be shaped through cultural transmission.     

Characterizing the socially transmitted foraging tactic “sponging” by bottlenose dolphins (Tursiops sp.) in the western gulf of Shark Bay,Western Australia

Individual foraging tactics are widespread in animals and have ecological and evolutionary implications. Indo‐Pacific bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia, exhibit a foraging tactic involving tool use, called “sponging.” Sponging is vertically, socially transmitted through the matriline and, to date, has been described in detail in the eastern gulf of Shark Bay (ESB). Here, we characterize sponging in the western gulf of Shark Bay (WSB), in which a different matriline engages in the behavior. We identified 40 individual “spongers” in 9 mo of boat‐based surveys over three field seasons. As is the case in ESB, the majority of WSB spongers was female and engaged in sponging in deep channel habitats. In contrast to ESB, however, there was no difference in the number of associates between spongers and nonspongers in WSB, and activity budgets differed between spongers and deep‐water nonspongers; spongers foraged more frequently and rested less than nonspongers. Group sizes in deep channel habitat, where sponging was prevalent, were typically larger than those in shallow habitat, except for foraging, perhaps indicative of higher predator abundance and/or scattered prey distribution in deep‐water habitat. This research improves our understanding of within‐population foraging variations in bottlenose dolphins.     

Fine-scale sociality reveals female–male affiliations and absence of male alliances in bottlenose dolphins (Tursiops truncatus) in the Shannon Estuary,Ireland

Knowledge of social behavior at an individual level is central to our understanding of complex mammalian societies. In this study, we analyzed the fine-scale sociality of wild bottlenose dolphins in the Shannon Estuary, Ireland, by examining associations between members of the whole population and between specific female and male dolphins. We carried out 51 boat-based individual focal follows on 18 identifiable bottlenose dolphins over 90.8 hr (39 days) between 2014 and 2016. Additionally, we conducted 353 boat-based surveys (with 607 sightings) between 2012 and 2015, and identified 121 distinct adult/juvenile dolphins. The mean group size of focal dolphin groups was 7.2 ± 4.1 (range = 1–20) and the mean fission-fusion rate was 3.06 ± 1.35 changes/hr. The most frequent composition of within-group affiliate pairs was female–male. Focal males spent more time with female nearest-neighbors than male nearest-neighbors (p = .013). Differences between female and male activity budgets were not strongly supported (p = .13). There was no evidence for male alliance formation in the Shannon Estuary population, and all of the known-sex top-ranked associates (7) of known males (n = 10) were females. This research reveals a distinct bottlenose dolphin society with female–male affiliations and an absence of male alliances.     

Whistle Convergence among Allied Male Bottlenose Dolphins (Delphinidae, Tursiops sp.)

Dolphins are adept at learning new vocalizations (whistles) throughout life, an ability thus far demonstrated in few nonhuman mammals. In dolphins, this ability is well documented in captivity but poorly studied in the wild, and little is known of its role in natural social behavior. This study documents the previously unknown phenomenon of whistle convergence among habituated free-living male bottlenose dolphins ( Tursiops sp.). Over a 4 yr study period, three male subjects formed an alliance, spending most of their time together and cooperating to herd females. Within individuals, whistle repertoires were more variable than expected based on previous studies, mostly performed with captive dolphins, but became less so during the course of the study. Among individuals, the distinctiveness of individual repertoires decreased such that the three males were virtually indistinguishable by the end of the study. Initially, some whistle types were shared. By the end of the study, the three males had formed a close alliance, and had all converged on one particular shared whistle form which they had rarely produced before forming the alliance. The results are discussed in terms of their implications for the prevailing 'signature whistle' hypothesis, as well as possible mechanisms and functional significance of whistle convergence among cooperating males.     

Mitochondrial and nuclear DNA analyses reveal fine scale geographic structure in bottlenose dolphins (<Emphasis Type="Italic">Tursiops truncatus</Emphasis>) in the Gulf of Mexico

There is a need for biological information to support current stock designations of bottlenose dolphins (Tursiops truncatus) in the Gulf of Mexico. The existence of many inshore, resident “communities” raises questions as to the relationship these dolphins may hold with dolphins inhabiting neighboring inshore and coastal areas. In this study, population subdivision was examined among four resident, inshore bottlenose dolphin stocks (Sarasota Bay, FL, Tampa Bay, FL, Charlotte Harbor, FL and Matagorda Bay, TX) and one coastal stock (1–12 km offshore) in the Gulf of Mexico. Evidence of significant population structure among all areas was found on the basis of both mitochondrial DNA (mtDNA) control region sequence data and nine nuclear microsatellite loci. Estimates of relatedness showed no population contained a significantly high number of related individuals, while separate AMOVAs for males and females indicated that both sexes exhibit a significant level of site philopatry. Results presented here provide the first genetic evidence of population subdivision between the coastal Gulf of Mexico and adjacent inshore areas along the central west coast of Florida. Such strong genetic subdivision is surprising given the short geographical distance between many of these areas and the lack of obvious geographic barriers to prevent gene flow. These findings support the current, separate identification of stocks for bottlenose dolphins inhabiting the eastern coastal and inshore areas of the Gulf of Mexico.     

POPULATION STRUCTURE IN AN INSHORE CETACEAN REVEALED BY MICROSATELLITE AND mtDNA ANALYSIS: BOTTLENOSE DOLPHINS (TURSIOPS SP.) IN SHARK BAY, WESTERN AUSTRALIA

We examined population substructure of bottlenose dolphins ( Tursiops sp). in Shark Bay, Western Australia, using 10 highly polymorphic microsatellite loci, and mitochondrial DNA (mtDNA). For microsatellite analysis, 302 different animals were sampled from seven localities throughout the bay. Analysis of genetic differentiation between sampling localities showed a significant correlation between the number of migrants ( Nm ) calculated from F _ST, R _ST and private alleles, and distance between localities–a pattern of isolation-by-distance. For mtDNA, 220 individuals from all seven localities were sequenced for a 351 base pair fragment of the control region, resulting in eight haplotypes, with two distinct clusters of haplotypes. Values of F _ST and (φ)_ST for mtDNA yielded statistically significant differences, mostly between localities that were not adjacent to each other, suggesting female gene flow over a scale larger than the sampled localities. We also observed a significant correlation between the number of female migrants calculated from F _ST and φ_ST and the distance of sampling localities. Our results indicate that dispersal in female dolphins in Shark Bay is more restricted than that of males.     

“Porpicide” in California: Killing of harbor porpoises (Phocoena phocoena) by coastal bottlenose dolphins (Tursiops truncatus)

Between 2007 and 2009, we witnessed three aggressive interactions between harbor porpoises and bottlenose dolphins in Monterey Bay, California. This is the first time such aggression has been documented in the Pacific, and the first time a harbor porpoise was collected immediately after witnessing its death, inflicted by bottlenose dolphins. Of the bottlenose dolphins present, 92% were males either confirmed (61%) or putative (31%). Since 2005, 44 harbor porpoise deaths inflicted by bottlenose dolphins were documented in California. Aberrant behavior was rejected as a cause of aggression, based on widespread documentation of similar behaviors in other populations of free‐ranging bottlenose dolphins. The evidence for interspecies territoriality as a form of competition for prey was weak: there is little dietary overlap and there are differences in bottlenose dolphin and harbor porpoise distribution patterns in California. Object‐oriented play was plausible as a form of practice to maintain intraspecific infanticidal skills or a form of play to maintain fighting skills between male associates. Contributing factors could be high‐testosterone levels, as attacks occurred at the height of the breeding season, and/or a skewed operational sex ratio. Ultimately, we need more information about bottlenose dolphin social structure at the time of the aggression.     

Spatial and Social Sexual Segregation Patterns in Indo-Pacific Bottlenose Dolphins (Tursiops aduncus)

Sexual segregation seems to be common in bottlenose dolphins, whereby males and females live in different pods that mix mainly for mating. Male dolphins often use aggressive behaviour to mate with females, while females with calves may have different activity and dietary requirements to males and different susceptibility to predation. We investigated the degree of spatial and social sexual segregation in Indo-Pacific bottlenose dolphins (Tursiops aduncus) in a subtropical estuary in Australia. Based on surveys completed over three years, dolphin groups were mostly mixed-sex or female. Mixed-sex groups were found in larger groups in mostly deeper water, whereas, female groups were foraging across all water depths in smaller groups. Aggressive coercive behaviour by males towards females was high, occurring mainly in deeper water, at higher tides, and outside the breeding season. Habitat use by female dolphin groups suggests that shallow tributaries may provide a sanctuary from aggressive males, access to suitable prey items and density for mothers and their calves, or a combination of these factors.     

Inbreeding tolerance and fitness costs in wild bottlenose dolphins

In wild populations, inbreeding tolerance is expected to evolve where the cost of avoidance exceeds that of tolerance. We show that in a wild population of bottlenose dolphins found in East Shark Bay, Western Australia, levels of inbreeding are higher than expected by chance alone, and demonstrate that inbreeding is deleterious to female fitness in two independent ways. We found that inbred females, and females with inbred calves, have reduced fitness (lower calving success). We further show that one of the costs of inbreeding is extended weaning age, and that females'' earlier calves are more likely to be inbred. While the exact causes of inbreeding remain obscure, our results indicate that one factor is female age, and thus experience. Any inbreeding avoidance mechanisms such as female evasion of kin, or male dispersal, do not seem to be completely effective in this population, which supports the view that inbreeding avoidance does not always evolve wherever inbreeding incurs a cost.     

Male reproductive success increases with alliance size in Indo-Pacific bottlenose dolphins (Tursiops aduncus)

1. Determining the extent of variation in male mating strategies and reproductive success is necessary to understand the fitness benefits of social and cooperative behaviour. 2. This study assesses the reproductive success of male Indo-Pacific bottlenose dolphins in a small embayment population where different behavioural strategies of males have previously been identified. Parentage for 44 sampled calves was examined using 23 microsatellite loci and one mitochondrial DNA marker. Our candidate parent pool of 70 males and 64 females contained individuals sampled from both the embayment and adjacent coastal populations. 3. A moderate level of polygyny was detected in our sample. We assigned paternity of 23 calves to 12 males at the strict 95% confidence level and an additional nine calves to two males at the 80% confidence level. The majority (92%) of successful males were identified as residents to the embayment, and 46% of offspring were located within the same social group or community as their father. 4. Our results suggest that the size of alliances was the best predictor of reproductive success for males in this population, while the strength of association among allied males, alliance stability and male ranging patterns had little influence. In line with predictions for male alliances formed between unrelated individuals, we found that reproductive skew within alliances was not large. 5. Together, our genetic and behavioural analyses demonstrate that alliance formation between male dolphins is a successful strategy to enhance reproductive output.     

Fine-scale population structure of bottlenose dolphins (Tursiops truncatus) in Tampa Bay, Florida

Some populations of coastal bottlenose dolphins ( Tursiops truncatus ) comprise discrete communities, defined by patterns of social association and long-term site fidelity. We tested the hypothesis that bottlenose dolphins in Tampa Bay, Florida, form a single community. The longitudinal study of dolphins in Sarasota Bay, adjacent to Tampa Bay, allowed us to ground-truth the definition of community and test whether our approach was robust to small sample sizes of resightings. We conducted photo-identification surveys in Tampa Bay during 1988–1993, and identified 102 dolphins with 10 or more sightings. We used hierarchical cluster analysis to examine the locations and association indices of these dolphins. We used analysis of variance (ANOVA) to test for differences in mean locations and determine whether mean coefficient of association (CoA) values within a community were higher than among communities. Dolphins in Tampa Bay clustered into five putative communities differing significantly in location and CoA values. Kernel estimates of the ranges of these five communities exhibited little overlap; some communities had no overlap at all. We conclude that five discrete communities of bottlenose dolphins exist in Tampa Bay and that such fine-scale structure may be a common feature of bottlenose dolphin populations throughout the southeastern United States.