Rapid wound healing in a reef manta ray masks the extent of vessel strike


Autoři: Frazer McGregor aff001;  Anthony J. Richardson aff002;  Amelia J. Armstrong aff004;  Asia O. Armstrong aff004;  Christine L. Dudgeon aff004
Působiště autorů: Murdoch University Field Station, 1 Banksia Drive Coral Bay, Australia aff001;  Centre for Applications in Natural Resource Mathematics (CARM), School of Mathematics and Physics, The University of Queensland, QLD, Australia aff002;  CSIRO Oceans and Atmosphere, Queensland Biosciences Precinct (QBP), QLD, Australia aff003;  School of Biomedical Sciences, The University of Queensland, St. Lucia, Qld, Australia aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225681

Souhrn

Increasing vessel traffic in the marine environment due to commercial and recreational activities has amplified the number of conflicts with marine animals. However, there are limited multi-year observations of the healing rate of marine animals following vessel strike. Here we document the healing rate of a reef manta ray Mobula alfredi, following lacerations caused by a propeller along the pectoral fin. We demonstrate a high healing capacity, with wound length following a negative exponential curve over time. Lacerations healed to 5% of the initial wound length (i.e. 95% closure) within 295 days. The wounds appeared to stabilise at this point as observed more than three years following the incident and resulted in a distinctive scarring pattern. Examination of an extensive photo-identification catalogue of manta rays from the Ningaloo Coast World Heritage Area showed that the scarring pattern occurs more frequently than previously recognised, as the wounds had been previously attributed to failed predation attempts. This study provides baseline information for wound healing from vessel strike in reef manta rays and indirect evidence for increased vessel strikes on manta rays within the Ningaloo Coast World Heritage Area. We discuss the implication for spatial and behavioural management of vessels around manta rays.

Klíčová slova:

Biological locomotion – Coral reefs – Elasmobranchii – Predation – Reefs – Sharks – Tissue repair – Wound healing


Zdroje

1. Tournardre J. Anthropogenic pressure on the open ocean: The growth of ship traffic revealed by altimeter data analysis. Geophysical Research Letters. 2014;41:7924–31.

2. Shimada T, Limpus C, Jones R, Hamaan M. Aligning habitat use with management zoning to reduce vessel strike of sea turtles. Ocean and Coastal Management. 2017;142:163–72.

3. Groom RA, Lawler IR, Marsh H. The risk to dugongs of vessel strike in the Southern Bay Islands area of Moreton Bay. 2004.

4. Hazel J, Gyuris E. Vessel-related mortality of sea turtles in Queensland, Australia. Wildlife Research. 2006;33(149–154).

5. Hodgson AJ, Marsh H. Response of dugongs to boat traffic: The risk of disturbance and displacement. Journa of Experimental Marine Biology and Ecology. 2007;340:50–61.

6. Redfern JV, McKenna MF, Moore TJ, Calambokidis J, deAngelis ML, Becker EA, et al. Assessing the risk of ships striking large whales in marine spatial planning. Conservation Biology. 2013;27:292–302. doi: 10.1111/cobi.12029 23521668

7. Dywer S, Kozmian-Ledward L, Stockin K. Short-term survival of severe propeller strike injuries and observations on wound progression in a bottlenose dolphin. New Zealand Journal of Marine and Freshwater Research. 2014;48:294–302.

8. Peel D, Kelly N, Smith J, Childerhouse S. Project C5—scoping of potential species for ship strike risk analysis: pressures and impacts. 2016.

9. Sims DW, Southall EJ, Tarling GA, Metcalfe JD. Habitat-specific normal and reverse diel vertical migration in the plankton-feeding basking shark. Journal of Animal Ecology. 2005;74:755–61.

10. Motta PJ, Maslanka M, Heuter 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. 2010;113:199–212. doi: 10.1016/j.zool.2009.12.001 20817493

11. Braun CD, Skomal GB, Thorrold SR, Berumen ML. Diving behavior of the reef manta ray links coral reefs with adjacent deep pelagic habitats. PloS ONE. 2014;9(2):e88170. doi: 10.1371/journal.pone.0088170 24516605

12. Thorrold SR, Afonso P, Fontes J, Braun CD, Santos RS, Skomal GB, et al. Extreme diving behaviour in devil rays links surface waters and the deep ocean. Nature communications. 2014;5:4274. doi: 10.1038/ncomms5274 24983949

13. Vaudo JJ, Wetherbee BM, Harvey G, Nemeth RS, Aming C, Burnie N, et al. Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic. Ecology and Evolution. 2014;4:1768–86. doi: 10.1002/ece3.1053 24963376

14. Campana SE, Joyce W, Fowler M, Showell M. Discards, hooking, and post-release mortality of porbeagle (Lamna nasus), shortfin mako (Isurus oxyrinchus), and blue shark (Prionace glauca) in the Canadian pelagic longline fishery. ICES Journal of Marine Science. 2015;73(2):520–8.

15. Marshall AD, Bennett MB. The frequency and effect of shark-inflicted bite injuries to the reef manta ray Manta alfredi. African Journal of Marine Science. 2010;32:573–80.

16. Kajiura SM, Sebastian AP, Tricas TC. Dermal bite wounds as indicators of reproducive seasonality and behaviour in the Atlantic stingray, Dasyatis sabina. Environmental Biology of Fishes. 2000;58:23–31.

17. Speed CW, Meekan MG, Rowat D, Pierce SJ, Marshall AD, Bradshaw CJA. Scarring patterns and relative mortality rates of Indian Ocean whale sharks. Journal of Fish Biology. 2008;72(6):1488–503. doi: 10.1111/j.1095-8649.2008.01810.x ISI:000254809200017.

18. Chin A, Mourier J, Rummer JL. Blacktip reef sharks (Carcharhinus melanopterus) show high capacity for wound healing and recovery following injury. Conservation Physiology. 2015;3(1):cov062. doi: 10.1093/conphys/cov062 27293741

19. Bansemer CS, Bennett MB. Retained fishing gear and associated injuries in the east Australian grey nurse sharks (Carcharias taurus): implications for population recovery. Marine and Freshwater Research. 2010;61:97–103. doi: 10.1071/MF08362

20. Deakos MH, Baker JD, Bejder L. Characteristics of a manta ray Manta alfredi population off Maui, Hawaii, and implications for management. Marine Ecology Progress Series. 2011;429:245–60.

21. Domeier M, Nasby-Lucas N. Annual re-sightings of photographically identified white sharks (Carcharodon carcharias) at an eastern Pacific aggregation site (Guadalupe Island, Mexico). Marine Biology. 2007;150:977–84.

22. Marra NJ, Richards VP, Early A, Bogdanowicz SM, Pavinski Bitar PD, Stanhope MJ, et al. Comparative transcriptomics of elasmobranchs and teleosts highlight important processes in adaptive immunity and regional endothermy. BMC Genomics. 2017;18:87 (2017). doi: 10.1186/s12864-016-3411-x 28132643

23. Heupel MR, Simpfendorfer CA, Bennett MB. Analysis of tissue responses to fin tagging in Australian carcharhinids. Journal of Fish Biology. 1998;52:610–20.

24. Kitchen-Wheeler AM. Visual identification of individual manta ray (Manta alfredi) in the Maldives Islands, Western Indian Ocean. Marine Biology Research. 2010;6:351–63.

25. Towner A, Smale MJ, Jewell OJD. Boat-strike wound healing in Carcharodon carcharias. In: Domeier ML, editor. Global perspectives on the biology and life history of the white shark. First ed. Boca Raton, USA: CRC Press; 2012.

26. Smallwood CB, Beckley LE, Moore SA. An analysis of visitor movement patterns using travel networks in a large marine park, north-western Australia. Tourism Management. 2012;33:517–28.

27. Smallwood CB, Beckley LE, Moore SA, Kobryn HT. Assessing patterns of recreational use in large marine parks: A case study from Ningaloo Marine Park, Australia. Ocean and Coastal Management. 2011;54:330–40.

28. Marshall AD, Compagno LJV, Bennett MB. Redescription of the genus Manta with resurrection of Manta alfredi (Krefft, 1868) (Chondrichthyes; Myliobatoidei; Mobulidae). Zootaxa. 2009;2301:1–28.

29. Meekan MG, Bradshaw CJA, Press M, McLean C, Richards A, Quasnichka S, et al. Population size and structure of whale sharks Rhincodon typus at Ningaloo Reef, Western Australia. Marine Ecology-Progress Series. 2006;319:275–85. ISI:000241102600024.

30. Stevens GMW, Hawkins JP, Roberts CM. Courtship and mating behaviour of manta rays Mobula alfredi and M. birostris in the Maldives. Journal of Fish Biology. 2018;93:344–59. doi: 10.1111/jfb.13768 30066396

31. Deakos M. Paired-laser photogrammetry as a simple and accurate system for measuring the body size of free-ranging manta rays Manta alfredi. Aquatic Biology. 2010;10:1–10.

32. Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics. 2017;18:529. doi: 10.1186/s12859-017-1934-z 29187165

33. Bates D, Mächler B, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 2015;67:1–48.

34. Team RC. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2019.

35. Grothendieck G. nls2: Non-linear regression with brute force. R package version 0.2. 2013.

36. Reif WE. Wound healing in sharks. Zoomorphologie. 1978;90:101–11.

37. Anderson CD, Roberts RJ. A comparison of the effects of temperature on wound healing in a tropical and a temperate teleost. Journal of Fish Biology. 1975;7:173–82. https://doi.org/10.1111/j.1095-8649.1975.tb04588.x.

38. Buray N, Mourier J, Planes S, Clua E. Underwater photo-identification of sicklefin lemon sharks, Negaprion acutidens, at Moorea (French Polynesia). Cybium. 2009;33(1):21–7.

39. Couturier LIE, Jaine FRA, Townsend KA, Weeks SJ, Richardson AJ, Bennett MB. Distribution, site affinity and regional movements of the manta ray, Manta alfredi (Krefft, 1868), along the east coast of Australia. Marine and Freshwater Research. 2011;62:628–37.

40. Foster SA. A possible role of cleaning stations. Copeia. 1985;1985:875–80.

41. O'Malley MP, Lee-Brooks K, Medd HB. The global economic impact of manta ray watching tourism. Plos ONE. 2013;8(5):e65061. doi: 10.1371/journal.pone.0065061

42. Venables S, McGregor F, Brain L, van Keulen M. Manta ray tourism management, precautionary strategies for a growing industry: a case study from the Ningaloo Marine Park, Western Australia. Pacific Conservation Biology. 2016;22:295–300.

43. Schofield G, Scott R, Dimadi A, Fossette S, Katselidis KA, Koutsoubas D, et al. Evidence-based marine protected area planning for a highly mobile endangered marine vertebrate. Biological Conservation. 2013;161:101–9.

44. Pante E, Simon-Bouhet B. marmap: A package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One. 2013;9(9):e73051. doi: 10.1371/journal.pone.0073051 24019892

45. Amante C, Eakins BW. Etopo1 1 arc-minute global relief model: Procedures, data sources and analysis. NOAA Technical Memorandum NESDIS NGDC. 2009;24:1–19.

46. UNEP-WCMC & IUCN, Protected Planet: The World Database on Protected Areas (WDPA) [Internet]. 2017. Available from: https://www.protectedplanet.net


Článek vyšel v časopise

PLOS One


2019 Číslo 12