Tracking 4 years in the life of a female whale shark shows consistent migrations in the Gulf of Mexico and Caribbean
Daniel Daye
A , Rafael de la Parra B , Jeremy Vaudo C , Jessica Harvey D , Guy Harvey D , Mahmood Shivji C and Bradley Wetherbee A C *
A
B
C
D
Abstract
Satellite telemetry has revolutionised the study of animal movement, particularly for mobile marine animals, whose movements and habitat make consistent, long-term observation difficult.
Summarise the movements of Rio Lady, a mature female whale shark (Rhincodon typus), to characterise these movements, and to predict expected behaviour throughout the Gulf of Mexico (GOM).
Rio Lady was tracked using satellite telemetry for over 1600 days, generating over 1400 locations and travelling over 40,000 km. State–space and move persistence modelling enabled characterisation of behaviour, and machine learning (ML) enabled the development of habitat-suitability models to predict habitat utilisation, on the basis of location transmissions and their environmental covariates.
Rio Lady exhibited annually consistent patterns of movements among three regions within the GOM. Final ML models produced seasonally dynamic predictions of habitat use throughout the GOM.
The application of these methods to long-term location data exemplifies how long-term movement patterns and core areas can be discovered and predicted for marine animals.
Despite our limited dataset, our integrative approach advances methods to summarise and predict behaviour of mobile species and improve understanding of their ecology.
Keywords: behaviour, conservation, habitat suitability, machine learning, movement ecology, remote sensing, Rhincodon typus, satellite telemetry.
References
Allen AM, Singh NJ (2016) Linking movement ecology with wildlife management and conservation. Frontiers in Ecology and Evolution 3, 155.
| Crossref | Google Scholar |
Azur MJ, Stuart EA, Frangakis C, Leaf PJ (2011) Multiple imputation by chained equations: what is it and how does it work? International Journal of Methods in Psychiatric Research 20, 40-49.
| Crossref | Google Scholar | PubMed |
Barry C, Legaspi C, Clarke TM, Araujo G, Bradshaw CJA, Gleiss AC, Meyer L, Huveneers C (2023) Estimating the energetic cost of whale shark tourism. Biological Conservation 284, 110164.
| Crossref | Google Scholar |
Berumen ML, Braun CD, Cochran JEM, Skomal GB, Thorrold SR (2014) Movement patterns of juvenile whale sharks tagged at an aggregation site in the Red Sea. PLoS ONE 9, e103536.
| Crossref | Google Scholar | PubMed |
Braun CD, Gaube P, Sinclair-Taylor TH, Skomal GB, Thorrold SR (2019) Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone. Proceedings of the National Academy of Sciences 116, 17187-17192.
| Crossref | Google Scholar |
Breiman L (2001) Random forests. Machine Learning 45, 5-32.
| Crossref | Google Scholar |
Brunnschweiler JM, Baensch H, Pierce SJ, Sims DW (2009) Deep-diving behaviour of a whale shark Rhincodon typus during long-distance movement in the western Indian Ocean. Journal of Fish Biology 74, 706-714.
| Crossref | Google Scholar | PubMed |
Chambault P, Fossette S, Heide-Jørgensen MP, Jouannet D, Vély M (2021) Predicting seasonal movements and distribution of the sperm whale using machine learning algorithms. Ecology and Evolution 11, 1432-1445.
| Crossref | Google Scholar | PubMed |
Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annual Review of Marine Science 7, 547-570.
| Crossref | Google Scholar | PubMed |
Cochran JEM, Braun CD, Cagua EF, Campbell MF Jr, Hardenstine RS, Kattan A, Priest MA, Sinclair-Taylor TH, Skomal GB, Sultan S, Sun L, Thorrold SR, Berumen ML (2019) Multi-method assessment of whale shark (Rhincodon typus) residency, distribution, and dispersal behavior at an aggregation site in the Red Sea. PLoS ONE 14, e0222285.
| Crossref | Google Scholar | PubMed |
Colman JG (1997) A review of the biology and ecology of the whale shark. Journal of Fish Biology 51, 1219-1234.
| Crossref | Google Scholar | PubMed |
Compagno LJV (2001) Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2. Bullhead, mackerel, and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO Species Catalogue for Fishery Purposes Number 1, Vol. 2. (Food and Agriculture Organization of the United Nations: Rome, Italy) Available at https://www.iucnssg.org/uploads/5/4/1/2/54120303/fao_species_catalogue_for_fishery_purposes_-_2001_-_sharks_of_the_world_-_an_annotated_and_illustrated_catalogue_of_shark_species_known_to_date_-_volume_2_-_bullhead_mackerel_and_carpet_sharks.pdf
Cruz-Castán R, Meiners-Mandujano C, Macías D, Jiménez-Badillo L, Curiel-Ramírez S (2019) Reproductive biology of little tunny Euthynnus alletteratus (Rafinesque, 1810) in the southwest Gulf of Mexico. PeerJ 7, e6558.
| Crossref | Google Scholar | PubMed |
Daye D (2023) Predicting habitat suitability of migratory sharks using machine learning methods. MSc(BESc) thesis, University of Rhode Island, College of the Environment and Life Sciences, Kingston, RI, USA. doi:10.23860/thesis-daye-daniel-2023
de la Parra Venegas R, Hueter R, González Cano J, Tyminski J, Gregorio Remolina J, Maslanka M, Ormos A, Weigt L, Carlson B, Dove A (2011) An unprecedented aggregation of whale sharks, Rhincodon typus, in Mexican coastal waters of the Caribbean Sea. PLoS ONE 6, e18994.
| Crossref | Google Scholar | PubMed |
Dinnel SP, Wiseman WJ, Jr (1986) Fresh water on the Louisiana and Texas shelf. Continental Shelf Research 6, 765-784.
| Crossref | Google Scholar |
Domeier ML, Nasby-Lucas N (2008) Migration patterns of white sharks Carcharodon carcharias tagged at Guadalupe Island, Mexico, and identification of an eastern Pacific shared offshore foraging area. Marine Ecology Progress Series 370, 221-237.
| Crossref | Google Scholar |
Dove ADM (2015) Foraging and ingestive behaviors of whale sharks, Rhincodon typus, in response to chemical stimulus cues. The Biological Bulletin 228, 65-74.
| Crossref | Google Scholar | PubMed |
Dunn DC, Crespo GO, Halpin PN (2019) Incorporating the dynamic and connected nature of the open ocean into governance of marine biodiversity beyond national jurisdiction. In ‘Predicting future oceans’. (Eds AM Cisneros-Montemayor, WWL Cheung, Y Ota) pp. 425–435. (Elsevier) doi:10.1016/B978-0-12-817945-1.00041-1
Eckert SA, Stewart BS (2001) Telemetry and satellite tracking of whale sharks, Rhincodon typus, in the Sea of Cortez, Mexico, and the North Pacific Ocean. Environmental Biology of Fishes 60, 299-308.
| Crossref | Google Scholar |
Fan J, Samworth R, Wu Y (2009) Ultrahigh dimensional feature selection: beyond the linear model. Journal of Machine Learning Research 10, 2013-2038.
| Google Scholar | PubMed |
Friedlaender AS, Halpin PN, Qian SS, Lawson GL, Wiebe PH, Thiele D, Read AJ (2006) Whale distribution in relation to prey abundance and oceanographic processes in shelf waters of the Western Antarctic Peninsula. Marine Ecology Progress Series 317, 297-310.
| Crossref | Google Scholar |
Gleiss AC, Norman B, Wilson RP (2011) Moved by that sinking feeling: variable diving geometry underlies movement strategies in whale sharks. Functional Ecology 25, 595-607.
| Crossref | Google Scholar |
Grémillet D, Chevallier D, Guinet C (2022) Big data approaches to the spatial ecology and conservation of marine megafauna. ICES Journal of Marine Science 79, 975-986.
| Crossref | Google Scholar |
Guzman HM, Gomez CG, Hearn A, Eckert SA (2018) Longest recorded trans-Pacific migration of a whale shark (Rhincodon typus). Marine Biodiversity Records 11, 8.
| Crossref | Google Scholar |
Guzman HM, Collatos CM, Gomez CG (2022) Movement, behavior, and habitat use of whale sharks (Rhincodon typus) in the Tropical Eastern Pacific Ocean. Frontiers in Marine Science 9, 793248.
| Crossref | Google Scholar |
Hays GC, Hawkes LA (2018) Satellite tracking sea turtles: opportunities and challenges to address key questions. Frontiers in Marine Science 5, 432.
| Crossref | Google Scholar |
Hays GC, Ferreira LC, Sequeira AMM, Meekan MG, Duarte CM, Bailey H, Bailleul F, Bowen WD, Caley MJ, Costa DP, Eguíluz VM, Fossette S, Friedlaender AS, Gales N, Gleiss AC, Gunn J, Harcourt R, Hazen EL, Heithaus MR, Heupel M, Holland K, Horning M, Jonsen I, Kooyman GL, Lowe CG, Madsen PT, Marsh H, Phillips RA, Righton D, Ropert-Coudert Y, Sato K, Shaffer SA, Simpfendorfer CA, Sims DW, Skomal G, Takahashi A, Trathan PN, Wikelski M, Womble JN, Thums M (2016) Key questions in marine megafauna movement ecology. Trends in Ecology & Evolution 31, 463-475.
| Crossref | Google Scholar | PubMed |
Hays GC, Bailey H, Bograd SJ, Bowen WD, Campagna C, Carmichael RH, Casale P, Chiaradia A, Costa DP, Cuevas E, Nico de Bruyn PJ, Dias MP, Duarte CM, Dunn DC, Dutton PH, Esteban N, Friedlaender A, Goetz KT, Godley BJ, Halpin PN, Hamann M, Hammerschlag N, Harcourt R, Harrison A-L, Hazen EL, Heupel MR, Hoyt E, Humphries NE, Kot CY, Lea JSE, Marsh H, Maxwell SM, McMahon CR, Notarbartolo di Sciara G, Palacios DM, Phillips RA, Righton D, Schofield G, Seminoff JA, Simpfendorfer CA, Sims DW, Takahashi A, Tetley MJ, Thums M, Trathan PN, Villegas-Amtmann S, Wells RS, Whiting SD, Wildermann NE, Sequeira AMM (2019) Translating marine animal tracking data into conservation policy and management. Trends in Ecology & Evolution 34, 459-473.
| Crossref | Google Scholar | PubMed |
Hays GC, Laloë J-O, Rattray A, Esteban N (2021) Why do Argos satellite tags stop relaying data? Ecology and Evolution 11, 7093-7101.
| Crossref | Google Scholar | PubMed |
Hearn AR, Green JR, Espinoza E, Peñaherrera C, Acuña D, Klimley A (2013) Simple criteria to determine detachment point of towed satellite tags provide first evidence of return migrations of whale sharks (Rhincodon typus) at the Galapagos Islands, Ecuador. Animal Biotelemetry 1, 11.
| Crossref | Google Scholar |
Hoffmayer ER, Franks JS, Driggers WB, Oswald KJ, Quattro JM (2007) Observations of a feeding aggregation of whale sharks, Rhincodon typus, in the north central Gulf of Mexico. Gulf and Caribbean Research 19, 69-73.
| Crossref | Google Scholar |
Hoffmayer ER, McKinney JA, Franks JS, Hendon JM, Driggers WB, III, Falterman BJ, Galuardi B, Byrne ME (2021) Seasonal occurrence, horizontal movements, and habitat use patterns of whale sharks (Rhincodon typus) in the Gulf of Mexico. Frontiers in Marine Science 7, 598515.
| Crossref | Google Scholar |
Hueter RE, Tyminski JP, de la Parra R (2013) Horizontal movements, migration patterns, and population structure of whale sharks in the Gulf of Mexico and northwestern Caribbean Sea. PLoS ONE 8, e71883.
| Crossref | Google Scholar |
Irvine LM, Winsor MH, Follett TM, Mate BR, Palacios DM (2020) An at-sea assessment of Argos location accuracy for three species of large whales, and the effect of deep-diving behavior on location error. Animal Biotelemetry 8, 20.
| Crossref | Google Scholar |
Jepsen N, Thorstad EB, Havn T, Lucas MC (2015) The use of external electronic tags on fish: an evaluation of tag retention and tagging effects. Animal Biotelemetry 3, 49.
| Crossref | Google Scholar |
Jonsen ID, McMahon CR, Patterson TA, Auger-Méthé M, Harcourt R, Hindell MA, Bestley S (2019) Movement responses to environment: fast inference of variation among southern elephant seals with a mixed effects model. Ecology 100, e02566.
| Crossref | Google Scholar |
Jonsen ID, Patterson TA, Costa DP, Doherty PD, Godley BJ, Grecian WJ, Guinet C, Hoenner X, Kienle SS, Robinson PW, Votier SC, Whiting S, Witt MJ, Hindell MA, Harcourt RG, McMahon CR (2020) A continuous-time state–space model for rapid quality control of argos locations from animal-borne tags. Movement Ecology 8, 31.
| Crossref | Google Scholar | PubMed |
Jonsen ID, Grecian WJ, Phillips L, Carroll G, McMahon C, Harcourt RG, Hindell MA, Patterson TA (2023) aniMotum, an R package for animal movement data: rapid quality control, behavioural estimation and simulation. Methods in Ecology and Evolution 14, 806-816.
| Crossref | Google Scholar |
Karp MA, Brodie S, Smith JA, Richerson K, Selden RL, Liu OR, Muhling BA, Samhouri JF, Barnett LAK, Hazen EL, Ovando D, Fiechter J, Jacox MG, Pozo Buil M (2023) Projecting species distributions using fishery-dependent data. Fish and Fisheries 24, 71-92.
| Crossref | Google Scholar |
Kuhn M (2008) Building predictive models in R using the caret package. Journal of Statistical Software 28, 1-26.
| Crossref | Google Scholar |
Logan RK, Vaudo JJ, Sousa LL, Sampson M, Wetherbee BM, Shivji MS (2020) Seasonal movements and habitat use of juvenile smooth hammerhead sharks in the western North Atlantic Ocean and significance for management. Frontiers in Marine Science 7, 566364.
| Crossref | Google Scholar |
Lowerre-Barbieri SK, Kays R, Thorson JT, Wikelski M (2019) The ocean’s movescape: fisheries management in the bio-logging decade (2018–2028). ICES Journal of Marine Science 76, 477-488.
| Crossref | Google Scholar |
Macena BCL, Hazin FHV (2016) Whale shark (Rhincodon typus) seasonal occurrence, abundance and demographic structure in the mid-equatorial Atlantic Ocean. PLoS ONE 11, e0164440.
| Crossref | Google Scholar | PubMed |
Malde K, Handegard NO, Eikvil L, Salberg A-B (2020) Machine intelligence and the data-driven future of marine science. ICES Journal of Marine Science 77, 1274-1285.
| Crossref | Google Scholar |
Manuhutu JF, Wiadnya DGR, Sambah AB, Herawati EY (2021) The presence of whale sharks based on oceanographic variations in Cenderawasih Bay National Park, Papua, Indonesia. Biodiversitas Journal of Biological Diversity 22, 4948-4955.
| Crossref | Google Scholar |
McKinney JA, Hoffmayer ER, Wu W, Fulford R, Hendon J (2012) Feeding habitat of the whale shark Rhincodon typus in the northern Gulf of Mexico determined using species distribution modelling. Marine Ecology Progress Series 458, 199-211.
| Crossref | Google Scholar |
Meyer H, Reudenbach C, Wöllauer S, Nauss T (2019) Importance of spatial predictor variable selection in machine learning applications – moving from data reproduction to spatial prediction. Ecological Modelling 411, 108815.
| Crossref | Google Scholar |
Meyers MM, Francis MP, Erdmann M, Constantine R, Sianipar A (2020) Movement patterns of whale sharks in Cenderawasih Bay, Indonesia, revealed through long-term satellite tagging. Pacific Conservation Biology 26, 353-364.
| Crossref | Google Scholar |
Motta PJ, Maslanka M, Hueter RE, Davis RL, de la Parra R, Mulvany SL, Habegger ML, Strother JA, Mara KR, Gardiner JM, Tyminski JP, Zeigler LD (2010) Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology 113, 199-212.
| Crossref | Google Scholar | PubMed |
Muhling B, Liu Y, Lee SK, Lamkin J, Ingram W (2014) Climate change impacts on spawning grounds of Atlantic tunas in the northern Gulf of Mexico. Bulletin of Fisheries Research Agency 38, 101-103.
| Google Scholar |
Natarajan N, Dhillon IS, Ravikumar PK, Tewari A (2013) Learning with noisy labels. In ‘Advances in Neural Information Processing Systems 26 (NIPS 2013)’, 5–10 December 2013, Lake Tahoe, NV, USA. (Eds CJ Burges, L Bottou, M Welling, Z Ghahramani, KQ Weinberger) pp. 1196–1204. (Curran Associates Inc.: Red Hook, NY, USA) Available at https://papers.nips.cc/paper_files/paper/2013/file/3871bd64012152bfb53fdf04b401193f-Paper.pdf
Patterson T, Thomas L, Wilcox C, Ovaskainen O, Matthiopoulos J (2008) State–space models of individual animal movement. Trends in Ecology & Evolution 23, 87-94.
| Crossref | Google Scholar | PubMed |
Pierce S, Norman B (2016) Whale shark Rhincodon typus. In ‘IUCN Red List of Threatened Species 2016’. e.T19488A2365291. (International Union for Conservation of Nature and Natural Resources) Available at https://www.iucnredlist.org/species/19488/2365291
Pikitch EK, Santora C, Babcock EA, Bakun A, Bonfil R, Conover DO, Dayton P, Doukakis P, Fluharty D, Heneman B, Houde ED, Link J, Livingston PA, Mangel M, McAllister MK, Pope J, Sainsbury KJ (2004) Ecosystem-based fishery management. Science 305, 346-347.
| Crossref | Google Scholar | PubMed |
Ramírez-Macías D, Queiroz N, Pierce SJ, Humphries NE, Sims DW, Brunnschweiler JM (2017) Oceanic adults, coastal juveniles: tracking the habitat use of whale sharks off the Pacific coast of Mexico. PeerJ 5, e3271.
| Crossref | Google Scholar | PubMed |
Robinson DP, Jaidah MY, Jabado RW, Lee-Brooks K, Nour El-Din NM, Malki AAA, Elmeer K, McCormick PA, Henderson AC, Pierce SJ, Ormond RFG (2013) Whale sharks, Rhincodon typus, aggregate around offshore platforms in Qatari waters of the Arabian Gulf to feed on fish spawn. PLoS ONE 8, e58255.
| Crossref | Google Scholar | PubMed |
Rohner CA, Prebble CEM (2021) Whale shark foraging, feeding, and diet. In ‘Whale sharks: biology, ecology, and conservation’. (Eds ADM Dove, SJ Pierce) pp. 153–180. (CRC Press: Boca Raton, FL, USA) doi:10.1201/b22502
Rowat D, Brooks KS (2012) A review of the biology, fisheries and conservation of the whale shark Rhincodon typus. Journal of Fish Biology 80, 1019-1056.
| Crossref | Google Scholar | PubMed |
Rowat D, Womersley F, Norman BM, Pierce SJ (2021) Global threats to whale sharks. In ‘Whale sharks: biology, ecology, and conservation’. (Eds ADM Dove, SJ Pierce) pp. 239–265. (CRC Press: Boca Raton, FL, USA) doi:10.1201/b22502
Royer F, Lutcavage M (2008) Filtering and interpreting location errors in satellite telemetry of marine animals. Journal of Experimental Marine Biology and Ecology 359, 1-10.
| Crossref | Google Scholar |
Sequeira AMM, Mellin C, Meekan MG, Sims DW, Bradshaw CJA (2013) Inferred global connectivity of whale shark Rhincodon typus populations. Journal of Fish Biology 82, 367-389.
| Crossref | Google Scholar | PubMed |
Shaw AK (2020) Causes and consequences of individual variation in animal movement. Movement Ecology 8, 12.
| Crossref | Google Scholar | PubMed |
Stevens JD (2007) Whale shark (Rhincodon typus) biology and ecology: a review of the primary literature. Fisheries Research 84, 4-9.
| Crossref | Google Scholar |
Taylor JG (2007) Ram filter-feeding and nocturnal feeding of whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Fisheries Research 84, 65-70.
| Crossref | Google Scholar |
Teo SLH, Boustany A, Dewar H, Stokesbury MJW, Weng KC, Beemer S, Seitz AC, Farwell CJ, Prince ED, Block BA (2007) Annual migrations, diving behavior, and thermal biology of Atlantic bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds. Marine Biology 151, 1-18.
| Crossref | Google Scholar |
Thomson PG, Pillans R, Jaine FRA, Harcourt RG, Taylor MD, Pattiaratchi CB, McLean DL (2021) Acoustic telemetry around western Australia’s oil and gas infrastructure helps detect the presence of an elusive and endangered migratory giant. Frontiers in Marine Science 8, 631449.
| Crossref | Google Scholar |
Tyminski JP, de la Parra-Venegas R, González Cano J, Hueter RE (2015) Vertical movements and patterns in diving behavior of whale sharks as revealed by pop-up satellite tags in the eastern Gulf of Mexico. PLoS ONE 10, e0142156.
| Crossref | Google Scholar | PubMed |
Vaudo JJ, Byrne ME, Wetherbee BM, Harvey GM, Shivji MS (2017) Long-term satellite tracking reveals region-specific movements of a large pelagic predator, the shortfin mako shark, in the western North Atlantic Ocean. Journal of Applied Ecology 54, 1765-1775.
| Crossref | Google Scholar |
Whitehead DA, Magaña FG, Ketchum JT, Hoyos EM, Armas RG, Pancaldi F, Olivier D (2021) The use of machine learning to detect foraging behaviour in whale sharks: a new tool in conservation. Journal of Fish Biology 98, 865-869.
| Crossref | Google Scholar | PubMed |
Wilson SG, Polovina JJ, Stewart BS, Meekan MG (2006) Movements of whale sharks (Rhincodon typus) tagged at Ningaloo Reef, Western Australia. Marine Biology 148, 1157-1166.
| Crossref | Google Scholar |
Womersley FC, Humphries NE, Queiroz N, Vedor M, da Costa I, Furtado M, Tyminski JP, Abrantes K, Araujo G, Bach SS, Barnett A, Berumen ML, Bessudo Lion S, Braun CD, Clingham E, Cochran JEM, de la Parra R, Diamant S, Dove ADM, Dudgeon CL, Erdmann MV, Espinoza E, Fitzpatrick R, Cano JG, Green JR, Guzman HM, Hardenstine R, Hasan A, Hazin FHV, Hearn AR, Hueter RE, Jaidah MY, Labaja J, Ladino F, Macena BCL, Morris JJ, Jr, Norman BM, Peñaherrera-Palma C, Pierce SJ, Quintero LM, Ramírez-Macías D, Reynolds SD, Richardson AJ, Robinson DP, Rohner CA, Rowat DRL, Sheaves M, Shivji MS, Sianipar AB, Skomal GB, Soler G, Syakurachman I, Thorrold SR, Webb DH, Wetherbee BM, White TD, Clavelle T, Kroodsma DA, Thums M, Ferreira LC, Meekan MG, Arrowsmith LM, Lester EK, Meyers MM, Peel LR, Sequeira AMM, Eguíluz VM, Duarte CM, Sims DW (2022) Global collision-risk hotspots of marine traffic and the world’s largest fish, the whale shark. Proceedings of the National Academy of Sciences 119, e2117440119.
| Crossref | Google Scholar |
Wyatt ASJ, Matsumoto R, Chikaraishi Y, Miyairi Y, Yokoyama Y, Sato K, Ohkouchi N, Nagata T (2019) Enhancing insights into foraging specialization in the world’s largest fish using a multi-tissue, multi-isotope approach. Ecological Monographs 89, e01339.
| Crossref | Google Scholar |
Yopak KE, Peele EE (2021) Whale shark sensory biology and neuroanatomy. In ‘Whale sharks: biology, ecology, and conservation’. (Eds ADM Dove, SJ Pierce) pp. 47–64. (CRC Press: Boca Raton, FL, USA) doi:10.1201/b22502
