Recent Publications

See all publications on the Shark Bay and the Monkey Mia dolphins here.

Sex, synchrony, and skin contact: integrating multiple behaviors to assess pathogen transmission risk (Leu et al., 2020)

“Direct pathogen and parasite transmission is fundamentally driven by a population’s contact network structure and its demographic composition and is further modulated by pathogen life-history traits. Importantly, populations are most often concurrently exposed to a suite of pathogens, which is rarely investigated, because contact networks are typically inferred from spatial proximity only. Here, we use 5 years of detailed observations of Indo-Pacific bottlenose dolphins (Tursiops aduncus) that distinguish between four different types of social contact. We investigate how demography (sex and age) affects these different social behaviors. Three of the four social behaviors can be used as a proxy for understanding key routes of direct pathogen transmission (sexual contact, skin contact, and aerosol contact of respiratory vapor above the water surface). We quantify the demography-dependent network connectedness, representing the risk of exposure associated with the three pathogen transmission routes, and quantify coexposure risks and relate them to individual sociability. Our results suggest demography-driven disease risk in bottlenose dolphins, with males at greater risk than females, and transmission route-dependent implications for different age classes. We hypothesize that male alliance formation and the divergent reproductive strategies in males and females drive the demography-dependent connectedness and, hence, exposure risk to pathogens. Our study provides evidence for the risk of coexposure to pathogens transmitted along different transmission routes and that they relate to individual sociability. Hence, our results highlight the importance of a multibehavioral approach for a more complete understanding of the overall pathogen transmission risk in animal populations, as well as the cumulative costs of sociality.”

 Sociality and tattoo skin disease among bottlenose dolphins in Shark Bay, Australia (Powell et al., 2019)

“Social behavior is an important driver of infection dynamics, though identifying the social interactions that foster infectious disease transmission is challenging. Here we examine how social behavior impacts disease transmission in Indo-Pacific bottlenose dolphins (Tursiops aduncus) using an easily identifiable skin disease and social network data. We analyzed tattoo skin disease (TSD) lesions based on photographs collected as part of a 34-year longitudinal study in relation to the sociality of T. aduncus using three metrics (degree, time spent socializing, and time in groups) and network structure, using the k-test. We show that calves with TSD in the second year of life associated more with TSD-positive individuals in the first year of life compared with calves that did not have TSD. Additionally, the network k-test showed that the social network links are epidemiologically relevant for transmission. However, degree, time spent in groups, and time spent socializing were not significantly different between infected and uninfected groups. Our findings indicate that association with infected individuals is predictive of an individual’s risk for TSD and that the social association network can serve as a proxy for studying the epidemiology of skin diseases in bottlenose dolphins.”

Causes and consequences of female centrality in cetacean societies (Rendell et al., 2019)

“Cetaceans are fully aquatic predatory mammals that have successfully colonized virtually all marine habitats. Their adaptation to these habitats, so radically different from those of their terrestrial ancestors, can give us comparative insights into the evolution of female roles and kinship in mammalian societies. We provide a review of the diversity of such roles across the Cetacea, which are unified by some key and apparently invariable life-history features. Mothers are uniparous, while paternal care is completely absent as far as we currently know. Maternal input is extensive, lasting months to many years. Hence, female reproductive rates are low, every cetacean calf is a significant investment, and offspring care is central to female fitness. Here strategies diverge, especially between toothed and baleen whales, in terms of mother–calf association and related social structures, which range from ephemeral grouping patterns to stable, multi-level, societies in which social groups are strongly organized around female kinship. Some species exhibit social and/or spatial philopatry in both sexes, a rare phenomenon in vertebrates. Communal care can be vital, especially among deep-diving species, and can be supported by female kinship. Female-based sociality, in its diverse forms, is therefore a prevailing feature of cetacean societies. Beyond the key role in offspring survival, it provides the substrate for significant vertical and horizontal cultural transmission, as well as the only definitive non-human examples of menopause.”

Maternal Care and Offspring Development in Odontocetes (Mann, 2019)

“Odontocetes are characterized by slow life histories and extensive maternal care, where offspring nurse for years in some species. Among some of the largest toothed whales, the mother and offspring of one or both sexes stay together for a lifetime, forming the basis of strong matrilineal social units and transmission of culture along maternal lines. Mother and calf face a series of challenges from the moment of birth. The newborn must quickly learn to follow and breathe alongside the mother—and wait for her while she dives for food. Within months the calf transitions to infant position for much of the time, although their swimming ability allows them to associate with others in the mother’s network. Because calves can easily become separated from their mothers, an effective communication system is necessary, and signature whistles and pod-specific dialects appear to serve this function. The mother plays a central role in the development of calf social and foraging tactics. Where this has been studied, calves adopt maternal behaviors, including foraging specializations, and share the mother’s network post-weaning. Although difficult to demonstrate “teaching” per se, dolphins are particularly good candidates given their exquisite learning ability and social tolerance. The role of non-mothers is clearly important in calf development, but whether calf interactions with non-mothers constitute “allomothering” remains unclear for most species. What is clear is that group living by cetaceans affords the calf protection from predators and possibly from infanticidal males. The causes of calf mortality are generally not known, as carcasses are rarely retrieved, but disease, predation, poor maternal condition, and anthropogenic causes (pollutants, provisioning, bycatch, boat strikes), and—rarely—infanticide, are all implicated. Weaning occurs when the calf no longer nurses, evident by cessation of infant position swimming. Interbirth intervals are also used as a proxy for weaning, though the calf frequently nurses during the mother’s subsequent pregnancy. Post-weaning, mothers and daughters continue to have preferential bonds, but in killer whales and pilot whales, sons also continue to have a strong relationship with the mother.”

Morphological differences between coastal bottlenose dolphin (Tursiops aduncus) populations identified using non-invasive stereo-laser photogrammetry (van Aswegen et al., 2019)

“Obtaining morphometric data on free-ranging marine megafauna is difcult, as traditional methods rely on post-mortem or live-capture techniques. We linked stereo-laser photogrammetry with longterm demographic data to compare length-at-age (LaA) growth curves of two well-studied populations of Indo-Pacifc bottlenose dolphins (Tursiops aduncus) in south-western (SW) and Shark Bay (SB), mid-western Australia. First, we determined the relationship between total length (TL) and blowholeto-dorsal fn (BH-DF) length from post-mortem subjects (R2=0.99, n=12). We then predicted TL from laser-derived BH-DF measurements of 129 and 74 known-age individuals in SW and SB, respectively. Richards growth models best described our LaA data. While birth length (103–110cm) was similar between study regions, TL estimates at 1, 3, 12, and 25 years difered signifcantly (p<0.001). Asymptotic length of adult males (SW=246cm, SB=201cm) and females (SW=244cm, SB=200cm) also difered signifcantly. Morphotypic variations likely refect regional adaptations to local water temperatures, with the temperate SW having cooler waters than sub-tropical SB. We demonstrate the efectiveness of a non-invasive technique to understand ecological, demographic and lifehistory characteristics of long-lived marine megafauna, which are critical parameters for informing conservation and management actions.”

Detecting respiratory bacterial communities of wild dolphins: implications for animal health (Nelson et al., 2019)

“Infectious diseases contribute to the vulnerable status of marine mammals, including respiratory illnesses. This study aimed to capture exhaled breath condensate (blow) for microbial identification from wild Indo-Pacific bottlenose dolphins Tursiops aduncus. Individual dolphins were sampled by holding a funnel connected to a 50 ml centrifuge tube over the blowhole of the animal near shore in Shark Bay (SB), Western Australia. Four individuals were sampled on 2 occasions along with seawater samples. Comparative blow and pool water samples were collected from 4 individual common bottlenose dolphins Tursiops truncatus housed in the National Aquarium (NA), Baltimore, Maryland, USA. Bacteria were identified using the V4 region of the 16S rRNA gene from extracted DNA. We identified bacteria independent of seawater in SB dolphins, which included the classes Alphaproteobacteria (26.1%) and Gammaproteobacteria (25.8%); the phyla Bacteroidetes (15.6%) and Fusobacteria (7.2%); and the genera Pseudomonas (11.5%), Pedomicrobium (4.5%), Streptobacillus (3.7%), Phenylobacterium (2.2%) and Sphingomonas (2.1%). There were broad similarities in phyla between SB and NA dolphins yet there were differences between lower taxonomic groups. A number of operational taxonomic units (OTUs) were shared between dolphin individuals, which may be a result of their genetic lineage (siblings or parentage), shared living and social interactions. A number of genera were observed in SB dolphins which have species known to be infectious in marine mammals such as Pseudomonas, Mycoplasma and Streptococcus. This study successfully characterised bacteria from DNA captured in blow from wild dolphins. The ability to capture these communities from individuals in the wild provides a novel health indicator.”

Quality and quantity of genetic relatedness data affect the analysis of social structure (Foroughirad et al., 2019)

“Kinship plays a fundamental role in the evolution of social systems and is considered a key driver of group living. To understand the role of kinship in the formation and maintenance of social bonds, accurate measures of genetic relatedness are critical. Genotype‐by‐sequencing technologies are rapidly advancing the accuracy and precision of genetic relatedness estimates for wild populations. The ability to assign kinship from genetic data varies depending on a species’ or population’s mating system and pattern of dispersal, and empirical data from longitudinal studies are crucial to validate these methods. We use data from a long‐term behavioural study of a polygynandrous, bisexually philopatric marine mammal to measure accuracy and precision of parentage and genetic relatedness estimation against a known partial pedigree. We show that with moderate but obtainable sample sizes of approximately 4,235 SNPs and 272 individuals, highly accurate parentage assignments and genetic relatedness coefficients can be obtained. Additionally, we subsample our data to quantify how data availability affects relatedness estimation and kinship assignment. Lastly, we conduct a social network analysis to investigate the extent to which accuracy and precision of relatedness estimation improve statistical power to detect an effect of relatedness on social structure. Our results provide practical guidance for minimum sample sizes and sequencing depth for future studies, as well as thresholds for post hoc interpretation of previous analyses.”

Every scar has a story: age and sex-specific conflict rates in wild bottlenose dolphins (Lee et al., 2019)

“Social living brings competition over mates, relationships, and resources, which can translate to direct conflict. In dolphins, tooth rakes received from conspecifics are highly visible and reliable indicators of conflict. New rakes indicate recent conflicts while healed rakes suggest older instances of conflict. Here, we investigate the healing time of conspecific tooth rakes in wild bottlenose dolphins, create a demographic profile of injury risk in the population, and consider the implications for age- and sex-specific aggression. Using photographic and scarring data from the Shark Bay Dolphin Research Project spanning 31 years (N = 269 tooth rakes), healing time was analyzed using a subset of sequential photographs of the same body part over 1–12 years (N = 70 tooth rakes). Ninety percent of tooth rakes in males and 95% of tooth rakes in females were no longer visible within 400 days, with males taking longer to heal than females. Using the full sample, we examined age and sex-effects on the prevalence of new tooth rakes. A negative quadratic model best fitted tooth rake prevalence patterns from ages 0 to 13 and a positive linear regression best fitted tooth rake prevalence patterns from ages 13 to 30. Both analyses revealed significant age and sex effects, where males had more tooth rakes than females. Age differences in tooth rake prevalence may be attributed to life history events such as sexual maturity onset, male-male competition and alliance formation, and sexual coercion. These results contribute to our understanding of the relationship between social conflict and life history strategies in long-lived mammals.”

Is MHC diversity a better marker for conservation than neutral genetic diversity? A case study of two contrasting dolphin populations (Manlik et al., 2019)

“Genetic diversity is essential for populations to adapt to changing environments. Measures of genetic diversity are often based on selectively neutral markers, such as microsatellites. Genetic diversity to guide conservation management, however, is better reflected by adaptive markers, including genes of the major histocompatibility complex (MHC). Our aim was to assess MHC and neutral genetic diversity in two contrasting bottlenose dolphin (Tursiops aduncus) populations in Western Australia—one apparently viable population with high reproductive output (Shark Bay) and one with lower reproductive output that was forecast to decline (Bunbury). We assessed genetic variation in the two populations by sequencing the MHC class II DQB, which encompasses the functionally important peptide binding regions (PBR). Neutral genetic diversity was assessed by genotyping twenty‐three microsatellite loci. We confirmed that MHC is an adaptive marker in both populations. Overall, the Shark Bay population exhibited greater MHC diversity than the Bunbury population—for example, it displayed greater MHC nucleotide diversity. In contrast, the difference in microsatellite diversity between the two populations was comparatively low.”

A Comparison of Tourism and Feeding Wild Dolphins at Monkey Mia and Bunbury, Australia (Mann et al., 2018)

“Animals are among the most sought after tourist attractions and the impact on them is a matter of concern to an increasing number of people. Tourism and Animal Welfare uniquely addresses the issue of animal welfare within the tourism experience. It explores important foundations such as the meaning of ‘animal welfare’ and its relation to ethics, animal rights and human obligations to animals. It also explores the nature and diversity of the position and role of animals within tourism.”

Senescence impacts reproduction and maternal investment in bottlenose dolphins (Karniski et al., 2018)

“Reproductive senescence is evident across many mammalian species. An emerging perspective considers components of reproductive senescence as evolutionarily distinct phenomena: fertility senescence and maternal-effect senescence. While fertility senescence is regarded as the ageing of reproductive physiology, maternal-effect senescence pertains to the declining capacity to provision and rear surviving offspring due to age. Both contribute to reproductive failure in utero making it difficult to differentiate between the two prenatally in the wild. We investigated both components in a long-lived mammal with prolonged maternal care through three parameters: calf survival, interbirth interval (IBI) and lactation period. We provide clear evidence for reproductive senescence in a wild population of bottlenose dolphins (Tursiops aduncus) using 34þ years of longitudinal data on 229 adult females and 562 calves. Calf survival decreased with maternal age, and calves with older mothers had lower survival than predicted by birth order, suggesting maternal-effect senescence. Both lactation period and IBIs increased with maternal age, and IBIs increased regardless of calf mortality, indicating interactions between fertility and maternal-effect senescence. Of calves that survived to weaning, last-born calves weaned later than earlier-born calves, evidence of terminal investment, a mitigating strategy given reduced reproductive value caused by either components of reproductive senescence.”

The reliability of pigment pattern-based identification of wild bottlenose dolphins (Bichell et al., 2018)

“Long-term studies often rely on natural markings for individual identification across time. The primary method for identification in small cetaceans relies on dorsal fin shape, scars, and other natural markings. However, dorsal fin markings can vary substantially over time and the dorsal fin can become unrecognizable after an encounter with a boat or shark. Although dorsal fins have the advantage in that they always break the water surface when the cetacean breathes, other physical features, such as body scars and pigmentation patterns can supplement. The goal of this study was to explore the use of dorso-lateral pigment patterns to identify wild bottlenose dolphins. We employed photographic pigment matching tests to determine if pigmentation patterns showed (1) longitudinal consistency and (2) bilateral symmetry using a 30 yr photographic database of bottlenose dolphins (Tursiops aduncus). We compared experienced dolphin researchers and inexperienced undergraduate student subjects in their ability to accurately match images. Both experienced and inexperienced subjects correctly matched dolphin individuals at a rate significantly above chance, even though they only had 10 s to make the match. These results demonstrate that pigment patterns can be used to reliably identify individual wild bottlenose dolphins, and likely other small cetacean species at other sites.”

Epidemiological investigation of tattoo-like skin lesions among bottlenose dolphins in Shark Bay, Australia (Powell et al., 2018)

“Bottlenose dolphins are excellent bioindicators of ocean ecosystem health for three reasons: (a) as long-lived apex predators they accumulate biotoxins and contaminants; (b) they are visible, routinely appearing at the water’s surface in coastal areas, often coming into close contact with humans; and, (c) they exhibit a range of pathogenic lesions attributable to environmental degradation. In this study, we analyzed tattoo-like skin lesions in a population of Tursiops aduncus studied for 30+ years in Shark Bay, Australia, a UNESCO World Heritage Site. We provide important baseline data by documenting epidemiological patterns of tattoo-like skin lesions in a healthy, free-ranging population that builds on the previous data of tattoo skin disease (TSD) derived from free ranging, stranded, and dead dolphins. Individual dolphins were classified as symptomatic with tattoo-like skin disease if at least one photograph showed a lesion similar to TSD. The average age of infection was 26.6 months (±34.8 months) with the symptomatic period lasting 137 ± 29.8 days. Overall prevalence of tattoo-like skin disease in the population was 19.4%. Age, but not sex, was significant, with yearlings (1–2 years) exhibiting tattoo-like lesions more than younger and older calves. Tattoo-like lesions were rare among juvenile and adult dolphins (N = 68 calves, 4 juveniles, and 3 adults). We hypothesize that the lower prevalence in youngest calves (b1 year) is due to maternal immunity, while older individuals (N2 years) have infection-acquired immunity, as reported for other small cetaceans. The low prevalence of tattoo-like lesions in Shark Bay compared to other populations with poxvirus is consistent with reproductive and demographic viability analyses. Furthermore, by documenting the demography of the disease, we can monitor changes in the prevalence of tattoo-like lesions as a sentinel indicator of ecosystem health.”

Calf age and sex affect maternal diving behavior in Shark Bay bottlenose dolphins (Miketa et al., 2018)

“Maternal care varies across taxa from brief, minimal care to long-term, intensive care. Mammalian mothers provide extensive and energetically expensive care by definition through pregnancy and lactation, which can extend for years, resulting in behavioural trade-offs between resource acquisition and direct care. In marine environments, mammalian mothers face unique challenges, such as the inability to cache or den their offspring while diving for prey. Dolphin newborns are precocious, accomplishing shallow dives in the first few weeks of life, however, fully mature diving and breathholding capabilities take years to develop. Consequently, mothers are faced with a trade-off between diving and foraging or remaining close to and protecting their calves at the surface. Here we examined this trade-off, specifically by investigating whether mothers change their dive durations, especially during foraging, as a function of calf age. We used a longitudinal (1988e2014) data set on wild bottlenose dolphins, Tursiops aduncus, in Shark Bay, Western Australia, which included 27 388 dive bouts from mothers (N ¼ 26) and calves (N ¼ 41). Our results show that maternal diving behaviour changes in response to calf age and sex. While both male and female calves increased their dive durations with age as expected, mothers were more likely to adjust their diving behaviour to accommodate female but not male calves, especially when daughters were in close proximity. This is consistent with findings that vertical social learning is more critical for daughters than for sons, and may reflect the sex-specific foraging and social tactics of the males and females more generally.”