Undersea Constellations: The Global Biology of an Endangered Marine Megavertebrate Further Informed through Citizen Science

The whale shark is an ideal flagship species for citizen science projects because of its charismatic nature, its size, and the associated ecotourism ventures focusing on the species at numerous coastal aggregation sites. An online database of whale shark encounters, identifying individuals on the basis of their unique skin patterning, captured almost 30,000 whale shark encounter reports from 1992 to 2014, with more than 6000 individuals identified from 54 countries. During this time, the number of known whale shark aggregation sites (hotspots) increased from 13 to 20. Examination of photo-identification data at a global scale revealed a skewed sex-ratio bias toward males (overall, more than 66%) and high site fidelity among individuals, with limited movements of sharks between neighboring countries but no records confirming large, ocean basin-scale migrations. Citizen science has been vital in amassing large spatial and temporal data sets to elucidate key aspects of whale shark life history and demographics and will continue to provide substantial long-term value

Global collision-risk hotspots of marine traffic and the world’s largest fish, the whale shark

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Womersley, F. C., Humphries, N. E., Queiroz, N., Vedor, M., da Costa, I., Furtado, M., Tyminski, J. P., Abrantes, K., Araujo, G., Bach, S. S., Barnett, A., Berumen, M. L., Bessudo Lion, S., Braun, C. D., Clingham, E., Cochran, J. E. M., de la Parra, R., Diamant, S., Dove, A. D. M., Dudgeon, C. L., Erdmann, M. V., Espinoza, E., Fitzpatrick, R., González Cano, J., Green, J. R., Guzman, H. M., Hardenstine, R., Hasan, A., Hazin, F. H. V., Hearn, A. R., Hueter, R. E., Jaidah, M. Y., Labaja, J., Ladinol, F., Macena, B. C. L., Morris Jr., J. J., Norman, B. M., Peñaherrera-Palmav, C., Pierce, S. J., Quintero, L. M., Ramırez-Macías, D., Reynolds, S. D., Richardson, A. J., Robinson, D. P., Rohner, C. A., Rowat, D. R. L., Sheaves, M., Shivji, M. S., Sianipar, A. B., Skomal, G. B., Soler, G., Syakurachman, I., Thorrold, S. R., Webb, D. H., Wetherbee, B. M., White, T. D., Clavelle, T., Kroodsma, D. A., Thums, M., Ferreira, L. C., Meekan, M. G., Arrowsmith, L. M., Lester, E. K., Meyers, M. M., Peel, L. R., Sequeira, A. M. M., Eguıluz, V. M., Duarte, C. M., & Sims, D. W. Global collision-risk hotspots of marine traffic and the world’s largest fish, the whale shark. Proceedings of the National Academy of Sciences of the United States of America, 119(20), (2022): e2117440119, https://doi.org/10.1073/pnas.2117440119.Marine traffic is increasing globally yet collisions with endangered megafauna such as whales, sea turtles, and planktivorous sharks go largely undetected or unreported. Collisions leading to mortality can have population-level consequences for endangered species. Hence, identifying simultaneous space use of megafauna and shipping throughout ranges may reveal as-yet-unknown spatial targets requiring conservation. However, global studies tracking megafauna and shipping occurrences are lacking. Here we combine satellite-tracked movements of the whale shark, Rhincodon typus, and vessel activity to show that 92% of sharks’ horizontal space use and nearly 50% of vertical space use overlap with persistent large vessel (>300 gross tons) traffic. Collision-risk estimates correlated with reported whale shark mortality from ship strikes, indicating higher mortality in areas with greatest overlap. Hotspots of potential collision risk were evident in all major oceans, predominantly from overlap with cargo and tanker vessels, and were concentrated in gulf regions, where dense traffic co-occurred with seasonal shark movements. Nearly a third of whale shark hotspots overlapped with the highest collision-risk areas, with the last known locations of tracked sharks coinciding with busier shipping routes more often than expected. Depth-recording tags provided evidence for sinking, likely dead, whale sharks, suggesting substantial “cryptic” lethal ship strikes are possible, which could explain why whale shark population declines continue despite international protection and low fishing-induced mortality. Mitigation measures to reduce ship-strike risk should be considered to conserve this species and other ocean giants that are likely experiencing similar impacts from growing global vessel traffic.Funding for data analysis was provided by the UK Natural Environment Research Council (NERC) through a University of Southampton INSPIRE DTP PhD Studentship to F.C.W. Additional funding for data analysis was provided by NERC Discovery Science (NE/R00997/X/1) and the European Research Council (ERC-AdG-2019 883583 OCEAN DEOXYFISH) to D.W.S., Fundação para a Ciência e a Tecnologia (FCT) under PTDC/BIA/28855/2017 and COMPETE POCI-01–0145-FEDER-028855, and MARINFO–NORTE-01–0145-FEDER-000031 (funded by Norte Portugal Regional Operational Program [NORTE2020] under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund–ERDF) to N.Q. FCT also supported N.Q. (CEECIND/02857/2018) and M.V. (PTDC/BIA-COM/28855/2017). D.W.S. was supported by a Marine Biological Association Senior Research Fellowship. All tagging procedures were approved by institutional ethical review bodies and complied with all relevant ethical regulations in the jurisdictions in which they were performed. Details for individual research teams are given in SI Appendix, section 8. Full acknowledgments for tagging and field research are given in SI Appendix, section 7. This research is part of the Global Shark Movement Project (https://www.globalsharkmovement.org)

Emergent community architecture despite distinct diversity in the global whale shark (Rhincodon typus) epidermal microbiome

Abstract Microbiomes confer beneficial physiological traits to their host, but microbial diversity is inherently variable, challenging the relationship between microbes and their contribution to host health. Here, we compare the diversity and architectural complexity of the epidermal microbiome from 74 individual whale sharks (Rhincodon typus) across five aggregations globally to determine if network properties may be more indicative of the microbiome-host relationship. On the premise that microbes are expected to exhibit biogeographic patterns globally and that distantly related microbial groups can perform similar functions, we hypothesized that microbiome co-occurrence patterns would occur independently of diversity trends and that keystone microbes would vary across locations. We found that whale shark aggregation was the most important factor in discriminating taxonomic diversity patterns. Further, microbiome network architecture was similar across all aggregations, with degree distributions matching Erdos–Renyi-type networks. The microbiome-derived networks, however, display modularity indicating a definitive microbiome structure on the epidermis of whale sharks. In addition, whale sharks hosted 35 high-quality metagenome assembled genomes (MAGs) of which 25 were present from all sample locations, termed the abundant ‘core’. Two main MAG groups formed, defined here as Ecogroup 1 and 2, based on the number of genes present in metabolic pathways, suggesting there are at least two important metabolic niches within the whale shark microbiome. Therefore, while variability in microbiome diversity is high, network structure and core taxa are inherent characteristics of the epidermal microbiome in whale sharks. We suggest the host-microbiome and microbe-microbe interactions that drive the self-assembly of the microbiome help support a functionally redundant abundant core and that network characteristics should be considered when linking microbiomes with host health