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Environmental Biology of Fishes

, Volume 97, Issue 4, pp 371–383 | Cite as

Restricted movements of juvenile rays in the lagoon of Ningaloo Reef, Western Australia – evidence for the existence of a nursery

  • F. Cerutti-PereyraEmail author
  • M. Thums
  • C. M. Austin
  • C. J. A. Bradshaw
  • J. D. Stevens
  • R. C. Babcock
  • R. D. Pillans
  • M. G. Meekan
Article

Abstract

Little information is available on the movements and behaviour of tropical rays despite their potential ecological roles and economic value as a fishery and a tourism resource. A description of the movement patterns and site fidelity of juvenile rays within a coral reef environment is provided in this study. Acoustic telemetry was used to focus on the use of potential nursery areas and describe movement patterns of 16 individuals of four species monitored for 1–21 months within an array of 51 listening stations deployed across a lagoon, reef crest, and reef slope at Mangrove Bay, Ningaloo Reef, Western Australia. Juveniles used a small (< 1 km2), shallow (1–2 m depth) embayment where three receivers recorded 60–80 % of total detections of tagged animals, although individuals of all species moved throughout the array and beyond the lagoon to the open reef slope. Detections at these primary sites were more frequent during winter and when water temperatures were highest during the day. Long-term use of coastal lagoons by juvenile rays suggests that they provide an important habitat for this life stage. Current marine park zoning appears to provide an effective protection for juveniles within this area.

Keywords

Batoids Key habitats Marine protected areas Indo-Pacific Spatial ecology Habitat use 

Notes

Acknowledgments

This research was approved by the Animal Ethics Committee from Charles Darwin University (no. A07026). We thank to the Australian Institute of Marine Science (AIMS) and CSIRO for financially supporting this project, and CONACYT-Mexico for international grant. We thank the tagging and receiver-deployment crews, P. Last for species identification, Y. Berger for analytical assistance, D. Lindsay for comments on the manuscript, A. Tan and D. McGaffin for tagging and sampling equipment manufacture, and C. Speed, F. McGregor, S. Baccarella, K. Wenziker, P. Haskell, Exmouth Light Engineering and Ningaloo Dreaming for field assistance.

Supplementary material

10641_2013_158_MOESM1_ESM.doc (446 kb)
Fig. S1 Mangrove Bay array range testing. Proportion of detections received by VR2 receivers at increasing distances from the test transmitter in the lagoon channel (filled circles, 4 m water depth) and at Mangrove Bay (white circles, 1 m water depth) (DOC 446 kb)
10641_2013_158_MOESM2_ESM.doc (190 kb)
Fig. S2 Proportion of days spent by each species inside and outside of the Mangrove Bay sanctuary zone (DOC 190 kb)
10641_2013_158_MOESM3_ESM.doc (726 kb)
Fig. S3 Number of daily detections per ray at Mangrove Bay. Individual plots of detections of juvenile rays primary receives (solid shapes) and other receivers (hollow shapes). (DOC 725 kb)

References

  1. Ache de Freitas RH, Rosa RS, Wetherbee BM, Gruber SH (2009) Population size and survivorship for juvenile lemon sharks (Negaprion brevirostris) on their nursery grounds at marine protected area in Brazil. Neotropical Ichthyol 7:205–212Google Scholar
  2. Ackerman JT, Kondratieff MC, Matern SA, Cech JJ (2000) Tidal influence on spatial dynamics of leopard sharks, Triakis semifasciata in Tomales Bay, California. Environ Biol Fishes 58:33–43CrossRefGoogle Scholar
  3. Bates DM, Sarkar D (2007) lme4: Linear mixed-effects models using S4 classes, R package version 0.99875-6Google Scholar
  4. Branstetter S (1990) Life style of sharks. In: Gruber SH (ed) One reason sharks are vulnerable to overfishing, a volume honoring the work of Stewart Springer. American Litoral Society Highlands, New Jersey, pp 23–29Google Scholar
  5. Burnham KP, Anderson DR (2002) Model selection and multimodel Inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  6. Castro JI (1993) The shark nursery of Bulls Bay, South Carolina, with a review of the shark nurseries of the southeastern coast of the United States. Environ Biol Fishes 38:37–48CrossRefGoogle Scholar
  7. Cerutti-Pereyra F, Meekan MG, Wei N-WV, O’Shea O, Bradshaw CJA, Austin CM (2012) Identification of Rays through DNA Barcoding: An Application for Ecologists. PLoS One 7:e36479PubMedCentralPubMedCrossRefGoogle Scholar
  8. Chapman DD, Babcock EA, Gruber SH, Dibattista JD, Franks BR, Kessel SA, Guttridge T, Pikitch EK, Feldheim KA (2009) Long-term natal site-fidelity by immature lemon sharks (Negaprion brevirostris) at a subtropical island. Mol Ecol 18:3500–3507PubMedCrossRefGoogle Scholar
  9. Collins A, Heupel MR, Motta PJ (2007) Residence and movement patterns of cownose rays Rhinoptera bonasus within a south-west Florida estuary. J Fish Biol 71:1159–1178CrossRefGoogle Scholar
  10. Conrath CL (2008) Investigations into depth and temperature habitat utilization and overwintering grounds of juvenile sandbar sharks, Carcharhinus plumbeus: the importance of near shore North Carolina waters. Environ Biol Fishes 82:123–131CrossRefGoogle Scholar
  11. Dale JJ, Wallsgrove NJ, Popp BN, Holland K (2011) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar Ecol Prog Ser 433:221–236CrossRefGoogle Scholar
  12. Dames L, Moore (2000) Ningaloo Marine Park (Commonwealth Waters) Literature reviewGoogle Scholar
  13. DeAngelis BM (2008) First characterization of shark nursery habitat in the United States Virgin Islands: evidence of habitat partitioning by two shark species. Mar Ecol Prog Ser 358:257–271CrossRefGoogle Scholar
  14. Department of Conservation and Land Management (2005) Management plan for the Ningaloo Marine Park and Muiron Islands Marine Management Area 2005–2015. Management Plan no. 52. Department of Conservation and Land Management, PerthGoogle Scholar
  15. Dewar H, Mous P, Domenier M, Muljadi A, Pet J, Whitty J (2008) Movements and site fidelity of the giant manta ray, Manta birostris, in the Komodo Marine Park, Indonesia. Mar Biol 151:121–133CrossRefGoogle Scholar
  16. Di Santo V, Bennett WA (2011) Is post-feeding thermotaxis advantageous in elasmobranch fishes? J Fish Biol 78:195–207PubMedCrossRefGoogle Scholar
  17. DiGirolamo AL, Gruber SH, Pomory C, Bennett WA (2012) Diel temperature patterns of juvenile lemon sharks Negaprion brevirostris, in a shallow-water nursery. J Fish Biol 80:1436–1448PubMedCrossRefGoogle Scholar
  18. Dulvy NK, Reynolds JD (2002) Predicting extinction vulnerability in skates. Predicción de la vulnerabilidad de extinción en rayas. Conserv Biol 16:440–450CrossRefGoogle Scholar
  19. Dulvy NK, Metcalfe JD, Glanville J, Pawson MG, Reynolds JD (2000) Fishery stability, local extinctions, and shifts in community structure in skates. Estabilidad de la pesquería, extinciones locales y cambios en la estructura de comunidades de rayas. Conserv Biol 14:283–293CrossRefGoogle Scholar
  20. Economakis AE, Lobel PS (1998) Aggregation behavior of the gray reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, central Pacific Ocean. Environ Biol Fishes 51:129–139CrossRefGoogle Scholar
  21. Fangue NA, Bennett WA, Douglas ME (2003) Thermal tolerance responses of laboratory-acclimated and seasonally acclimatized Atlantic stingray, Dasyatis sabina. Copeia 2003:315–325CrossRefGoogle Scholar
  22. Frisk MG (2010) Life history strategies of Batoids. In: Carrier JC, Musick JA, Heithaus MR (eds) The Biology of Sharks and their Relatives. CRC Press, Boca Raton, pp 283–316CrossRefGoogle Scholar
  23. Garla RC, Chapman DD, Shivji MS, Wetherbee BM, Amorim AF (2006a) Habitat of juvenile Caribbean reef sharks, Carcharhinus perezi, at two oceanic insular marine protected areas in the southwestern Atlantic Ocean: Fernando de Noronha Archipelago and Atol das Rocas, Brazil. Fish Res 81:236–241CrossRefGoogle Scholar
  24. Garla RC, Chapman DD, Wetherbee BM, Shivji M (2006b) Movement patterns of young Caribbean reef sharks, Carcharhinus perezii, at Fernando de Noronha Archipelago, Brazil: the potential of marine protected areas for conservation of a nursery ground. Mar Biol 149:189–199CrossRefGoogle Scholar
  25. Grubbs RD, Musick JA, Conrath CL, Romine JG (2005) Long-term movements, migration and temporal delineation of a summer nursery for juvenile sandbar sharks in the Chesapeake Bay Region. American Fisheries Society Symposium:1–22Google Scholar
  26. Heupel M (2007) Exiting Terra Ceia Bay: an examination of cues stimulating migration from a summer nursery area. Am Fish Soc Symp 50:265–280Google Scholar
  27. Heupel M, Heuter R (2001) Use of a remote acoustic telemetry system to monitor shark movements in a coastal nursery area. In: Sibert JR, Nielsen JL (eds) Electronic Tagging and Tracking in Marine Fisheries. Kluwer Academic Publishers, Amsterdam, pp 217–223CrossRefGoogle Scholar
  28. Heupel M, Simpfendorfer CA, Hueter RE (2004) Estimation of shark home ranges using passive monitoring techniques. Environ Biol Fishes 71:135–142CrossRefGoogle Scholar
  29. Heupel M, Simpfendorfer CA, Collins AB, Tyminski JP (2006) Residency and movement patterns of bonnethead sharks, Sphyrna tiburo, in a large Florida estuary. Environ Biol Fishes 76:47–67CrossRefGoogle Scholar
  30. Heupel MR, Carslon JK, Simpfendorfer C (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser 337:287–297CrossRefGoogle Scholar
  31. Hight BV, Lowe CG (2007) Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: Evidence for behavioral thermoregulation? J Exp Mar Biol Ecol 352:114–128CrossRefGoogle Scholar
  32. Holland KN, Wheatherbee BM, Peterson JD, Lowe CG (1993) Movements and distribution of hammerhead shark pups on their natal ground. Copeia 1993:495–502CrossRefGoogle Scholar
  33. Hopkins TE, Cech JJ Jr (2003) The influence of environmental variables on the distribution and abundance of three elasmobranchs in Tomales Bay. Calif Environ Biol Fish 66:279–291CrossRefGoogle Scholar
  34. Huveneers C, Harcourt R, Boomer A, Hobday AJ, Pederson H, Semmens JM, Stieglitz T, Vallee R, Webber D, Heupel M, Simpfendorfer C, Peddemors V (2009) The influence of environmental parameters (meteorological and oceanographic) on the performance of acoustic receivers. Papers from 2nd AATAMS Workshop AATAMS Workshop, Mosman, NSW, AustraliaGoogle Scholar
  35. Kinney MJ, Simpfendorfer CA (2009) Reassessing the value of nursery areas to shark conservation and management. Conserv Lett 2:53–60CrossRefGoogle Scholar
  36. Klimley AP, Kihslinger RL, Kelly JT (2005) Directional and non-directional Movements of bat rays, Myliobatis californica, in Tomales Bay, California. Environ Biol Fishes 74:79–88CrossRefGoogle Scholar
  37. Last P, Stevens J (2009) Sharks and Rays of Australia, 2nd edn. CSIRO, CollingwoodGoogle Scholar
  38. Marshall AD, Kyne PM, Bennett MB (2008) Comparing the diet of two sympatric urolophid elasmobranchs (Trygonoptera testacea Muller & Henle and Urolophus kapalensis Yearsley & Last): evidence of ontogenetic shifts and possible resource partitioning. J Fish Biol 72:883–898CrossRefGoogle Scholar
  39. Matern SA, Cech JJ, Hopkins TE (2000) Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: evidence for behavioral thermoregulation? Environ Biol Fishes 58:173–182CrossRefGoogle Scholar
  40. MATLAB (2010) MathWorks, Natick, Massachusetts, USA, http://www.mathworks.com/products/matlab/
  41. Medved RJ, Marshall JA (1983) Short-term movements of young sandbar sharks Carcharhinus plumbeus (Pisces, Carcharhinidae). Bull Mar Sci 33:87–93Google Scholar
  42. Meyer CG, Clark TB, Papastamatiou YP, Whitey NM, Holland KN (2009) Long-term movement patterns of tiger sharks Galeocerdo cuvier in Hawaii. Mar Ecol Prog Ser 381:223–235CrossRefGoogle Scholar
  43. Morrisey JF, Gruber SH (1993) Habitat selection by juvenile lemon sharks, Negaprion brevirostris. Environ Biol Fishes 38:311–319CrossRefGoogle Scholar
  44. O’Shea OR, Thums M, van Keulen M, Meekan M (2012) Bioturbation by stingrays at Ningaloo Reef, Western Australia. Mar Freshw Res 63:189–197CrossRefGoogle Scholar
  45. Papastamatiou YP, Lowe CG, Caselle JE, Friedlander AM (2009) Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecol Soc 90:996–1008CrossRefGoogle Scholar
  46. Payne NL, Gillanders BM, Webber DM, Semmens JM (2010) Interpreting diel activity patterns from acoustic telemetry: the need for controls. Mar Ecol Prog Ser 419:295–301CrossRefGoogle Scholar
  47. Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2011) nlme: linear and nonlinear mixed effects models. R package version 3.1-101.Google Scholar
  48. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Romanov EV (2001) Bycatch in the tuna purse-seine fishery in the western Indian Ocean. Fish Bull 100:90Google Scholar
  50. Rousset J (1990) Population structure of thornback rays Raja clavata and their movements in the Bay of Douarnenez. J Mar Biol Assoc UK 70:261–268CrossRefGoogle Scholar
  51. Simpfendorfer CA, Heupel M (2004) Assessing habitat use and movement. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of Sharks and their Relatives. CRC Press, Boca Raton, pp 533–571Google Scholar
  52. Sims DW, Wearmouth VJ, Southall EJ, Hill JM, Moore P, Rawlinson K, Hutchinson N, Budd GC, Righton D, Metcalfe JD, Nash JP, Morritt D (2006) Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark. J Anim Ecol 75:176–190PubMedCrossRefGoogle Scholar
  53. Speed CW, Field I, Meekan MG, Bradshaw CJA (2010) Complexities of coastal shark movements and their implications for management. Mar Ecol Prog Ser 408:275–293CrossRefGoogle Scholar
  54. Springer S (1960) Natural history of the sandbar shark, Eulamia milberti. Fish Bull 61:1–38Google Scholar
  55. Stevens J (2002) A review of Australian elasmobranch fisheries. Pages 122–126 in Elasmobranch, biodiversity, conservation and management: Proceedings of the international seminar and workshop. IUCN SSC Shark Specialist Group. IUCN, Gland and Cambridge, Sabah, Malayisia, July 1997Google Scholar
  56. Stevens J, Last PR, White WT, McAuley RB, Meekan MG (2009) Diversity, abundance and habitat utilization of sharks and rays. Final report to Western Australian Marine Science Institute. CSIROGoogle Scholar
  57. Vaudo J, Heithaus M (2009) Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay, Australia. Mar Biol 156:2579–2590CrossRefGoogle Scholar
  58. Vaudo JJ, Lowe CG (2006) Movement patterns of the round stingray Urobatis halleri (Cooper) near a thermal outfall. J Fish Biol 68:1756–1766CrossRefGoogle Scholar
  59. Ward RD, Hanner R, Hebert PDN (2009) The campaign to DNA barcode all fishes, FISH-BOL. J Fish Biol 74:329–356PubMedCrossRefGoogle Scholar
  60. Yeiser BG, Heupel MR, Simpfendorfer CA (2008) Occurrence, home range and movement patterns of juvenile bullshark (Carcharhinus leucas) and lemon (Negaprion brevirostris) sharks within a Florida estuary. Mar Freshw Res 59:489–501CrossRefGoogle Scholar
  61. Yokota L, Lessa R (2006) A nursery area for sharks and rays in northeastern Brazil. Environ Biol Fishes 75:349–360CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • F. Cerutti-Pereyra
    • 1
    Email author
  • M. Thums
    • 2
    • 3
  • C. M. Austin
    • 4
  • C. J. A. Bradshaw
    • 5
    • 6
  • J. D. Stevens
    • 7
  • R. C. Babcock
    • 8
  • R. D. Pillans
    • 8
  • M. G. Meekan
    • 2
  1. 1.Research Institute of Environment and LivelihoodsCharles Darwin UniversityCasuarinaAustralia
  2. 2.Australian Institute of Marine Science, c/o UWA Oceans Institute (MO96)CrawleyAustralia
  3. 3.School of Environmental Systems Engineering and UWA Oceans InstituteUniversity of Western Australia M470CrawleyAustralia
  4. 4.School of Science Monash University Sunway CampusPetaling JayaMalaysia
  5. 5.The Environment Institute and School of Earth and Environmental SciencesThe University of AdelaideAdelaideAustralia
  6. 6.South Australian Research and Development InstituteHenley BeachAustralia
  7. 7.CSIRO Marine and Atmospheric ResearchHobartAustralia
  8. 8.CSIRO Marine and Atmospheric Research, Ecosciences PrecinctBrisbaneAustralia

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