Marine Biology

, Volume 161, Issue 9, pp 1987–1998 | Cite as

Reliance of mobile species on sensitive habitats: a case study of manta rays (Manta alfredi) and lagoons

  • Douglas J. McCauleyEmail author
  • Paul A. DeSalles
  • Hillary S. Young
  • Yannis P. Papastamatiou
  • Jennifer E. Caselle
  • Mark H. Deakos
  • Jonathan P. A. Gardner
  • David W. Garton
  • John D. Collen
  • Fiorenza Micheli
Original Paper


Quantifying the ecological importance of individual habitats to highly mobile animals is challenging because patterns of habitat reliance for these taxa are complex and difficult to observe. We investigated the importance of lagoons to the manta ray, Manta alfredi, a wide-ranging and vulnerable species in a less-disturbed atoll ecosystem. Lagoons are highly sensitive to anthropogenic disturbance and are known to be ecologically important to a wide variety of mobile species. We used a novel combination of research tools to examine the reliance of M. alfredi on lagoon habitats. Stable isotope analysis was used to assay the recent energetic importance of lagoons to M. alfredi; high-resolution tracking data provided information about how M. alfredi utilised lagoonal habitats over long and short time periods; acoustic cameras logged patterns of animal entrances and departures from lagoons; and photo identification/laser photogrammetry provided some insight into why they may be using this habitat. M. alfredi showed strong evidence of energetic dependence on lagoon resources during the course of the study and spent long periods of residence within lagoons or frequently transited into them from elsewhere. While within lagoons, they demonstrated affinities for particular structural features within this habitat and showed evidence of temporal patterning in habitat utilization. This work sheds light on how and why M. alfredi uses lagoons and raises questions about how this use may be altered in disturbed settings. More generally, these observations contribute to our knowledge of how to assess the ecological importance of particular habitats situated within the broader home range of mobile consumers.


Atoll Forereef Habitat Utilization Disk Width Mobile Animal 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank staff at The Nature Conservancy and US Fish and Wildlife Service for field support and research permission. Funding was provided by the National Science Foundation, Stanford University, the Woods Institute for the Environment, and the Marisla Foundation. We also thank Sound Metrics Corp. and VEMCO for invaluable technical assistance. For important contributions in the laboratory and field, we thank: A. Briggs, C. Burniske, A. Carlisle, R. Dunbar, M. DeGraff, E. Hoffman, A.M. Friedlander, T. Jen, D. Mucciarone, N. Wenner, and E. Wulczyn. This represents publication #0105 of the Palmyra Atoll Research Consortium.

Supplementary material

227_2014_2478_MOESM1_ESM.doc (4 mb)
Supplementary material 1 (DOC 4087 kb)

Supplementary material 2 (MOV 18493 kb)


  1. Amerson AB Jr, Shelton PC (1976) The natural history of Johnston Atoll, central Pacific Ocean. Atoll Res Bull 192:1–479CrossRefGoogle Scholar
  2. Belcher E, Hanot W, Burch J (2002) Dual-frequency identification sonar (DIDSON). In: Underwater Technology 2002—Proceedings of the 2002 international symposium of underwater technology, Institute of Electrical and Electronics Engineers, Tokyo, 16–19 May 2002, pp 187–192Google Scholar
  3. Block BA, Dewar H, Blackwell SB, Williams TD, Prince ED, Farwell CJ, Boustany A, Teo SLH, Seitz A, Walli A, Fudge D (2001) Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna. Science 17:1310–1314CrossRefGoogle Scholar
  4. Block BA, Jonsen ID, Jorgensen SJ, Winship AJ, Shaffer SA, Bograd SJ, Hazen EL, Foley DG, Breed GA, Harrison AL, Ganong JE, Swithenbank A, Castleton M, Dewar H, Mate BR, Shillinger GL, Schaefer KM, Bensen SR, Weise MJ, Henry RW, Costa DP (2011) Tracking marine apex predator movements in a dynamic ocean. Nature 475:86–90CrossRefGoogle Scholar
  5. Blumenthal JM, Austin TJ, Bothwell JB, Broderick AC, Ebanks-Petrie G, Olynik JR, Orr MF, Solomon JL, Witt MJ, Godley BJ (2010) Life in (and out of) the lagoon: fine-scale movements of green turtles tracked using time-depth recorders. Aquat Biol 9:113–121CrossRefGoogle Scholar
  6. Braun CD, Skomal GB, Thorrold SR, Berumen ML (2014) Diving behavior of the reef manta ray links coral reefs with adjacent deep pelagic habitats. PLoS One 9:e88170CrossRefGoogle Scholar
  7. Cartamil DP, Vaudo JJ, Lowe CG, Wetherbee BM, Holland KN (2003) Diel movement patterns of the Hawaiian stingray, Dasyatis lata: implications for ecological interactions between sympatric elasmobranch species. Mar Biol 143:841–847Google Scholar
  8. Clark TB (2010) Abundance, home range, and movement patterns of manta rays (Manta alfredi, Manta birostris) in Hawai’i. Dissertation, University of Hawai’iGoogle Scholar
  9. Collen JD, Garton DW, Gardner JPA (2009) Shoreline changes and sediment redistribution at Palmyra Atoll (Equatorial Pacific Ocean): 1874–present. J Coast Res 25:711–722CrossRefGoogle Scholar
  10. Couturier LI, Jaine FRA, Townsend KA, Weeks SJ, Richardson AJ, Bennett MB (2011) Distribution, site affinity, and regional movements of the manta ray, Manta alfredi (Krefft, 1868), along the east coast of Australia. Mar Freshw Res 62:628–637CrossRefGoogle Scholar
  11. Couturier LIE, Rohner CA, Richardson AJ, Marshall AD, Jaine FRA, Bennett MB, Townsend KA, Weeks SJ, Nichols PD (2013) Stable isotope and signature fatty acid analyses suggest reef mantas feed on demersal zooplankton. PLoS One 8(10):e77152. doi: 10.1371/journal.pone.0077152 CrossRefGoogle Scholar
  12. Dale JI, Wallsgrove NJ, Popp BN, Holland KN (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
  13. Deakos MH (2010) Paired-laser photogrammetry as a simple and accurate system for measuring the body size of free-ranging manta rays Manta alfredi. Aquat Biol 10:1–10CrossRefGoogle Scholar
  14. Debinski DM, Holt RD (2000) A survey and overview of habitat fragmentation experiments. Conserv Biol 14:342–355CrossRefGoogle Scholar
  15. Delesalle B, Sournia A (1992) Residence time of water and phytoplankton biomass in coral-reef lagoons. Cont Shelf Res 12:939–949CrossRefGoogle Scholar
  16. Dewar H, Mous P, Domeier 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 155:121–133CrossRefGoogle Scholar
  17. Economakis AE, Lobel PS (1998) Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environ Biol Fish 51:129–139CrossRefGoogle Scholar
  18. Fagoonee I (1990) Coastal marine ecosystems of Mauritius. Hydrobiologia 208:55–62CrossRefGoogle Scholar
  19. Ferraroli S, Georges JY, Gaspar P, Maho YL (2004) Where leatherback turtles meet fisheries. Nature 429:521–522CrossRefGoogle Scholar
  20. Gardner JPA, Garton DW, Collen JD (2011) Near-surface mixing and pronounced deep-water stratification in a compartmentalised, human-disturbed atoll lagoon system. Coral Reefs 30:271–282CrossRefGoogle Scholar
  21. Graham RT, Witt MJ, Castellanos DW, Remolina F, Maxwell S, Godley BJ, Hawkes LA (2012) Satellite tracking of manta rays highlights challenges to their conservation. PLoS One 7:e36834. doi: 10.1371/journal.pone.0036834 CrossRefGoogle Scholar
  22. Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization, and assumptions. Mar Ecol Prog Ser 337:287–297CrossRefGoogle Scholar
  23. Homma K, Maruyama T, Itoh T, Ishihara H, Uchida S (1997) In: Séret B, Sire JY (eds) Biology of the manta ray, Manta birostris, Walbaum, in the Indo-Pacific. Proceedings of the 5th Indo-Pacific fish conference, Nouméa, 3–8 November 1997, pp 209–216Google Scholar
  24. Hooge PN, Eichenlaub WM (2000) Animal movement extension to Arcview. Version 2.0. Alaska Science Center-Biological Science Office, U.S. Geological Survey, Anchorage, AK, USAGoogle Scholar
  25. Jacquet S, Delesalle B, Torreton JP, Blanchot J (2006) Response of phytoplankton communities to increased anthropogenic influences (southwestern lagoon, New Caledonia). Mar Ecol Prog Ser 320:65–78CrossRefGoogle Scholar
  26. James MC, Ottensmeyer CA, Myers RA (2005) Identification of high-use habitats and threats to leatherback sea turtles in northern waters: new directions for conservation. Ecol Lett 8:195–201CrossRefGoogle Scholar
  27. Karczmarski L, Würsig B, Gailey G, Larson KW, Vanderlip C (2005) Spinner dolphins in a remote Hawaiian atoll: social grouping and population structure. Behav Ecol 16:675–685CrossRefGoogle Scholar
  28. Koch PL (2007) Isotopic study of the biology of modern and fossil vertebrates. In: Michener RH, Lajtha K (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell, Massachusetts, pp 99–154CrossRefGoogle Scholar
  29. Le Borgne R, Rodier M, Le Bouteiller A, Kulbicki M (1997) Plankton biomass and production in an open atoll lagoon: Uvea, New Calendonia. J Exp Mar Biol Ecol 212:187–210CrossRefGoogle Scholar
  30. Logan JM, Lutcvage ME (2010) Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644:231–244CrossRefGoogle Scholar
  31. Luiz OJ Jr, Balboni AP, Kodja G, Andrade M, Marum H (2009) Seasonal occurrences of Manta birostris (Chondrichthyes: Mobulidae) in southeastern Brazil. Ichthyol Res 56:96–99CrossRefGoogle Scholar
  32. Madhupratap M, Achuthankutty CT, Nair SRS (1991) Zooplankton of the lagoons of the Laccadives—diel patterns and emergence. J Plankton Res 13:947–958CrossRefGoogle Scholar
  33. Malpica-Cruz L, Herzka SZ, Sosa-Nishizaki O, Lazo JP (2012) Tissue-specific isotope trophic discrimination factors and turnover rates in a marine elasmobranch: empirical and modeling results. Can J Fish Aquat Sci 69:551–564CrossRefGoogle Scholar
  34. Marshall AD, Bennett MB (2010) The frequency and effect of shark-inflicted bite injuries to the reef manta ray Manta alfredi. Afr J Mar Sci 32:573–580CrossRefGoogle Scholar
  35. Marshall AD, Dudgeon CL, Bennett MB (2011a) Size and structure of a photographically identified population of manta rays Manta alfredi in southern Mozambique. Mar Biol 158:1111–1124CrossRefGoogle Scholar
  36. Marshall A, Kashiwagi T, Bennett MB, Deakos M, Stevens G, McGregor F, Clark T, Ishihara H, Sato K (2011) Manta alfredi. In: IUCN 2011. IUCN Red List of Threatened Species (Version 2011.2).
  37. Matern SA, Cech JJ Jr, Hopkins TE (2000) Diel movements of bat rays, Myliobatis californica in Tomales Bay, California: evidence for behavioral thermoregulation? Environ Biol Fish 58:173–182CrossRefGoogle Scholar
  38. McCauley DJ, Micheli F, Young HS, Tittensor DP, Brumbaugh DR, Madin EMP, Holmes KE, Smith JE, Lotze HK, DeSalles PA, Arnold SN, Worm B (2010) Acute effects of removing large fish from a near-pristine coral reef. Mar Biol 157:2739–2750CrossRefGoogle Scholar
  39. McCauley DJ, DeSalles PA, Young HS, Dunbar RB, Dirzo R, Mills MM, Micheli F (2012a) From wing to wing: the persistence of long ecological interaction chains in less-disturbed ecosystems. Sci Rep 2. doi: 10.1038/srep00409
  40. McCauley DJ, McLean KA, Bauer J, Young HS, Micheli F (2012b) Evaluating the performance of methods for estimating the abundance of rapidly declining coastal shark populations. Ecol Appl 22:385–392CrossRefGoogle Scholar
  41. McCauley DJ, Young HS, Dunbar RB, Estes JA, Micheli F (2012c) Assessing the effects of large mobile predators on ecosystem connectivity. Ecol Appl 22:1711–1717CrossRefGoogle Scholar
  42. Mendonca MT, Ehrhart LM (1982) Activity, population size and structure of immature Chelonia mydas and Caretta caretta in Mosquito Lagoon, Florida. Copeia 1982:161–167CrossRefGoogle Scholar
  43. Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480CrossRefGoogle Scholar
  44. Morrissey JF, Gruber SH (1993) Habitat selection by juvenile lemon sharks, Negaprion brevirostris. Environ Biol Fish 38:311–319CrossRefGoogle Scholar
  45. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283CrossRefGoogle Scholar
  46. NOAA (2006) Office of Coast Survey. Palmyra Atoll; Approaches to Palmyra Atoll. Chart 83157, Ed. 6.
  47. Noss RF, Quigley HB, Hornocker MG, Merrill T, Paquet PC (1996) Conservation biology and carnivore conservation in the Rocky Mountains. Conserv Biol 10:949–963CrossRefGoogle Scholar
  48. Papastamatiou YP, Lowe CG, Caselle JE, Friedlander AM (2009a) Scale-dependent effects of habitat on movements and path structure of reef sharks at a predator-dominated atoll. Ecology 90:996–1008CrossRefGoogle Scholar
  49. Papastamatiou YP, Caselle JE, Friedlander AM, Lowe CG (2009b) Distribution, size frequency, and sex ratios of blacktip reef sharks Carcharhinus melanopterus at Palmyra Atoll: a predator-dominated ecosystem. J Fish Biol 75:647–654CrossRefGoogle Scholar
  50. Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Biol Ecol 386:94–102CrossRefGoogle Scholar
  51. Papastamatiou YP, DeSalles PD, McCauley DJ (2012) Area-restricted searching by manta rays and their response to spatial scale in lagoon habitats. Mar Ecol Prog Ser 456:233–244CrossRefGoogle Scholar
  52. Pedersen MW, Weng KC (2013) Estimating individual animal movement from observation networks. Methods Ecol Evol 4:920–929Google Scholar
  53. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  54. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  55. Seaman DE, Powell RA (1996) An evaluation of the accuracy of kernel density estimators for home range analysis. Ecology 77:2075–2085CrossRefGoogle Scholar
  56. Silliman W, Gruber S (1999) Behavioral biology of the spotted eagle ray, Aetobatus narinari. Bahamas J Sci 7:13–20Google Scholar
  57. Techera EJ, Klein N (2011) Fragmented governance: reconciling legal strategies for shark conservation and management. Mar Pol 35:73–78CrossRefGoogle Scholar
  58. Terborgh J, Estes J (2010) Trophic cascades: predators, prey, and the changing dynamics of nature. Island Press, WashingtonGoogle Scholar
  59. Vaudo JJ, Heithaus MR (2012) Diel and seasonal variation in the use of a nearshore sandflat by a ray community in a near pristine system. Mar Freshw Res 63:1077–1084CrossRefGoogle Scholar
  60. Williams ID, Richards BM, Sandin SA, Baum JK, Schroeder RE, Nadon MO, Zgliczynski B, Craig P, McIlwain JL, Brainard RE (2011) Differences in reef fish assemblages between populated and remote reefs spanning multiple archipelagos across the central and western Pacific. J Mar Biol. doi: 10.1155/2011/826234 Google Scholar
  61. Woodroffe R, Ginsberg JR (1998) Edge effects and the extinctions of populations inside protected areas. Science 280:2126–2128CrossRefGoogle Scholar
  62. Yong W, Finch DM, Moore FR, Kelly JF (1998) Stopover ecology and habitat use of migratory Wilson’s warblers. Auk 115:829–842CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Douglas J. McCauley
    • 1
    Email author
  • Paul A. DeSalles
    • 2
  • Hillary S. Young
    • 1
  • Yannis P. Papastamatiou
    • 3
  • Jennifer E. Caselle
    • 4
  • Mark H. Deakos
    • 5
  • Jonathan P. A. Gardner
    • 6
  • David W. Garton
    • 7
  • John D. Collen
    • 6
  • Fiorenza Micheli
    • 2
  1. 1.Department of Ecology, Evolution, and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  2. 2.Hopkins Marine StationStanford UniversityPacific GroveUSA
  3. 3.School of BiologyUniversity of St AndrewsSt Andrews, FifeUK
  4. 4.Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA
  5. 5.Hawaii Association for Marine Education and Research, Inc.LahainaUSA
  6. 6.Centre for Marine Environmental and Economic ResearchVictoria University of WellingtonWellingtonNew Zealand
  7. 7.School of BiologyGeorgia Institute of TechnologyAtlantaUSA

Personalised recommendations