Multi-method assessment of whale shark (Rhincodon typus) residency, distribution, and dispersal behavior at an aggregation site in the Red Sea
Autoři:
Jesse E. M. Cochran aff001; Camrin D. Braun aff002; E. Fernando Cagua aff004; Michael F. Campbell, Jr. aff001; Royale S. Hardenstine aff001; Alexander Kattan aff001; Mark A. Priest aff005; Tane H. Sinclair-Taylor aff001; Gregory B. Skomal aff006; Sahar Sultan aff001; Lu Sun aff001; Simon R. Thorrold aff003; Michael L. Berumen aff001
Působiště autorů:
Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia
aff001; Massachusetts Institute of Technology–Woods Hole Oceanographic Institution Joint Program in Oceanography/Applied Ocean Science and Engineering, Cambridge, MA, United States of America
aff002; Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, United States of America
aff003; Centre for Integrative Ecology, School of Biological Sciences, University of Canterbury, Private Bag, Christchurch, New Zealand
aff004; Marine Spatial Ecology Lab, School of Biological Sciences, University of Queensland, St. Lucia, Queensland, Australia
aff005; Massachusetts Division of Marine Fisheries, New Bedford, MA, United States of America
aff006; School of Biology, University of St Andrews, St Andrews, Scotland, United Kingdom
aff007; Key Laboratory of Science and Engineering for Marine Ecology and Environment, First Institute of Oceanography, Ministry of Natural Resources, Qingdao, China
aff008
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222285
Souhrn
Whale sharks (Rhincodon typus) are typically dispersed throughout their circumtropical range, but the species is also known to aggregate in specific coastal areas. Accurate site descriptions associated with these aggregations are essential for the conservation of R. typus, an Endangered species. Although aggregations have become valuable hubs for research, most site descriptions rely heavily on sightings data. In the present study, visual census, passive acoustic monitoring, and long range satellite telemetry were combined to track the movements of R. typus from Shib Habil, a reef-associated aggregation site in the Red Sea. An array of 63 receiver stations was used to record the presence of 84 acoustically tagged sharks (35 females, 37 males, 12 undetermined) from April 2010 to May 2016. Over the same period, identification photos were taken for 76 of these tagged individuals and 38 were fitted with satellite transmitters. In total of 37,461 acoustic detections, 210 visual encounters, and 33 satellite tracks were analyzed to describe the sharks’ movement ecology. The results demonstrate that the aggregation is seasonal, mostly concentrated on the exposed side of Shib Habil, and seems to attract sharks of both sexes in roughly equal numbers. The combined methodologies also tracked 15 interannual homing-migrations, demonstrating that many sharks leave the area before returning in later years. When compared to acoustic studies from other aggregations, these results demonstrate that R. typus exhibits diverse, site-specific ecologies across its range. Sightings-independent data from acoustic telemetry and other sources are an effective means of validating more common visual surveys.
Klíčová slova:
Biology and life sciences – Organisms – Eukaryota – Physical sciences – Research and analysis methods – Neuroscience – Psychology – Animals – Social sciences – Vertebrates – Research design – Physics – Survey research – Earth sciences – Geomorphology – Topography – Landforms – Islands – Marine and aquatic sciences – Reefs – Sensory perception – Fish – Chondrichthyes – Elasmobranchii – Sharks – Bioacoustics – Vision – Acoustics – Census – Bodies of water – Red Sea
Zdroje
1. Ebert DA, Fowler SL, Compagno LJ. Sharks of the world: a fully illustrated guide: Wild Nature Press; 2013.
2. Taylor J. Seasonal occurrence, distribution and movements of the whale shark, Rhincodon typus, at Ningaloo Reef, Western Australia. Marine and Freshwater Research. 1996;47(4):637–42. http://dx.doi.org/10.1071/MF9960637.
3. Eckert SA, Stewart BS. Telemetry and satellite tracking of whale sharks, Rhincodon typus, in the Sea of Cortez, Mexico, and the north Pacific Ocean. Environmental Biology of Fishes. 2001;60(1):299–308. doi: 10.1023/a:1007674716437
4. Heyman WD, Graham RT, Kjerfve B, Johannes RE. Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belize. Marine Ecology Progress Series. 2001;215:275–82.
5. Rowat D, Meekan M, Engelhardt U, Pardigon B, Vely M. Aggregations of juvenile whale sharks (Rhincodon typus) in the Gulf of Tadjoura, Djibouti. Environmental Biology of Fishes. 2007;80(4):465–72.
6. Brooks K, Rowat D, Pierce SJ, Jouannet D, Vely M. Seeing spots: photo-identification as a regional tool for whale shark identification. Western Indian Ocean Journal of Marine Science. 2010;9(2):185–94.
7. Riley M, Hale M, Harman A, Rees R. Analysis of whale shark Rhincodon typus aggregations near South Ari Atoll, Maldives Archipelago. Aquatic Biology. 2010;8(2):145–50. doi: 10.3354/ab00215
8. Ramírez-Macías D, Meekan M, La Parra-Venegas D, Remolina-Suárez F, Trigo-Mendoza M, Vázquez-Juárez R. Patterns in composition, abundance and scarring of whale sharks Rhincodon typus near Holbox Island, Mexico. Journal of Fish Biology. 2012;80(5):1401–16. doi: 10.1111/j.1095-8649.2012.03258.x 22497390
9. Ramírez-Macías D, Vázquez-Haikin A, Vázquez-Juárez R. Whale shark Rhincodon typus populations along the west coast of the Gulf of California and implications for management. Endangered Species Research. 2012;18(2):115–28.
10. Robinson DP, Jaidah MY, Jabado RW, Lee-Brooks K, El-Din NMN, Malki AAA, et al. Whale sharks, Rhincodon typus, aggregate around offshore platforms in Qatari waters of the Arabian Gulf to feed on fish spawn. PLoS One. 2013;8(3):e58255. doi: 10.1371/journal.pone.0058255 23516456
11. Rohner C, Pierce S, Marshall A, Weeks S, Bennett M, Richardson A. Trends in sightings and environmental influences on a coastal aggregation of manta rays and whale sharks. Marine Ecology Progress Sereis. 2013;482:153–68.
12. Acuña-Marrero D, Jiménez J, Smith F, Doherty PF Jr, Hearn A, Green JR, et al. Whale shark (Rhincodon typus) seasonal presence, residence time and habitat use at Darwin Island, Galapagos Marine Reserve. PLoS One. 2014;9(12):e115946. doi: 10.1371/journal.pone.0115946 25551553
13. Berumen ML, Braun CD, Cochran JE, Skomal GB, Thorrold SR. Movement patterns of juvenile whale sharks tagged at an aggregation site in the Red Sea. PLoS One. 2014;9(7):e103536. doi: 10.1371/journal.pone.0103536 25076407
14. Cagua EF, Cochran JE, Rohner CA, Prebble CE, Sinclair-Taylor TH, Pierce SJ, et al. Acoustic telemetry reveals cryptic residency of whale sharks. Biology Letters. 2015;11(4):20150092. doi: 10.1098/rsbl.2015.0092 25832816
15. Diamant S, Rohner CA, Kiszka JJ, d Echon AG, d Echon TG, Sourisseau E, et al. Movements and habitat use of satellite-tagged whale sharks off western Madagascar. Endangered Species Research. 2018;36:49–58.
16. Rowat D, Engelhardt U. Seychelles: A case study of community involvement in the development of whale shark ecotourism and its socio-economic impact. Fisheries Research. 2007;84(1):109–13.
17. Jones T, Wood D, Catlin J, Norman B. Expenditure and ecotourism: predictors of expenditure for whale shark tour participants. Journal of Ecotourism. 2009;8(1):32–50.
18. Cagua EF, Collins N, Hancock J, Rees R. Whale shark economics: a valuation of wildlife tourism in South Ari Atoll, Maldives. PeerJ. 2014;2:e515. doi: 10.7717/peerj.515 25165629
19. Graham RT, Roberts CM. Assessing the size, growth rate and structure of a seasonal population of whale sharks (Rhincodon typus Smith 1828) using conventional tagging and photo identification. Fisheries Research. 2007;84(1):71–80. doi: 10.1016/j.fishres.2006.11.026
20. Holmberg J, Norman B, Arzoumanian Z. Robust, comparable population metrics through collaborative photo-monitoring of whale sharks Rhincodon typus. Ecological Applications. 2008;18(1):222–33. 18372568
21. Fox S, Foisy I, De La Parra Venegas R, Galván Pastoriza B, Graham R, Hoffmayer E, et al. Population structure and residency of whale sharks Rhincodon typus at Utila, Bay Islands, Honduras. Journal of Fish Biology. 2013;83(3):574–87. doi: 10.1111/jfb.12195 23991875
22. Araujo G, Lucey A, Labaja J, So CL, Snow S, Ponzo A. Population structure and residency patterns of whale sharks, Rhincodon typus, at a provisioning site in Cebu, Philippines. PeerJ. 2014;2:e543. doi: 10.7717/peerj.543 25279256
23. Robinson DP, Jaidah MY, Bach S, Lee K, Jabado RW, Rohner CA, et al. Population structure, abundance and movement of whale sharks in the Arabian Gulf and the Gulf of Oman. PLoS One. 2016;11(6):e0158593. doi: 10.1371/journal.pone.0158593 27362839
24. McKinney JA, Hoffmayer ER, Holmberg J, Graham RT, Driggers WB III, de la Parra-Venegas R, et al. Long-term assessment of whale shark population demography and connectivity using photo-identification in the Western Atlantic Ocean. PLoS One. 2017;12(8):e0180495. doi: 10.1371/journal.pone.0180495 28817569
25. Norman BM, Holmberg JA, Arzoumanian Z, Reynolds SD, Wilson RP, Rob D, et al. Undersea constellations: the global biology of an endangered marine megavertebrate further informed through citizen science. BioScience. 2017;67(12):1029–43.
26. McKinney JA, Hoffmayer ER, Wu W, Fulford R, Hendon JM. Feeding habitat of the whale shark Rhincodon typus in the northern Gulf of Mexico determined using species distribution modelling. Marine Ecology Progress Series. 2012;458:199–211.
27. Cárdenas-Palomo N, Herrera-Silveira J, Velázquez-Abunader I, Reyes O, Ordonez U. Distribution and feeding habitat characterization of whale sharks Rhincodon typus in a protected area in the north Caribbean Sea. Journal of Fish Biology. 2015;86(2):668–86. doi: 10.1111/jfb.12589 25523625
28. Cochran J, Hardenstine R, Braun C, Skomal G, Thorrold S, Xu K, et al. Population structure of a whale shark Rhincodon typus aggregation in the Red Sea. Journal of Fish Biology. 2016;89(3):1570–82. doi: 10.1111/jfb.13054 27401632
29. Sequeira A, Mellin C, Rowat D, Meekan MG, Bradshaw CJ. Ocean-scale prediction of whale shark distribution. Diversity and Distributions. 2012;18(5):504–18.
30. Eckert SA, Dolar LL, Kooyman GL, Perrin W, Rahman RA. Movements of whale sharks (Rhincodon typus) in South-east Asian waters as determined by satellite telemetry. Journal of Zoology. 2002;257(1):111–5. doi: 10.1017/s0952836902000705
31. Hsu HH, Joung SJ, Liao YY, Liu KM. Satellite tracking of juvenile whale sharks, Rhincodon typus, in the Northwestern Pacific. Fisheries Research. 2007;84(1):25–31.
32. Rowat D, Gore M. Regional scale horizontal and local scale vertical movements of whale sharks in the Indian Ocean off Seychelles. Fisheries Research. 2007;84(1):32–40.
33. Gifford A, Compagno LJ, Levine M, Antoniou A. Satellite tracking of whale sharks using tethered tags. Fisheries Research. 2007;84(1):17–24.
34. Brunnschweiler JM, Baensch H, Pierce SJ, Sims DW. Deep-diving behaviour of a whale shark Rhincodon typus during long-distance movement in the western Indian Ocean. Journal of Fish Biology. 2009;74(3):706–14. doi: 10.1111/j.1095-8649.2008.02155.x 20735591
35. Sleeman JC, Meekan MG, Wilson SG, Polovina JJ, Stevens JD, Boggs GS, et al. To go or not to go with the flow: Environmental influences on whale shark movement patterns. Journal of Experimental Marine Biology and Ecology. 2010;390(2):84–98. doi: 10.1016/j.jembe.2010.05.009
36. Wang Y, Li W, Zeng X, Cui Y. A short note on the horizontal and vertical movements of a whale shark, Rhincodon typus, tracked by satellite telemetry in the South China Sea. Integrative Zoology. 2012;7(1):94–8. doi: 10.1111/j.1749-4877.2011.00278.x 22405452
37. Hueter RE, Tyminski JP, de la Parra R. Horizontal movements, migration patterns, and population structure of whale sharks in the Gulf of Mexico and Northwestern Caribbean Sea. PloS One. 2013;8(8):e71883. doi: 10.1371/journal.pone.0071883 23991000
38. Rohner CA, Richardson AJ, Jaine FR, Bennett MB, Weeks SJ, Cliff G, et al. Satellite tagging highlights the importance of productive Mozambican coastal waters to the ecology and conservation of whale sharks. PeerJ. 2018;6:e4161. doi: 10.7717/peerj.4161 29312815
39. Norman B, Whitty J, Beatty S, Reynolds S, Morgan D. Do they stay or do they go? Acoustic monitoring of whale sharks at Ningaloo Marine Park, Western Australia. Journal of Fish Biology. 2017;91(6):1713–20. doi: 10.1111/jfb.13461 29023767
40. Norman BM, Stevens JD. Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in Western Australia. Fisheries Research. 2007;84(1):81–6. doi: 10.1016/j.fishres.2006.11.015
41. Rohner CA, Richardson AJ, Prebble CE, Marshall AD, Bennett MB, Weeks SJ, et al. Laser photogrammetry improves size and demographic estimates for whale sharks. PeerJ. 2015;3:e886. doi: 10.7717/peerj.886 25870776
42. Cagua EF, Berumen ML, Tyler E. Topography and biological noise determine acoustic detectability on coral reefs. Coral Reefs. 2013;32(4):1123–34.
43. Papastamatiou YP, Itano DG, Dale JJ, Meyer CG, Holland KN. Site fidelity and movements of sharks associated with ocean-farming cages in Hawaii. Marine and Freshwater Research. 2011;61(12):1366–75.
44. Simpfendorfer CA, Yeiser BG, Wiley TR, Poulakis GR, Stevens PW, Heupel MR. Environmental influences on the spatial ecology of juvenile smalltooth sawfish (Pristis pectinata): results from acoustic monitoring. PLoS One. 2011;6(2):e16918. doi: 10.1371/journal.pone.0016918 21347294
45. Knip D, Heupel M, Simpfendorfer C. Habitat use and spatial segregation of adult spottail sharks Carcharhinus sorrah in tropical nearshore waters. Journal of Fish Biology. 2012;80(4):767–84. doi: 10.1111/j.1095-8649.2012.03223.x 22471798
46. Brunnschweiler JM, Barnett A. Opportunistic visitors: long-term behavioural response of bull sharks to food provisioning in Fiji. PLoS One. 2013;8(3):e58522. doi: 10.1371/journal.pone.0058522 23516496
47. Chin A, Heupel M, Simpfendorfer C, Tobin A. Ontogenetic movements of juvenile blacktip reef sharks: evidence of dispersal and connectivity between coastal habitats and coral reefs. Aquatic Conservation: Marine and Freshwater Ecosystems. 2013;23(3):468–74.
48. Filmalter J, Dagorn L, Cowley P. Spatial behaviour and site fidelity of the sicklefin lemon shark Negaprion acutidens in a remote Indian Ocean atoll. Marine Biology. 2013;160(9):2425–36.
49. Daley RK, Williams A, Green M, Barker B, Brodie P. Can marine reserves conserve vulnerable sharks in the deep sea? A case study of Centrophorus zeehaani, (Centrophoridae) examined with acoustic telemetry. Deep Sea Research Part II: Topical Studies in Oceanography. 2014.
50. Wood SN. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society: Series B (Statistical Methodology). 2011;73(1):3–36.
51. Skomal GB, Braun CD, Chisholm JH, Thorrold SR. Movements of the white shark Carcharodon carcharias in the North Atlantic Ocean. Marine Ecology Progress Series. 2017 580:1–16
52. Braun CD, Galuardi B, Thorrold SR (2018) HMMoce: An R package for improved geolocation of archival-tagged fishes using a hidden Markov method. Methods in Ecology Evolution 9:1212–1220
53. Hozumi A, Kaartvedt S, Røstad A, Berumen ML, Cochran JE, Jones BH. Acoustic backscatter at a Red Sea whale shark aggregation site. Regional Studies in Marine Science. 2018.
54. Braun CD, Skomal GB, Thorrold SR, Berumen ML. Movements of the reef manta ray (Manta alfredi) in the Red Sea using satellite and acoustic telemetry. Marine Biology. 2015;162:2351–236
55. Braun CD, Skomal GB, Thorrold SR. Integrating Archival Tag Data and a High-Resolution Oceanographic Model to Estimate Basking Shark (Cetorhinus maximus) Movements in the Western Atlantic. Frontiers in Marine Science. 2018;5(25). doi: 10.3389/fmars.2018.00025
56. Rowat D. Occurrence of whale shark (Rhincodon typus) in the Indian Ocean: A case for regional conservation. Fisheries Research. 2007;84(1):96–101.
57. Clingham E, Brown J, Henry L, Beard A, Dove AD. Evidence that St. Helena island is an important multi-use habitat for whale sharks, Rhincodon typus, with the first description of putative mating in this species. PeerJ Preprints. 2016;4:e1885v1. doi: 10.7287/peerj.preprints.1885v1
58. Rowat D, Brooks K, March A, McCarten C, Jouannet D, Riley L, et al. Long-term membership of whale sharks (Rhincodon typus) in coastal aggregations in Seychelles and Djibouti. Marine and Freshwater Research. 2011;62:621–7.
59. Ramírez‐Macías D, Meekan M, De La Parra‐Venegas R, Remolina‐Suárez F, Trigo‐Mendoza M, Vázquez‐Juárez R. Patterns in composition, abundance and scarring of whale sharks Rhincodon typus near Holbox Island, Mexico. Journal of Fish Biology. 2012;80(5):1401–16. doi: 10.1111/j.1095-8649.2012.03258.x 22497390
60. Ketchum JT, Galván-Magaña F, Klimley AP. Segregation and foraging ecology of whale sharks, Rhincodon typus, in the southwestern Gulf of California. Environmental Biology of Fishes. 2013;96(6):779–95.
61. Motta PJ, Maslanka M, Hueter RE, Davis RL, de la Parra R, Mulvany SL, et al. Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology (Jena, Germany). 2010;113(4):199–212.
62. Rohner CA, Armstrong AJ, Pierce SJ, Prebble CE, Cagua EF, Cochran JE, et al. Whale sharks target dense prey patches of sergestid shrimp off Tanzania. Journal of Plankton Research. 2015:fbv010.
63. Clark E, Nelson D. Young whale sharks, Rhincodon typus, feeding on a copepod bloom near La Paz, Mexico. Environmental Biology of Fishes. 1997;50(1):63–73. doi: 10.1023/a:1007312310127
64. Nelson JD, Eckert SA. Foraging ecology of whale sharks (Rhincodon typus) within Bahía de Los Angeles, Baja California Norte, México. Fisheries Research. 2007;84(1):47–64. doi: 10.1016/j.fishres.2006.11.013
65. Cárdenas-Palomo N, Noreña-Barroso E, Herrera-Silveira J, Galván-Magaña F, Hacohen-Domené A. Feeding habits of the whale shark (Rhincodon typus) inferred by fatty acid profiles in the northern Mexican Caribbean. Environmental Biology of Fishes. 2018;101(11):1599–612. doi: 10.1007/s10641-018-0806-3
66. Hueter RE, Tyminski JP, de la Parra R. Horizontal movements, migration patterns, and population structure of whale sharks in the Gulf of Mexico and northwestern Caribbean Sea. PLoS One. 2013;8(8):e71883. doi: 10.1371/journal.pone.0071883 23991000
67. Ryan JP, Green JR, Espinoza E, Hearn AR. Association of whale sharks (Rhincodon typus) with thermo-biological frontal systems of the eastern tropical Pacific. PLoS One. 2017;12(8):e0182599. doi: 10.1371/journal.pone.0182599 28854201
68. Thums M, Meekan M, Stevens J, Wilson S, Polovina J. Evidence for behavioural thermoregulation by the world's largest fish. Journal of The Royal Society Interface. 2012:rsif20120477.
69. Meekan M, Fuiman L, Davis R, Berger Y, Thums M. Swimming strategy and body plan of the world's largest fish: implications for foraging efficiency and thermoregulation. Frontiers in Marine Science. 2015;2(64). doi: 10.3389/fmars.2015.00064
70. Siedler G. General circulation of water masses in the Red Sea. In: Degens ET, Ross DA, editors. Hot brines and recent heavy metal deposits in the Red Sea: a geochemical and geophysical account. Berlin, Heidelberg: Springer Berlin Heidelberg; 1969. p. 131–7.
71. Heupel MR, Carlson JK, Simpfendorfer CA. Shark nursery areas: concepts, definition, characterization and assumptions. Marine Ecology Progress Series. 2007;337:287–97.
72. Kinney MJ, Simpfendorfer CA. Reassessing the value of nursery areas to shark conservation and management. Conservation letters. 2009;2(2):53–60.
73. Pierce SJ, Norman B. Rhincodon typus. The IUCN Red List of Threatened Species 2016: e.T19488A2365291 2016 [30/09/2016]. Available from: http://dx.doi.org/10.2305/IUCN.UK.2016-1.RLTS.T19488A2365291.en.
74. Spaet JL, Berumen ML. Fish market surveys indicate unsustainable elasmobranch fisheries in the Saudi Arabian Red Sea. Fisheries Research. 2015;161:356–64.
75. Monroe AA, Ziegler M, Roik A, Röthig T, Hardenstine RS, Emms MA, et al. In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event. PLoS One. 2018;13(4):e0195814. doi: 10.1371/journal.pone.0195814 29672556
76. Queiroz N, Humphries NE, Couto A, Vedor M, da Costa I, Sequeira AMM, et al. Global spatial risk assessment of sharks under the footprint of fisheries. Nature. 2019. doi: 10.1038/s41586-019-1444-4 31340216
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Je Fuchsova endotelová dystrofie rohovky neurodegenerativní onemocnění?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania