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Environmental Biology of Fishes

, Volume 102, Issue 12, pp 1559–1567 | Cite as

Tiger shark predation on large ocean sunfishes (Family Molidae) – two Australian observations

  • Marianne NyegaardEmail author
  • Samantha Andrzejaczek
  • Curt S. Jenner
  • Micheline-Nicole M. Jenner
Article

Abstract

Sharks are commonly listed as predators of the large ocean sunfishes (genera Mola and Masturus), yet documented shark predation events on adult sunfish are exceedingly infrequent in the literature. Here we recount two Australian observations of tiger shark (Galeocerdo cuvier) predation on sunfish of ca. 1.3 and 2 m total length, respectively. The attacks demonstrate that tiger sharks are both able and willing to predate on large sunfish; however, based on a paucity of sunfish remains in tiger shark stomach analyses, and a lack of reports of the common sunfish parasite Molicola horridus in tiger sharks, these observations likely represent opportunistic predation events. The seemingly limited interactions may reflect differing habitat use by sunfish and tiger sharks within their overlapping distribution ranges, alternatively, large sunfish may comprise low quality or undesired prey for tiger sharks. Further, despite indications of prey debilitation during both accounts, the attacks likely represent indiscriminate tiger shark feeding events with no particular prey handling strategy.

Keywords

Mola alexandrini Mola tecta Galeocerdo cuvier Feeding strategy Molicola horridus Predator-prey interactions 

Notes

Acknowledgements

We are grateful to Jim Prescott (formerly Australian Fisheries Management Authority), Jeff Jeffersen (Queensland Museum), Alastair Graham (Australian National Fish Collection in Hobart) and the staff at RV Whale Song, as well as to Patricio Alberto Zapata Bustos, Remy Sautaux, Roser Gari Perez and Jess Hadden for kindly allowing the use of their images.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abe T, Sekiguchi K, Onishi H, Muramatsu K, Kamito T (2012) Observations on a school of ocean sunfish and evidence for a symbiotic cleaning association with albatrosses. Mar Biol 159:1173–1176.  https://doi.org/10.1007/s00227-011-1873-6 CrossRefGoogle Scholar
  2. Acuña-Marrero D, Smith ANH, Hammerschlag N, Hearn A, Anderson MJ, Calich H, Pawley MDM, Fischer C, Salinas-de-León P (2017) Residency and movement patterns of an apex predatory shark (Galeocerdo cuvier) at the Galapagos marine reserve. PLoS One 12:e0183669.  https://doi.org/10.1371/journal.pone.0183669 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ahuir-Baraja AE, Yamanoue Y, Kubicek L (2017) First confirmed record of Mola sp. a in the western Mediterranean Sea: morphological, molecular and parasitological findings. J Fish Biol 90:1133–1141.  https://doi.org/10.1111/jfb.13247 CrossRefPubMedGoogle Scholar
  4. Aines AC, Carlson JK, Boustany A, Mathers A, Kohler NE (2018) Feeding habits of the tiger shark, Galeocerdo cuvier, in the Northwest Atlantic Ocean and Gulf of Mexico. Environ Biol Fish 101:403–415.  https://doi.org/10.1007/s10641-017-0706-y CrossRefGoogle Scholar
  5. Allain V (2003) Diet of mahi-mahi, wahoo and lancetfish in the western and central Pacific. 16th meeting of the standing committee on tuna and billfish Working Paper BBRG-6, Oceanic Fisheries Programme Secretariat of the Pacific Community Noumea, New CaledoniaGoogle Scholar
  6. Alves PV, De Chambrier A, Scholz T, Luque JL (2017) Annotated checklist of fish cestodes from South America. Zookeys 650:1–205.  https://doi.org/10.3897/zookeys.650.10982 CrossRefGoogle Scholar
  7. Andrzejaczek S, Gleiss AC, Lear KO, Pattiaratchi CB, Chapple TK, Meekan MG (2019) Biologging tags reveal links between fine-scale horizontal and vertical movement behaviors in tiger sharks (Galeocerdo cuvier). Front Mar Sci 6:229.  https://doi.org/10.3389/fmars.2019.00229 CrossRefGoogle Scholar
  8. Animal Diversity web (2019). Mola mola ocean sunfish. https://animaldiversity.org/accounts/Mola_mola/. Accessed 7 Aug 2019
  9. Beveridge I, Bray RA, Cribb TH, Justine J-L (2014) Diversity of trypanorhynch metacestodes in teleost fishes from coral reefs off eastern Australia and New Caledonia. Parasite 21:60.  https://doi.org/10.1051/parasite/2014060 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cartamil DP, Lowe CG (2004) Diel movement patterns of ocean sunfish Mola mola off southern California. Mar Ecol Prog Ser 266:245–253.  https://doi.org/10.3354/meps266245 CrossRefGoogle Scholar
  11. Celona A, Donato N, de Maddalena A (2001) In relation to the captures of a great white shark, Carcharodon carcharias (Linnaeus, 1758), and a shortfin mako, Isurus oxyrinchus Rafinesque, 1809, in the Messina Strait. Ann Ser Hist Nat 11:13–16Google Scholar
  12. Cliff G, Dudley SF (1991) Sharks caught in the protective gill nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes. South African J Mar Sci 10:253–270.  https://doi.org/10.2989/02577619109504636 CrossRefGoogle Scholar
  13. Cliff G, Dudley SFJ, Davis B (1989) Sharks caught in the protective gill nets off natal, South Africa. 2. The great white shark carcharodon carcharias (Linnaeus). South African J Mar Sci 8:131–144.  https://doi.org/10.2989/02577618909504556 CrossRefGoogle Scholar
  14. Davenport J, Phillips ND, Cotter E, Eagling LE, Houghton JDR (2018) The locomotor system of the ocean sunfish Mola mola (L.): role of gelatinous exoskeleton, horizontal septum, muscles and tendons. J Anat 233:347–357.  https://doi.org/10.1111/joa.12842 CrossRefGoogle Scholar
  15. Fergusson IK, Compagno LJV, Marks MA (2000) Predation by white sharks Carcharodon carcharias (Chondrichthyes: Lamnidae) upon chelonians, with new records from the Mediterranean Sea and a first record of the ocean sunfish Mola mola (Osteichthyes: Molidae) as stomach contents. Environ Biol Fish 58:447–453.  https://doi.org/10.1023/A:1007639324360 CrossRefGoogle Scholar
  16. Fernández I, Oyarzún C, Valenzuela A, Burgos C, Guaqucín V, Camposi V (2016) Parásitos del pez luna Mola mola (Pisces: Molidae). Primer registro en aguas de la costa centro sur de Chile. Gayana 80:192.  https://doi.org/10.4067/S0717-65382016000200192 CrossRefGoogle Scholar
  17. Ferreira LC, Thums M, Meeuwig JJ, Vianna GMS, Stevens J, McAuley R, Meekan MG (2015) Crossing latitudes-long-distance tracking of an apex predator. PLoS One 10:e0116916.  https://doi.org/10.1371/journal.pone.0116916 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fricke R, Eschmeyer WN, Laan R Van Der (2019) Catalog of fishes: Genera, Species, References. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 16 Sept 2019
  19. Garibaldi F, Orsi Relini L (2000) Summer abundance, size and feeding habits of the blue shark, Prionace glauca, in the pelagic sanctuary of the Ligurian Sea. Biol Mar Mediterr 71:324–333Google Scholar
  20. Gladstone W (1988) Killer whale feeding observed underwater. J Mammal 69:629–630.  https://doi.org/10.2307/1381360 CrossRefGoogle Scholar
  21. Gudger EW (1936) The natural history and geographical distribution of the pointed-tailed ocean sunfish (Masturus lanceolatus), with notes on the shape of the tail. Proc Zool Soc London A107:353–396.  https://doi.org/10.1111/j.1096-3642.1937.tb00818.x CrossRefGoogle Scholar
  22. Gustinelli A, Nardini G, Aureli G, Trentini M, Affronte M, Fioravanti MI (2006) Parasitofauna of Mola mola (Linnaeus, 1758) from Italian Sea. Biol Mar Mediterr 13:872–876Google Scholar
  23. Hammerschlag N, Broderick AC, Coker JW, Coyne MS, Dodd M, Frick MG, Godfrey MH, Godley MH, Godley BJ, Griffin DBB, Hartog K, Murphy SR, Murphy TM, Rose Nelson E, Williams KL, Witt M, Hawkes LA (2015) Evaluating the landscape of fear between apex predatory sharks and mobile sea turtles across a large dynamic seascape. Ecology 96:2117–2126.  https://doi.org/10.1890/14-2113.1 CrossRefPubMedGoogle Scholar
  24. Harrod C, Syväranta J, Kubicek L, Cappanera V, Houghton JDR (2013) Reply to Logan & Dodge: ‘stable isotopes challenge the perception of ocean sunfish Mola mola as obligate jellyfish predators’. J Fish Biol 82:10–16.  https://doi.org/10.1111/j.1095-8649.2012.03485.x CrossRefPubMedGoogle Scholar
  25. Heinz ML, Dailey MD (1974) The Trypanorhyncha (Cestoda) of elasmobranch fishes from Southern California and northern Mexico. Proc Helminthol Soc Wash 41:161–169Google Scholar
  26. Heithaus MR (2001) The biology of tiger sharks, Galeocerdo cuvier, in Shark Bay, Western Australia: sex ratio, size distribution, diet, and seasonal changes in catch rates. Environ Biol Fish 61:25–36.  https://doi.org/10.1023/A:1011021210685 CrossRefGoogle Scholar
  27. Heithaus MR (2004) Predator–prey interactions. In: Carrier J, Musick J, Heithaus M (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 487–521.  https://doi.org/10.1201/9780203491317 CrossRefGoogle Scholar
  28. Heithaus M, Dill L, Marshall G, Buhleier B (2002) Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Mar Biol 140:237–248.  https://doi.org/10.1007/s00227-001-0711-7 CrossRefGoogle Scholar
  29. Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Bejder L (2007) State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844.  https://doi.org/10.1111/j.1365-2656.2007.01260.x CrossRefPubMedGoogle Scholar
  30. Heithaus MR, Wirsing AJ, Thomson JA, Burkholder DA (2008) A review of lethal and non-lethal effects of predators on adult marine turtles. J Exp Mar Biol Ecol 356:43–51.  https://doi.org/10.1016/j.jembe.2007.12.013 CrossRefGoogle Scholar
  31. Holland KN, Wetherbee BM, Lowe CG, Meyer CG (1999) Movements of tiger sharks (Galeocerdo cuvier) in coastal Hawaiian waters. Mar Biol 134:665–673.  https://doi.org/10.1007/s002270050582 CrossRefGoogle Scholar
  32. King JE (1951) Notes. Two juvenile pointed-tailed ocean sunfish, Masturus lanceolatus, from Hawaiian waters. Pac Sci 5:108–109Google Scholar
  33. Klein-MacPhee G (2002) Ocean sunfishes. Family Molidae. In: Collette BB, Klein-MacPhee G (eds) Bigelow & Schroeder’s fishes of the Gulf of Maine, 3rd edn. Smithsonian Institution Press, Washington, D.C., pp 603–607.  https://doi.org/10.1046/j.1467-2979.2003.0139a.x CrossRefGoogle Scholar
  34. Knoff M, Clemente SCDS, Pinto RM, Lanfredi RM, Gomes DC (2004) Taxonomic reports of Otobothrioidea (Eucestoda, Trypanorhyncha) from elasmobranch fishes of the southern coast off Brazil. Mem Inst Oswaldo Cruz 99:31–36.  https://doi.org/10.1590/S0074-02762004000100006 CrossRefPubMedGoogle Scholar
  35. Leis JL, Matsuura K, Shao K-T, Hardy G, Zapfe G, Liu M, Jing L, Robertson R, Tyler J (2015) Masturus lanceolatus (errata version published in 2017). The IUCN Red List of Threatened Species 2015: e.T193634A115330232Google Scholar
  36. Lowe CG, Wetherbee BM, Crow GL, Tester AL (1996) Ontogenetic dietary shifts and feeding behavior of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environ Biol Fish 47:203–211.  https://doi.org/10.1007/BF00005044 CrossRefGoogle Scholar
  37. MacNeil MA, Carlson JK, Beerkircher LR (2009) Shark depredation rates in pelagic longline fisheries: a case study from the Northwest Atlantic. ICES J Mar Sci 66:708–719.  https://doi.org/10.1093/icesjms/fsp022 CrossRefGoogle Scholar
  38. Markaida U, Sosa-Nishizaki O (2010) Food and feeding habits of the blue shark Prionace glauca caught off Ensenada, Baja California, Mexico, with a review on its feeding. J Mar Biol Assoc UK 90:977–994.  https://doi.org/10.1017/S0025315409991597 CrossRefGoogle Scholar
  39. Martin FD, Drewry GE (1978) Development of Fishes of the Mid-Atlantic Bight: An Atlas of Egg, Larval, and Juvenile Stages, Vol VI - Stromateidae through Ogcocephalidae. Department of the Interior, Fish and Wildlife Service, Office of Biological Services, Fort CollinsGoogle Scholar
  40. Matthews FD, Damkaer DM, Knapp LW, Collette BB (1977) Food of western North Atlantic tunas (Thunnus) and lancetfishes (Alepisaurus). NOAA Technical Report NMFS SSRF -706. U.S. Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries ServiceGoogle Scholar
  41. Nakamura I, Sato K (2014) Ontogenetic shift in foraging habit of ocean sunfish Mola mola from dietary and behavioral studies. Mar Biol 161:1263–1273.  https://doi.org/10.1007/s00227-014-2416-8 CrossRefGoogle Scholar
  42. Nakamura I, Goto Y, Sato K (2015) Ocean sunfish rewarm at the surface after deep excursions to forage for siphonophores. J Anim Ecol 84:590–603.  https://doi.org/10.1111/1365-2656.12346 CrossRefPubMedGoogle Scholar
  43. Nyegaard M (2018) There be giants! The importance of taxonomic clarity of the large ocean sunfishes (genus Mola, Family Molidae) for assessing sunfish vulnerability to anthropogenic pressures. PhD thesis. Perth (Western Australia): Murdoch UniversityGoogle Scholar
  44. Nyegaard M, Sawai E (2018) Species identification of sunfish specimens (genera Mola and Masturus, family Molidae) from Australian and New Zealand natural history museum collections and other local sources. Data Br 19:2404–2415.  https://doi.org/10.1016/j.dib.2018.07.015 CrossRefGoogle Scholar
  45. Nyegaard M, Loneragan N, Hall S, Andrew J, Sawai E, Nyegaard M (2018a) Giant jelly eaters on the line: species distribution and bycatch of three dominant sunfishes in the Southwest Pacific. Estuar Coast Shelf Sci 207:1–15.  https://doi.org/10.1016/j.ecss.2018.03.017 CrossRefGoogle Scholar
  46. Nyegaard M, Sawai E, Gemmell N, Gillum J, Loneragan NR, Yamanoue Y, Stewart AL (2018b) Hiding in broad daylight: molecular and morphological data reveal a new ocean sunfish species (Tetraodontiformes: Molidae) that has eluded recognition. Zool J Linnean Soc 182:631–658.  https://doi.org/10.1093/zoolinnean/zlx040 CrossRefGoogle Scholar
  47. Oyafuso ZS, Toonen RJ, Franklin EC (2016) Temporal and spatial trends in prey composition of wahoo Acanthocybium solandri: a diet analysis from the central North Pacific Ocean using visual and DNA bar-coding techniques. J Fish Biol 88:1501–1523.  https://doi.org/10.1111/jfb.12928 CrossRefPubMedGoogle Scholar
  48. Palko JB, Beardsley GL, Richards WJ (1982) Synopsis of the biological data on dolphin-fishes, Coryphaena hippurus Linnaeus and Coryphaena equiselis Linnaeus. NOA Technical Report NMFS Circular 43. FAO Fisheries, synopsis 130. U.S. Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries ServiceGoogle Scholar
  49. Palm HW, Waeschenbach A, Olson PD, Littlewood DTJ (2009) Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Mol Phylogenet Evol 52:351–367.  https://doi.org/10.1016/j.ympev.2009.01.019 CrossRefPubMedGoogle Scholar
  50. Phillips ND, Reid N, Thys T, Harrod C, Payne NL, Morgan CA et al (2017) Applying species distribution modelling to a data poor, pelagic fish complex: the ocean sunfishes. J Biogeogr 44:2176–2187.  https://doi.org/10.1111/jbi.13033 CrossRefGoogle Scholar
  51. Phillips ND, Kubicek L, Payne N, Harrod C, Eagling LE, Carson CD, Cappanera V, Houghton JDR (2018) Isometric growth in the world's largest bony fishes (genus Mola)? Morphological insights from fisheries bycatch data. J Morphol 279:1312–1320.  https://doi.org/10.1002/jmor.20872 CrossRefPubMedGoogle Scholar
  52. Pitman (2017) Humpback whales interfering when mammal-eating killerwhales attack other species: mobbing behavior and interspecific altruism? Mar Mammal Sci 33:7–58.  https://doi.org/10.1111/mms.12343 CrossRefGoogle Scholar
  53. Pollerspöck J, Staube N (2015) Bibliography database of living/fossil sharks, rays and chimaeras (Chondrichthyes: Elasmobranchii, Holocephali) Host-Parasite List & Parasite-Host List Version: 01.04.2015. https://shark-references.com/species/host-parasites-list/A. Accessed 22 Apr 2019
  54. Pope EC, Hays GC, Thys TM, Doyle TK, Sims DW, Queiroz N, Hobson VJ, Kubicek L, Houghton JDR (2010) The biology and ecology of the ocean sunfish Mola mola: a review of current knowledge and future research perspectives. Rev Fish Biol Fish 20:471–487.  https://doi.org/10.1007/s11160-009-9155-9 CrossRefGoogle Scholar
  55. Powell DC (2003) A fascination for fish: adventures of an underwater pioneer. University of California Press, BerkeleyGoogle Scholar
  56. Robinson ES (1959) Records of Cestodes from marine fishes of New Zealand. T Roy Soc NZ 86:143–153Google Scholar
  57. Ryan C, Holmes JMC (2012) Killer whale Orcinus orca predation on sunfish Mola mola. Mar Biodivers Rec 5:e10.  https://doi.org/10.1017/S1755267211001187 CrossRefGoogle Scholar
  58. Sawai E, Yamanoue Y, Nyegaard M, Sakai Y (2018) Redescription of the bump-head sunfish Mola alexandrini (Ranzani 1839), senior synonym of Mola ramsayi (Giglioli 1883), with designation of a neotype for Mola mola (Linnaeus 1758) (Tetraodontiformes: Molidae). Ichthyol Res 65:142–160.  https://doi.org/10.1007/s10228-017-0603-6 CrossRefGoogle Scholar
  59. Schmidt (1921) New studies of sun-fishes made during the “Dana” expedition, 1920. Nature 107:76–79.  https://doi.org/10.1038/107076a0 CrossRefGoogle Scholar
  60. Seitz AC, Weng K, Boustany AM, Block BA (2002) Behaviour of a sharptail mola in the Gulf of Mexico. J Fish Biol 60:1597–1602.  https://doi.org/10.1006/jfbi.2002.2009 CrossRefGoogle Scholar
  61. Shimose T, Yokawa K, Tachihara K (2013) Occurrence of slender mola Ranzania laevis (pennant, 1776) in stomachs of blue marlin Makaira nigricans Lacépède, 1802. J Appl Ichthyol 29:1160–1162.  https://doi.org/10.1111/jai.12206 CrossRefGoogle Scholar
  62. Simpfendorfer CA, Goodreid AB, Mcauley RB (2001) Size, sex and geographic variation in the diet of the tiger shark, Galeocerdo cuvier, from Western Australian waters. Environ Biol Fish 61:37–46.  https://doi.org/10.1023/A:1011021710183 CrossRefGoogle Scholar
  63. Sousa LL, Xavier R, Costa V, Humphries NE, Trueman C, Rosa R, Sims DW, Queiroz N (2016) DNA barcoding identifies a cosmopolitan diet in the ocean sunfish. Sci Rep 6:28762.  https://doi.org/10.1038/srep28762 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Strong WR, Snelson FF, Gruber SH (1990) Hammerhead shark predation on stingrays: an observation of prey handling by Sphyrna mokarran. Copeia 3:836–840.  https://doi.org/10.2307/1446449 CrossRefGoogle Scholar
  65. Syväranta J, Harrod C, Kubicek L, Cappanera V, Houghton JDR (2012) Stable isotopes challenge the perception of ocean sunfish Mola mola as obligate jellyfish predators. J Fish Biol 80:225–231.  https://doi.org/10.1111/j.1095-8649.2011.03163.x CrossRefPubMedGoogle Scholar
  66. Thys TM, Hearn AR, Weng KC, Ryan JP, Peñaherrera-Palma C (2017) Satellite tracking and site fidelity of short ocean sunfish, Mola ramsayi, in the Galapagos Islands. J Mar Biol 2017:7097965.  https://doi.org/10.1155/2017/7097965 CrossRefGoogle Scholar
  67. Vaudo JJ, Wetherbee BM, Wood AD, Weng K, Howey-Jordan LA, Harvey GM, Shivji MS (2016) Vertical movements of shortfin mako sharks Isurus oxyrinchus in the western North Atlantic Ocean are strongly influenced by temperature. Mar Ecol Prog Ser 547:163–175.  https://doi.org/10.3354/meps11646 CrossRefGoogle Scholar
  68. Visser IN, Bonoccorso FJ (2003) New observations and a review of killer whale (Orcinus orca) sightings in Papua New Guinea waters. Aquat Mamm 29:150–172.  https://doi.org/10.1578/016754203101024004 CrossRefGoogle Scholar
  69. Watanabe Y, Sato K (2008) Functional dorsoventral symmetry in relation to lift-based swimming in the ocean sunfish Mola mola. PLoS One 3:e3446.  https://doi.org/10.1371/journal.pone.0003446 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Weng KC, Boustany AM, Pyle P, Anderson SD, Brown A, Block BA (2007) Migration and habitat of white sharks (Carcharodon carcharias) in the eastern Pacific Ocean. Mar Biol 152:877–894.  https://doi.org/10.1007/s00227-007-0739-4 CrossRefGoogle Scholar
  71. Wikipedia (2019) Ocean sunfish. https://en.wikipedia.org/wiki/Ocean_sunfish. Accessed 7 Aug 2019
  72. Young JW, Lansdell MJ, Campbell RA et al (2010) Feeding ecology and niche segregation in oceanic top predators off eastern Australia. Mar Biol 157:2347–2368.  https://doi.org/10.1007/s00227-010-1500-y CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Auckland War Memorial Museum Tamaki Paenga Hira, Natural SciencesAucklandNew Zealand
  2. 2.Hopkins Marine StationStanford UniversityPacific GroveUSA
  3. 3.Centre for Whale Research (WA) Inc.FremantleAustralia

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