Simon J. Allen

Social cohesion in a hierarchically structured embayment population of Indo-Pacific bottlenose dolphins

We investigated community structure and association patterns for a small population of Indo-Pacific bottlenose dolphins, Tursiops aduncus, inhabiting the Port Stephens embayment in southeastern Australia. Association data for 120 regularly sighted individuals were obtained from seasonal photoidentification surveys collected over 7 years (1998–2007). Using a combined cluster and social network analysis approach, we found association patterns between dolphins were hierarchically structured, where two mixed-sex communities were subdivided into smaller, temporarily dynamic social groups. Community membership corresponded to differences in individual ranging patterns and habitat occupation. The larger eastern community inhabits a typically marine environment, while individuals of the western community range over a larger area that is dominated by estuarine processes. Both communities were composed of long-term preferred companions; however, the degree of social cohesion differed considerably between the two communities. Associations between individuals were considerably stronger and temporally more stable in the western community. Western individuals also had significantly fewer preferred associates despite living in similar-sized schools. Finally, in direct contrast to associations within each community, intercommunity associations were highly variable and resulted primarily from aggregative behaviour. We propose the segregation of communities resulted from individual adaptation to local environmental conditions, facilitated by individual variability in association preferences. The disparity in association patterns between communities may have resulted from a combination of ecological, population density, kinship and anthropogenic factors.

Association patterns and kinship in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) of southeastern Australia

Kinship has been shown to be an important correlate of group membership and associations among many female mammals. In this study, we investigate association patterns in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) inhabiting an embayment in southeastern Australia. We combine the behavioral data with microsatellite DNA and mitochondrial DNA data to test the hypotheses that genetic relatedness and maternal kinship correlate with associations and social clusters. Mean association between females was not significantly different from a random mean, but the standard deviation was significantly higher than a random standard deviation, indicating the presence of nonrandom associates in the dataset. A neighbor-joining tree, based on the distance of associations between females, identified four main social clusters in the area. Mean genetic relatedness between pairs of frequent female associates was significantly higher than that between pairs of infrequent associates. There was also a significant correlation between mtDNA haplotype sharing and the degree of female association. However, the mean genetic relatedness of female pairs within and between social clusters and the proportion of female pairs with the same and different mtDNA haplotypes within and between clusters were not significantly different. This study demonstrates that kinship correlates with associations among female bottlenose dolphins, but that kinship relations are not necessarily a prerequisite for membership in social clusters. We hypothesize that different forces acting on female bottlenose dolphin sociality appear to promote the formation of flexible groups which include both kin and nonkin.

Habitat type promotes rapid and extremely localised genetic differentiation in dolphins

The high potential for dispersal of many marine organisms often results in low population differentiation over large distances. Here, we report that dolphin communities living in very close geographic proximity (<16 km) but in two different environments – open coast and enclosed embayment – exhibit unexpected genetic differentiation at nine microsatellite loci. Results based on a fixation index and a Bayesian clustering approach suggested that gene flow between communities within an embayment is high, as is gene flow between coastal communities. However, lower gene flow between embayment and open coast communities translated into substantial genetic differentiation between dolphin communities from the two environments, and assignment of individuals into two populations. Along with patterns observed in 403 bp of the mitochondrial DNA control region, the results suggest that restriction of gene flow likely occurred in the last 6000 years, after coastal dolphins colonised the embayment. We hypothesise that factors such as fidelity to the local area and resource and behavioural specialisations may have played a major role in promoting and maintaining genetic subdivision between dolphins of the two environments. Importantly, our study shows that habitat type can rapidly promote extremely fine-scale genetic structure in a long-lived, highly mobile marine mammal.

Environmental and social influences on the genetic structure of bottlenose dolphins (Tursiops aduncus) in Southeastern Australia

Determining genetic connectivity of bottlenose dolphin communities helps identify evolutionary mechanisms, such as environmental and social factors, that interact to shape dispersal in highly social marine mammals. Here, we expand on a localized study that found marked genetic differentiation among resident dolphins (Tursiops aduncus) in the Port Stephens embayment and adjacent coastal communities, to include four additional communities inhabiting different environment types along the New South Wales coast, Southeastern Australia. Analysis of the mitochondrial DNA control region and seven microsatellite loci suggest the nine communities may have originated from a single ancestral population that progressively colonised the coast in a southward direction. Gene flow among communities was predominately governed by habitat type. The two enclosed embayments showed the highest level of genetic differentiation from other communities, while genetic differentiation among coastal and open embayment communities generally followed a pattern of isolation by distance. Directional bias in recent migration rates was evident, with the centrally located Hunter coast communities consisting of individuals with mixed ancestry from the Northern, Southern and Port Stephens communities. Emigration from Port Stephens was substantially higher than in the opposite direction, indicating there may be social barriers to dispersal created by Port Stephens dolphins. Our results suggest that the scale of connectivity of bottlenose dolphin communities inhabiting heterogeneous environments is likely to be affected by local habitat adaptation. This has important implications for the management of communities exposed to increasing levels of anthropogenic disturbances, such as the intensive commercial dolphin-watching industry operating in Port Stephens.

Population differentiation and hybridisation of Australian snubfin (Orcaella heinsohni) and Indo-Pacific humpback (Sousa chinensis) dolphins in North-Western Australia

Little is known about the Australian snubfin (Orcaella heinsohni) and Indo-Pacific humpback (Sousa chinensis) dolphins (‘snubfin’ and ‘humpback dolphins’, hereafter) of north-western Australia. While both species are listed as ‘near threatened’ by the IUCN, data deficiencies are impeding rigorous assessment of their conservation status across Australia. Understanding the genetic structure of populations, including levels of gene flow among populations, is important for the assessment of conservation status and the effective management of a species. Using nuclear and mitochondrial DNA markers, we assessed population genetic diversity and differentiation between snubfin dolphins from Cygnet (n = 32) and Roebuck Bays (n = 25), and humpback dolphins from the Dampier Archipelago (n = 19) and the North West Cape (n = 18). All sampling locations were separated by geographic distances >200 km. For each species, we found significant genetic differentiation between sampling locations based on 12 (for snubfin dolphins) and 13 (for humpback dolphins) microsatellite loci (F ST = 0.05–0.09; P<0.001) and a 422 bp sequence of the mitochondrial control region (F ST = 0.50–0.70; P<0.001). The estimated proportion of migrants in a population ranged from 0.01 (95% CI 0.00–0.06) to 0.13 (0.03–0.24). These are the first estimates of genetic diversity and differentiation for snubfin and humpback dolphins in Western Australia, providing valuable information towards the assessment of their conservation status in this rapidly developing region. Our results suggest that north-western Australian snubfin and humpback dolphins may exist as metapopulations of small, largely isolated population fragments, and should be managed accordingly. Management plans should seek to maintain effective population size and gene flow. Additionally, while interactions of a socio-sexual nature between these two species have been observed previously, here we provide strong evidence for the first documented case of hybridisation between a female snubfin dolphin and a male humpback dolphin.

Abundance, survival and temporary emigration of bottlenose dolphins (Tursiops sp.) off Useless Loop in the western gulf of Shark Bay, Western Australia

Capture–recapture models were used to provide estimates of abundance, apparent survival and temporary emigration of Indo-Pacific bottlenose dolphins (Tursiops sp.) in a 226-km2 study area off Useless Loop in the western gulf of Shark Bay, Western Australia. Photo-identification data were collected during boat-based surveys in Austral autumn to early spring (April–September) from 2007 to 2011. Abundance estimates varied from 115 (s.e. 5.2, 95% CI 105–126) individuals in 2008 to 208 (s.e. 17.3, 95% CI 177–245) individuals in 2010. The variability in abundance estimates is likely to be a reflection of how individuals used the study area, rather than fluctuations in true population size. The best fitting capture–recapture model suggested a random temporary emigration pattern and, when coupled with relatively high temporary emigration rates (0.33 (s.e. 0.07) – 0.66 (s.e. 0.05)) indicated that the study area did not cover the entire ranges of the photo-identified dolphins. Apparent survival rate is a product of true survival and permanent emigration and was estimated annually at 0.95 (s.e. 0.02). Since permanent emigration from the study area is unlikely, true survival was estimated to be close to 0.95. This study provides a robust baseline for future comparisons of dolphin demographics, which may be of importance should climate change or increasing anthropogenic activity affect this population.

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.

Genes or Culture: Are Mitochondrial Genes Associated with Tool Use in Bottlenose Dolphins (Tursiops sp.)?

Some bottlenose dolphins use marine sponges as foraging tools (‘sponging’), which appears to be socially transmitted from mothers mainly to their female offspring. Yet, explanations alternative to social transmission have been proposed. Firstly, the propensity to engage in sponging might be due to differences in diving ability caused by variation of mitochondrial genes coding for proteins of the respiratory chain. Secondly, the cultural technique of sponging may have selected for changes in these same genes (or other autosomal ones) among its possessors. We tested whether sponging can be predicted by mitochondrial coding genes and whether these genes are under selection. In 29 spongers and 54 non-spongers from two study sites, the non-coding haplotype at the HVRI locus was a significant predictor of sponging, whereas the coding mitochondrial genes were not. There was no evidence of selection in the investigated genes. Our study shows that mitochondrial gene variation is unlikely to be a viable alternative to cultural transmission as a primary driver of tool use in dolphins.

Sex-Specific Patterns in Abundance, Temporary Emigration and Survival of Indo-Pacific Bottlenose Dolphins (Tursiops aduncus) in Coastal and Estuarine Waters

Inherent difficulties in determining the sex of free-ranging sexually monomorphic species often prevents a sex-specific focus on estimating abundance, movement patterns and survival rates. This study provides insights into sex-specific population parameters of Indo-Pacific bottlenose dolphins (Tursiops aduncus). Systematic, boat-based photo-identification surveys (n = 417) were conducted year-round from 2007-2013 in coastal and estuarine waters off Bunbury, Western Australia. Pollock’s Robust Design was used to quantify population parameters for three datasets: i) adults and juveniles combined, ii) adult females and iii) adult males. For all datasets, abundance estimates varied seasonally, with general highs during summer and/or autumn, and lows during winter. Dolphins had seasonally structured temporary emigration rates with similar trends between sexes. The derived return rate (1-γ’) of temporary emigrants into the study area was highest from winter to spring, indicating that dolphins had a high probability of return into the study area during spring. We suggest that the return of dolphins into the study area and increase in abundance is influenced by the breeding season (summer/autumn). Prey availability is likely a main driver responsible for the movement of dolphins out of the study area during winter. Seasonal apparent survival rates were constant and high (0.98-0.99) for all datasets. High apparent survival rates suggest there is no permanent emigration from the study area. Our sex-specific modeling approach offers a comprehensive interpretation of the population dynamics of a top predator in a coastal and estuarine environment and acts as a model for future sex-based population studies on sexually monomorphic species.

Site-specific assessments of the abundance of three inshore dolphin species to inform conservation and management

Assessing the abundance of wildlife populations is essential to their effective conservation and management. Concerns have been raised over the vulnerability of tropical inshore dolphins in waters off northern Australia to anthropogenic impacts on local populations, yet a lack of abundance data precludes assessment of their conservation status and the management of threats. Using small vessels as cost-effective research platforms, photo-identification surveys and capture-recapture models were applied to provide the first quantitative abundance data for Australian snubfin (Orcaella heinsohni), Australian humpback (Sousa sahulensis), and Indo-Pacific bottlenose dolphins (Tursiops aduncus) at five sites in the Kimberley region of north-western Australia. The abundance of each species was highly variable between different sites, likely reflecting species-specific habitat preferences. Within the c. 130 km2 study sites, the estimated abundance of most species was ≤ 60 individuals (excluding calves), and fewer than 20 humpback dolphins were identified at each site in any one 3-5 week sampling period. However, larger estimates of c. 130 snubfin and c. 160 bottlenose dolphins were obtained at two different sites. Several local populations showed evidence of site fidelity, particularly snubfin dolphins. By implementing a standardized, multi-site approach, data on local populations were provided within a broader, regional context, and indicated that each species is patchily distributed in the region. This highlights the need for site-specific baseline data collection using appropriate survey techniques to quantitatively assess the potential impacts of threatening activities to local populations. These findings further illustrate the need to gain a greater understanding of known and potential threats to inshore dolphin populations, their relative impacts, and to mitigate where necessary. In particular, the level of interactions with inshore gillnet fisheries requires urgent assessment. An ideal candidate site for a long-term study of snubfin dolphin population dynamics is identified, where trends in abundance and their influencing factors could be investigated. The methods employed herein provide an example of rigorous, site-specific population assessments of inshore dolphins that are broadly applicable to such studies elsewhere.