This week sees another paper out of our long-term research in the eastern and western gulfs of Shark Bay. It includes science AND pretty pictures!

Title: Vocal behaviour of allied male dolphins during cooperative mate guarding.

Authors: King SL, Allen SJ, Krützen M, Connor RC.

Get your piece of this open-access action right here: https://doi.org/10.1007/s10071-019-01290-1

Abstract: Coercive mate guarding, where males use aggression to control female movements, is a form of sexual coercion which functions to constrain female mate choice. Non-human primates, for example, herd females to keep them away from competing males, but male bottlenose dolphins (Tursiops aduncus) also herd females to keep them close to their alliance partners. Indeed, pairs and trios of male dolphins work together to sequester single estrus females and defend them from competing alliances. Yet how males facilitate such coordination remains unknown. Here, we investigate the vocal behaviour of allied male bottlenose dolphins during the herding of individual females, examining how the production of whistles and ‘pops’ (a threat vocalisation) varied with behavioural state and inter-animal distances. Allied males produced both whistles and pops significantly more often and at higher rates during social interactions, though they differed in function. Whistle rates increased significantly when new individuals joined the consorting group, consistent with previous work showing that whistles are part of a greeting sequence for this species. Whistle matching also appeared to play a role in within-alliance coordination. Pop vocalisations increased significantly when the nearest male to the female changed, likely inducing the female to remain close as the males coordinate a guard switch. Building upon prior research examining female movements in response to pops, we show that males approach the female and current guard whilst popping, leading to a guard switch. Our results provide new insights into the use of vocal signals during cooperative mate guarding between allied male dolphins.

Full citation: King SL, Allen SJ, Krützen M and Connor RC 2019. Vocal behaviour of allied male dolphins during cooperative mate guarding. Animal Cognition https://doi.org/10.1007/s10071-019-01290-1

Ethics: Permits for the use of animals for scientific purposes were obtained from the Department of Biodiversity, Conservation and Attractions. The University of Zurich and University of Western Australia granted animal ethics approvals.

Funding: SLK was supported by The Branco Weiss Fellowship – Society in Science. SLK and RCC were supported by the National Geographic Society (050R-17). MK was supported by the Swiss National Science Foundation (31003A_149956).

Acknowledgements: We thank RAC Monkey Mia, Shark Bay rangers (Department of Biodiversity, Conservation and Attractions), Shark Bay Resources, the Useless Loop community and all field assistants for help in this study. We thank David Allen of Wolf Design Limited (www.wolfd esign ltd.co.uk) for the dolphin template in Fig. 3b. Lastly, we thank two anonymous reviewers and the handling editor for their valuable comments on the manuscript.

Blurb: The beautiful and remote Shark Bay World Heritage Area (and Marine Protected Area) is home to the only known communities of tool-using dolphins on Planet Ocean. Only certain matrilines of dolphins engage in the tool-using behaviour, wearing basket sponges over the beaks/rostra as they forage. It’s thought to act as a protective ‘glove’ against sharp rocks, stingray barbs and the dorsal spines on some fish as the dolphins probe the sea floor.

There’s a general female-bias to this behaviour, with a much greater proportion of female calves adopting the behaviour her mum performs than do young males. This difference was long thought to be explained by the incompatibility of such a solitary and time-consuming behaviour with a male lifestyle – who should instead be investing time and energy into formulating alliances with other males.

Well, after a fateful survey in the western gulf of Shark Bay in May 2011, however, we discovered the existence of male alliances of sponging dolphins. About 8 years and two weeks later, here is the paper explaining this phenomenon.

Highlights: Diving into the behaviour of male dolphins that engage in tool-use for the first time and comparing them to non-tool-using males, we found that:

• The male spongers spend more time associating with other male spongers than they do non-spongers, irrespective of relatedness or other factors.
• They also devote more time to foraging and less time to resting and travelling than do non-sponging males.
• Nevertheless, they spend just as much time socialising as do non-spongers.
• Our study indicates social homophily in the second-order alliance composition of tool-using bottlenose dolphins.

Title: Tool use and social homophily among male bottlenose dolphins.

Authors: Bizzozzero MR, Allen SJ, Gerber L, Wild S, King SL, Connor RC, Friedman WR, Wittwer S, Krützen M.

Abstract: Homophilous behaviour plays a central role in the formation of human friendships. Individuals form social ties with others that show similar phenotypic traits, independently of relatedness. Evidence of such homophily can be found in bottlenose dolphins (Tursiops aduncus) in Shark Bay, Western Australia, where females that use marine sponges as foraging tools often associate with other females that use sponges. ‘Sponging’ is a socially learned, time-consuming behaviour, transmitted from mother to calf. Previous research illustrated a strong female bias in adopting this technique. The lower propensity for males to engage in sponging may be due to its incompatibility with adult male-specific behaviours, particularly the formation of multi-level alliances. However, the link between sponging and male behaviour has never been formally tested. Here, we show that male spongers associated significantly more often with other male spongers irrespective of their level of relatedness. Male spongers spent significantly more time foraging, and less time resting and travelling, than did male non-spongers. Interestingly, we found no difference in time spent socializing. Our study provides novel insights into the relationship between tool use and activity budgets of male dolphins, and indicates social homophily in the second-order alliance composition of tool-using bottlenose dolphins.  

Full citation: Bizzozzero MR, Allen SJ, Gerber L, Wild S, King SL, Connor RC, Friedman WR, Wittwer S, Krützen M. 2019 Tool use and social homophily among male bottlenose dolphins. Proc. R. Soc. B 286: 20190898. http://dx.doi.org/10.1098/rspb.2019.0898

Funding: This study was supported by a Swiss National Science Foundation grant 31003A_149956) to M.K. Further financial assistance was provided by grants from the National Geographic Society, W. V. Scott Foundation, Sea World Research and Rescue Foundation Inc., A. H. Schultz Stiftung, and the University of Zurich. S.L.K. was supported by The Branco Weiss Fellowship—Society in Science. W.R.F. was supported by a Graduate Fellowship in Anthropogeny from the University of California, San Diego.

Acknowledgements: We thank Shark Bay Resources and the Useless Loop community for their generous, long-term, in-kind and logistical support. We also thank all field assistants for their help during this study.

Title: Is MHC diversity a better marker for conservation than neutral genetic diversity? A case study of two contrasting dolphin populations.

Authors: Manlik O, Krützen M, Kopps AM, Mann J, Bejder L, Allen SJ, Frère C, Connor RC, Sherwin WB.

Abstract: 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.

Our findings are consistent with the hypothesis that viable populations typically display greater genetic diversity than less viable populations. The results also suggest that MHC variation is more closely associated with population viability than neutral genetic variation. Although the inferences from our findings are limited, because we only compared two populations, our results add to a growing number of studies that highlight the usefulness of MHC as a potentially suitable genetic marker for animal conservation. The Shark Bay population, which carries greater adaptive genetic diversity than the Bunbury population, is thus likely more robust to natural or human‐induced changes to the coastal ecosystem it inhabits.

Full citation: Manlik O, Krützen M, Kopps AM, Mann J, Bejder L, Allen SJ, Frère C, Connor RC, Sherwin WB 2019. Is MHC diversity a better marker for conservation than neutral genetic diversity? A case study of two contrasting dolphin populations. Ecology and Evolution 2019;00: 1-13 DOI: 10.1002/ECE3.5265

Funding: WV Scott Foundation; National Science Foundation, Grant/Award Number: 0918308, 0941487 and 1559380; Sea World Research and Rescue Foundation, Grant/Award Number: RM09107; NSERC; National Geographic Society; PADI Foundation; Australian Research Council; Shark Bay Shire; United Arab Emirates University.

Feature image: This tiny calf of “Sunny”, a sponging mother dolphin in Shark Bay, did not make it to one year of age in the hard times following a marine heatwave.

Blurb: The remote and beautiful Shark Bay World Heritage Area (and marine park) got itself into some hot water in the summer of 2011. Various negative impacts across trophic levels followed this unprecedented marine heat wave, exacerbated by some anomalous flooding events, including the loss of habitat-forming seagrass meadows, crashes in invertebrate and fish populations, as well declines in marine turtle health.

For a little not-so-light reading, check out these prior papers by our friends and colleagues: Thomson et al. (2015). Extreme temperatures, foundation species, and abrupt ecosystem change: an example from an iconic seagrass ecosystem. Global Change Biology 21:1463–1474. And: Arias-Ortiz et al. (2018). A marine heatwave drives massive losses from the world’s largest seagrass carbon stocks. Nature Climate Change 8: 338–344.

Piccolo, daughter of Puck, is a famous Shark Bay dolphin. Here, she works hard to round up a bream in the shallows of Monkey Mia beach.

Highlights:This should probably read “lowlights” but, in this paper, we used our long-term demographic data to report on the subsequent (arguably cascading) effects of habitat degradation on the survival and reproduction of the iconic bottlenose dolphin population that inhabits this globally unique ecosystem.

Title: Long-term decline in survival and reproduction of dolphins following a marine heatwave. 

Authors: Sonja Wild, Michael Krützen, Robert W Rankin, Will JE Hoppitt, Livia Gerber, Simon J Allen.

Abstract: It’s a two-page correspondence piece, so there isn’t really an abstract per se, but here is the first paragraph, a pseudo-abstract of sorts: One of many challenges in the conservation of biodiversity is the recent trend in the frequency and intensity of extreme climatic events. The Shark Bay World Heritage Area, Western Australia, endured an unprecedented marine heatwave in 2011. Catastrophic losses of habitat-forming seagrass meadows followed, along with mass mortalities of invertebrate and fish communities. Our long-term demographic data on Shark Bay’s resident Indo-Pacific bottlenose dolphin (Tursiops aduncus) population revealed a significant decline in female reproductive rates following the heatwave. Moreover, capture–recapture analyses indicated 5.9% and 12.2% post heatwave declines in the survival of dolphins that use tools to forage and those that do not, respectively. This implies that the tool-using dolphins may have been somewhat buffered against the cascading effects of habitat loss following the heatwave by having access to a less severely affected foraging niche. Overall, however, lower survival has persisted post-heatwave, suggesting that habitat loss following extreme weather events may have prolonged, negative impacts on even behaviourally flexible, higher-trophic level predators.

Oakley and calf cruise over the seagrass and sand in western Shark Bay.

Full citation: Wild S, Krützen M, Rankin RW, Hoppitt WJE, Gerber L and Allen SJ. 2019. Long-term decline in survival and reproduction of dolphins following a marine heatwave. Current Biology 29: R1-R2. DOI: 10.1016/j.cub.2019.02.047

Funding and acknowledgements: This research was funded by grants from the Swiss Science Foundation, National Geographic Society, Sea World Research and Rescue Foundation, WV Scott Foundation and the AH Schultz Stiftung. We thank Mitsui, Shark Bay Resources, and the Useless Loop community for in-kind support, and field assistants for contributions to data collection. This research was conducted with scientific investigation permits from the Department of Biodiversity, Conservation and Attractions, as well as animal ethics approvals from the University of Zurich, University of Western Australia, Murdoch University and the University of New South Wales.

An alliance of males follows the foraging female in western Shark Bay. We hope we are not consigned to documenting the demise of the remarkable wildlife population.

Watch this space for more research findings in the coming months…

Happy 2018! Time for a quick update: The last year has been a productive one for the Shark Bay Dolphin Research Alliance (SBDRA), with successful field seasons in both eastern (#36!) and western (#11) gulfs, a solid showing at the 22^nd Biennial Conference in Halifax, Nova Scotia, and a number of papers published.

With field seasons wrapped up, we went on our way to Canada for the conference. Quite a few of us shared flights with other members of the group, plus colleagues from other labs. In various airports, we’d find the time to catch up and talk marine mammal science… oh wait. No, we wouldn’t. We’d just stare at our mobile devices…

Members of the SBDRA gave eight oral presentations and one poster presentation…

We also had a lovely ‘Friends of Shark Bay’ dinner for a gaggle of researchers past, present and future…

Amongst a few others, we published a paper on male alliance behaviour and mating access in the open social network of Shark Bay’s bottlenose dolphins (http://www.nature.com/articles/srep46354) in Nature’s Scientific Reports.

Also in Scientific Reports, another on sexual displays involving posturing and sponge presentation by male Australian humpback dolphins across north-western Australia (http://rdcu.be/w3tL).

There are so many intriguing parallels in behaviour and social complexity that exist between some of the cetacea and the great apes, but who would have thought that one charismatic, tool-using species might remain undiscovered until late 2017!? Congrats to Michael and colleagues on this wonderful result: http://www.cell.com/current-biology/fulltext/S0960-9822(17)31245-9.

2018 is shaping up to be a bumper year for papers and fieldwork. We look forward to sharing it with you, so stay tuned…