Alligators in the abyss: The first experimental reptilian food fall in the deep ocean

English version

Autoři: Craig Robert McClain ^aff001; Clifton Nunnally ^aff001; River Dixon ^aff001; Greg W. Rouse ^aff003; Mark Benfield ^aff004
Působiště autorů: Louisiana Universities Marine Consortium, Chauvin, LA, United States of America ^aff001; Department of Biology, University of Louisiana, Lafayette, LA, United States of America ^aff002; Scripps Oceanography, UC San Diego, La Jolla, CA, United States of America ^aff003; Department of Oceanography and Coastal Sciences, College of the Coast and Environment, Louisiana State University, Baton Rouge, LA, United States of America ^aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0225345

Souhrn

The high respiration rates of the deep-sea benthos cannot be sustained by known carbon supply pathways alone. Here, we investigate moderately-sized reptilian food falls as a potential alternative carbon pathway. Specifically, three individual carcasses of Alligator mississippiensis were deployed along the continental slope of the northern Gulf of Mexico at depths of ~2000m in early 2019. We posit the tough hide of alligators would impeded scavengers by limiting access to soft tissues of the alligator fall. However, the scavengers began consuming the food fall 43 hours post-deployment for one individual (198.2cm, 29.7kg), and the carcass of another individual (175.3 cm, 19.5kg) was completely devoid of soft tissue at 51 days post-deployment. A third individual (172.7cm, 18.5kg) was missing completely after 8 days, with only the deployment harness and weight remaining drug 8 meters away, suggesting a large elasmobranch scavenger. Additionally, bones recovered post-deployment reveal the first observations of the bone-eating Osedax in the Gulf of Mexico and are confirmed here as new to science. The findings of this study indicate the quick and successful utilization of terrestrial and aquatic-based carbon food sources in the deep marine environment, though outcome variability may be high.

Klíčová slova:

Sharks – Autumn – Sediment – Whales – Gulf of Mexico – Marine fossils – Deep sea

Zdroje

1. McClain CR, Allen AP, Tittensor DP, Rex MA. The energetics of life on the deep seafloor. Proceedings of the National Academy of Science, USA. 2012;109:5366–15371.

2. Lampitt RS, Anita AN. Particle flux in the deep seas: regional characteristics and temporal variability. Deep-Sea Research I. 1997;44:1377–403.

3. Smith KLJ. Food energy supply and demand: a discrepancy between particulate organic carbon flux and sediment community oxygen consumption in the deep sea. Limnology and Oceanography. 1987;32:201–20.

4. Van Dover CL. The Ecology of Deep-Sea Hydrothermal Vents. Princeton, NJ: Princeton University Press; 2000.

5. Smith CR, Baco-Taylor AR, Hannides A, Ruplinger D. Chemosynthetic habitats on the California slope: whale-, wood- and kelp-falls compared to vents and seeps. Biogeography and Biodiversity of Chemosynthetic Ecosystems: Planning for the Future; Southampton Oceanography Centre, Southampton, UK2003.

6. Smith CR, Baco-Taylor AR. Ecology of whale falls at the deep-sea floor. Oceanography and Marine Biology Annual Review. 2003;41:311–54.

7. McClain CR, Barry JP, Eernisse D, Horton T, Judge J, Kakui K, et al. Multiple processes generate productivity-diversity relationships in experimental wood-fall communities. Ecology. 2016;online early.

8. McClain CR, Barry JP. Beta-diversity on deep-sea wood falls reflects gradients in energy availability. Biology Letters. 2014;10:20140129. doi: 10.1098/rsbl.2014.0129 24718094

9. Bienhold C, Risotva PP, Wenzhofer F, Dittmar T, Boetius A. How deep-sea wood falls sustain chemosynthetic life. PLoS One. 2013;8:e53590. doi: 10.1371/journal.pone.0053590 23301092

10. Bernardino AF, Smith CR, Baco AR, Altamira I, Sumida PYG. Macrofaunal succession in sediments around kelp and woodfalls in the deep NE Pacific and community overlap with other reducing habitats. Deep-Sea Research I. 2010;57:708–23.

11. Voight JR. Experimental deep-sea deployments reveal diverse Northeast Pacific wood-boring bivalves of Xylophagainae (Myoida: Pholoadidae). Journal of Molluscan Studies. 2007;73:377–91.

12. Yeh J, Drazen JC. Baited-camera observations of deep-sea megafaunal scavenger ecology on the California slope. Marine Ecology Progress Series. 2011;424:145–56.

13. Priede IG, Bagley PM, Smith A, Creasey S, Merrett N. Scavenging deep demersal fishes of the Porcupine Seabight, north-east Atlantic: observations by baited camera, trap and trawl. Journal of the Marine Biological Association of the United Kingdom. 1994;74(3):481–98.

14. Henriques C, Priede I, Bagley P. Baited camera observations of deep-sea demersal fishes of the northeast Atlantic Ocean at 15–28 N off West Africa. Marine Biology. 2002;141(2):307–14.

15. Vrijenhoek R, Johnson SB, Rouse GW. A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida). BMC Biology. 2009;7:74. doi: 10.1186/1741-7007-7-74 19903327

16. Smith CR, Bernardino AF, Baco A, Hannides A, Altamira I. Seven-year enrichment: macrofaunal succession in deep-sea sediments around a 30 tonne whale fall in the Northeast Pacific. Marine Ecology Progress Series. 2014;515:133–49.

17. Smith CR, Baco AR, Glover AG. Faunal succession on replicate deep-sea whale falls: time scales and vent-seep affinities. Cahiers de Biologie Marine. 2002;43(3/4):293–8.

18. Braby CE, Rouse GW, Johnson SB, Jones WJ, Vrijenhoek RC. Bathymetric and temporal variation among Osedax boneworms and associated megafauna on whale-falls in Monterey Bay, California. Deep Sea Research Part I: Oceanographic Research Papers. 2007;54(10):1773–91.

19. Sumida PY, Alfaro-Lucas JM, Shimabukuro M, Kitazato H, Perez JA, Soares-Gomes A, et al. Deep-sea whale fall fauna from the Atlantic resembles that of the Pacific Ocean. Scientific reports. 2016;6:22139. doi: 10.1038/srep22139 26907101

20. Amon DJ, Glover AG, Wiklund H, Marsh L, Linse K, Rogers AD, et al. The discovery of a natural whale fall in the Antarctic deep sea. Deep Sea Research Part II: Topical Studies in Oceanography. 2013;92:87–96.

21. Baco AR, Smith CR. High species richness in deep-sea chemoautotrophic whale skeleton communities. Marine Ecology Progress Series. 2003;260:109–14.

22. Lundsten L, Schlining KL, Frasier K, Johnson SB, Kuhnz LA, Harvey JB, et al. Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA. Deep Sea Research Part I: Oceanographic Research Papers. 2010;57(12):1573–84.

23. Goffredi SK, Paull CK, Fulton-Bennett K, Hurtado LA, Vrijenhoek RC. Unusual benthic fauna associated with a whale fall in Monterey Canyon, California. Deep Sea Research Part I: Oceanographic Research Papers. 2004;51(10):1295–306.

24. Fujiwara Y, Kawato M, Yamamoto T, Yamanaka T, Sato‐Okoshi W, Noda C, et al. Three‐year investigations into sperm whale‐fall ecosystems in Japan. Marine Ecology. 2007;28(1):219–32.

25. West AJ, Lin C-W, Lin T-C, Hilton rG, Liu S-H, Chang C-T, et al. Mobilization and transport of course woody debris to the oceans triggered by an extreme tropical storm. Limnology and Oceanography. 2011;56:77–85.

26. Davison P, Checkley D Jr, Koslow J, Barlow J. Carbon export mediated by mesopelagic fishes in the northeast Pacific Ocean. Progress in Oceanography. 2013;116:14–30.

27. Jones EG, Collins MA, Bagley PM, Addison S, Priede IG. The fate of cetacean carcasses in the deep sea: observations on consumption rates and succession of scavenging species in the abyssal north-east Atlantic Ocean. Proceedings of the Royal Society of London Series B: Biological Sciences. 1998;265(1401):1119–27.

28. Higgs ND, Gates AR, Jones DOB. Fish Food in the Deep Sea: Revisiting the Role of Large Food-Falls. PLoS One. 2014;9:e96016. doi: 10.1371/journal.pone.0096016 24804731

29. Nicholls EL, Manabe M. Giant ichthyosaurs of the Triassic—a new species of Shonisaurus from the Pardonet Formation (Norian: Late Triassic) of British Columbia. Journal of Vertebrate Paleontology. 2004;24(4):838–49.

30. Knutsen EM. A taxonomic revision of the genus Pliosaurus (Owen, 1841a) Owen, 1841b. Norwegian Journal of Geology. 2012;92:259–76.

31. Liu J, Hu S-x, Rieppel O, Jiang D-y, Benton MJ, Kelley NP, et al. A gigantic nothosaur (Reptilia: Sauropterygia) from the Middle Triassic of SW China and its implication for the Triassic biotic recovery. Scientific reports. 2014;4:7142. doi: 10.1038/srep07142 25429609

32. Hogler JA. Speculations on the role of marine reptile deadfalls in Mesozoic deep-sea paleoecology. Palaios. 1994:42–7.

33. Jenkins RG, Kaim A, Sato K, Moriya K, Hikida Y, Hirayama R. Discovery of chemosynthesis-based association on the Cretaceous basal leatherback sea turtle from Japan. Acta Palaeontologica Polonica. 2017;62(4):683–90.

34. Martill D, Cruickshank A, Taylor M. Dispersal via whale bones. Nature. 1991;351(6323):193. doi: 10.1038/351193b0

35. Danise S, Twitchett RJ, Matts K. Ecological succession of a Jurassic shallow-water ichthyosaur fall. Nature communications. 2014;5:4789. doi: 10.1038/ncomms5789 25205249

36. Danise S, Higgs ND. Bone-eating Osedax worms lived on Mesozoic marine reptile deadfalls. Biology letters. 2015;11(4):20150072. doi: 10.1098/rsbl.2015.0072 25878047

37. IUCN. The IUCN Red List of Threatened Species. 2019 [Downloaded on 18 July 2019]. Version 2019–2:[Available from: http://www.iucnredlist.org/.

38. Campbell HA, Watts ME, Sullivan S, Read MA, Choukroun S, Irwin SR, et al. Estuarine crocodiles ride surface currents to facilitate long‐distance travel. Journal of Animal Ecology. 2010;79(5):955–64. doi: 10.1111/j.1365-2656.2010.01709.x 20546063

39. Read MA, Grigg GC, Irwin SR, Shanahan D, Franklin CE. Satellite tracking reveals long distance coastal travel and homing by translocated estuarine crocodiles, Crocodylus porosus. PLoS one. 2007;2(9):e949. doi: 10.1371/journal.pone.0000949 17895990

40. Langley L. The stanges deep-sea creatures whased ashore by hurricanes. National Geographic. 2018.

41. Masson T. Alligator surprises angler in Elmer's Island surf Saturday. NOLAcom. 2015.

42. Staff W. Second alligator in a week captured in ocean off Oak Island. WCNC. 2017.

43. Peterson B. Another gator goes for a dip in ocean Reptile captured on Sullivan’s likely swept along by tide. The Post and Courier. 2016.

44. Hooper B. 7-foot alligator emerges from the ocean in South Carolina. UPI. 2015.

45. Elsey RM. Unusual offshore occurrence of an American alligator. Southeastern Naturalist. 2005;4(3):533–7.

46. Staff. Beach goers outraged after 10-foot gator shot, killed on beach. ABC News 4. 2014.

47. O’Donnell A. 13-foot alligator washes up dead on Galveston beach. Statesman. 2016.

48. Shoop CR, Ruckdeschel CA. Alligators as predators on terrestrial mammals. American Midland Naturalist. 1990:407–12.

49. Gibbons JW, Coker JW. Herpetofaunal colonization patterns of Atlantic coast barrier islands. American Midland Naturalist. 1978:219–33.

50. Bartels M. Alligators lurking on sandy beaches from Texas to Florida is definitely a thing. Business Insider. 2016.

51. Chabreck RH, Joanen T. Growth rates of American alligators in Louisiana. Herpetologica. 1979;35(1):51–7.

52. Leak F, Lane T, Johnson D, Lamkey J. Increasing the Profitability of Florida Alligator Carcasses1. Institute of Food and Agricultural Services, AN137U-University of Florida. 2003.

53. Carr CM, Hardy SM, Brown TM, Macdonald TA, Herbert PDN. A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS One. 2011;6:e22232. doi: 10.1371/journal.pone.0022232 21829451

54. Rouse GW, Goffredi SK, Johnson SB, Vrijenhoek RC. An inordiante fondness for Osedax (Sioglinidae: Annelida): Fourteen new species of bone worms form California. Zootaxa. 2018;4377(451–489).

55. Smith CR, Glover AG, Truede T, Higgs ND, Amon DJ. Whale-fall ecosystems: Recent insights into ecology, paleoecology, and evoluton. Annual Review of Marine Science. 2015;7:571–96. doi: 10.1146/annurev-marine-010213-135144 25251277

56. Alfaro-Lucas JM, Shimabukuro M, Ferreira GD, Kitazato H, Fujiwara Y, Sumida PY. Bone-eating Osedax worms (Annelida: Siboglinidae) regulate biodiversity of deep-sea whale-fall communities. Deep Sea Research Part II: Topical Studies in Oceanography. 2017;146:4–12.

57. Khalil F, Abdel-Messeih G. Tissue constituents of reptiles in relation to their mode of life—II. Lipid content. Comparative biochemistry and physiology. 1962;6(2):171–4.

58. Jones WJ, Johnson SB, Rouse GW, Vrijenhoek RC. Marine worms (genus Osedax) colonize cow bones. Proceedings of the Royal Society B: Biological Sciences. 2007;275(1633):387–91.

59. Rouse GW, Goffredi SK, Johnson SB, Vrijenhoek RC. Not whale-fall specialists, Osedax worms also consume fishbones. Biology letters. 2011;7(5):736–9. doi: 10.1098/rsbl.2011.0202 21490008

60. Rouse GW, Worsaae K, Johnson SB, Vrjenhoek RC. Acquisition of dwarf male 'harems' by recently settled females of Osedax roseus n. sp. (Siboglinidae; Annelida). Biological Bulletin. 2008;214:67–82. doi: 10.2307/25066661 18258777

61. Fujiwara Y, Jimi N, Sumida PY, Kawato M, Kitazato H. New species of bone-eating worm Osedax from the abyssal South Atlantic Ocean (Annelida, Siboglinidae). ZooKeys. 2019;(814):53. doi: 10.3897/zookeys.814.28869 30651712

62. Froese R, Paulay G. Fishbase. version (04/2015) ed2015.

63. Nielsen J, Hedeholm RB, Simon M, Steffensen JF. Distribution and feeding ecology of the Greenland shark (Somniosus microcephalus) in Greenland waters. Polar biology. 2014;37(1):37–46.

64. MacNeil M, McMeans B, Hussey N, Vecsei P, Svavarsson J, Kovacs K, et al. Biology of the Greenland shark Somniosus microcephalus. Journal of fish biology. 2012;80(5):991–1018. doi: 10.1111/j.1095-8649.2012.03257.x 22497371

65. McMeans BC, Svavarsson J, Dennard S, Fisk AT. Diet and resource use among Greenland sharks (Somniosus microcephalus) and teleosts sampled in Icelandic waters, using δ13C, δ15N, and mercury. Canadian Journal of Fishery and Aquatic Science. 2010;67:1428–38.

66. Ebert D. Diet of the sixgill shark Hexanchus griseus off southern Africa. South African Journal of Marine Science. 1994;14(1):213–8.

67. Castro JI. The sharks of North American waters. College Station, TX: Texas A&M University Press.; 1983. 194 p.

68. Nelson JA, Johnson DS, Deegan LA, Spivak AC, Sommer NR. Feedbacks Between Nutrient Enrichment and Geomorphology Alter Bottom-Up Control on Food Webs. Ecosystems. 2019;22(2):229–42.

69. Yoshinaga J, Minagawa M, Suzuki T, Ohtsuka R, Kawabe T, Hongo T, et al. Carbon and nitrogen isotopic characterization for Papua New Guinea foods. Ecology of Food and Nutrition. 1991;26(1):17–25.

70. Sterner RW, Elser JJ. Ecological stoichiometry: the biology of elements from molecules to the biosphere: Princeton university press; 2002.

71. Rowe GT, Wei C, Nunnally C, Haedrich R, Montagna P, Baguley JG, et al. Comparative biomass structure and estimated carbon flow in food webs in the deep Gulf of Mexico. Deep Sea Research Part II: Topical Studies in Oceanography. 2008;55(24–26):2699–711.

72. McClain CR, Barry JP. Habitat heterogeneity, biogenic disturbance, and resource availability work in concert to regualte biodiversity in deep submarine canyons. Ecology. 2010;91:964–76. doi: 10.1890/09-0087.1 20462112

Alligators in the abyss: The first experimental reptilian food fall in the deep ocean

Souhrn

Klíčová slova:

Zdroje

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