Coral Reefs

, Volume 35, Issue 1, pp 103–112 | Cite as

An assessment of shallow and mesophotic reef brachyuran crab assemblages on the south shore of O‘ahu, Hawai‘i

  • Kaleonani K. C. HurleyEmail author
  • Molly A. Timmers
  • L. Scott Godwin
  • Joshua M. Copus
  • Derek J. Skillings
  • Robert J. Toonen


Shallow coral reefs are extensively studied but, although scleractinian corals have been recorded to 165 m, little is known about other mesophotic coral reef ecosystem (MCE) inhabitants. Brachyuran crabs fill many ecological and trophic niches on reefs, making them ideal candidates for evaluating species composition among depths to ask whether MCEs host the same communities as shallower reef communities that have been well studied. Here we deployed autonomous reef monitoring structures for 2 yr on the south shore of O‘ahu along a depth gradient (12, 30, 60, and 90 m) to sample and assess brachyuran crab communities. A total of 663 brachyuran crabs representing 69 morphospecies (16 families) were found. Community composition was not significantly different within depths, but was highly stratified by depth. Each depth was distinct, but the 30 and 60 m depths were least dissimilar from one another. We show that deeper reefs host significantly different brachyuran communities, and at much lower total abundance, than shallow reefs in Hawai‘i, with 4–27 unique morphospecies per depth and only 3 of 69 morphospecies (~4 %) occurring across the entire depth range sampled.


Biodiversity Depth gradient Cryptic fauna Autonomous reef monitoring structures (ARMS) 



This work was funded through a combination of grants including NSF OCE 12-60169, NSF GRFP DGE-1329626, the Jessie D. Kay Fellowship, the Seaver Institute, a UH Mānoa Arts and Humanities Grant, and the Carol Ann & Myron K. Hayashida Scholarship. We thank NOAA Coral Reef Ecosystem Division and K. Reardon for generous assistance with the shallow ARMS sites and crab identifications and the UH Mānoa Dive Safety Office, D. Pence, K. Stender, J. Jones, and C.J. Bradley for installation and retrieval of the mesophotic ARMS. We thank the ToBo laboratory members, particularly M. Iacchei, C. Ka‘apu-Lyons, and Z. Hee, for discussion, support, and their efforts in the disassembly and sorting of ARMS samples on retrieval. We also thank M. Donahue, R. Coleman, and I. Knapp for their assistance with the analyses and writing. Special thanks are due to B. Bowen & M. Donahue for their service as committee members and their valuable feedback on the manuscript. This is HIMB Contribution #1640 and SOEST #9545.

Supplementary material

338_2015_1382_MOESM1_ESM.docx (3.3 mb)
Supplementary material 1 (DOCX 3424 kb)


  1. Abele LG (1972) Comparative habitat diversity and faunal relationships between the Pacific and Caribbean Panamanian decapod Crustacea: a preliminary report with remarks on the crustacean fauna of Panama. Bull Biol Soc Wash 2:125–138Google Scholar
  2. Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust N Z J Stat 45:301–318CrossRefGoogle Scholar
  3. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth, UKGoogle Scholar
  4. Bahr KD, Jokiel PL, Toonen RJ (2015) The unnatural history of Kāne‘ohe Bay: coral reef resilience in the face of centuries of anthropogenic impacts. PeerJ 3:e950PubMedCentralCrossRefPubMedGoogle Scholar
  5. Bickford D, Lohman DJ, Sodhi NS, Ng PK, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155CrossRefPubMedGoogle Scholar
  6. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327CrossRefGoogle Scholar
  7. Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh-Guldberg O (2015) Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. R Soc Open Sci 2:140297PubMedCentralCrossRefPubMedGoogle Scholar
  8. Brainard R, Moffitt R, Timmers M, Paulay G, Plaisance L, Knowlton N, Caley J, Rohrer F, Charette A, Meyer C, Toonen RJ, Godwin S, Martin J, Harris L, Geller J, Moews M (2009) Autonomous reef monitoring structures (ARMS): a tool for monitoring indices of biodiversity in the Pacific Islands. 11th Pacific Science Inter-Congress, Papeete, Tahiti
  9. Bridge TCL, Fabricius KE, Bongaerts P, Wallace CC, Muir PR, Done TJ, Webster JM (2012) Diversity of Scleractinia and Octocorallia in the mesophotic zone of the Great Barrier Reef, Australia. Coral Reefs 31:179–189CrossRefGoogle Scholar
  10. Bryan DR, Kilfoyle K, Gilmore RG, Spieler RE (2013) Characterization of the mesophotic reef fish community in south Florida, USA. J Appl Ichthyol 29:108–117CrossRefGoogle Scholar
  11. Castro P (2011) Catalog of the anomuran and brachyuran crabs (Crustacea: Decapoda: Anomura, Brachyura) of the Hawaiian Islands. Zootaxa 2947:1–154Google Scholar
  12. Chao A, Colwell RK, Lin CW, Gotelli NJ (2009) Sufficient sampling for asymptotic minimum species richness estimators. Ecology 90:1125–1133CrossRefPubMedGoogle Scholar
  13. Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UKGoogle Scholar
  14. Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User’s guide and application available at
  15. Copus JM, Pyle RL, Earle JL (2015a) Neoniphon pencei, a new species of holocentrid (Teleostei: Beryciformes) from Rarotonga, Cook Islands. Biodivers Data J 3:e4180CrossRefPubMedGoogle Scholar
  16. Copus JM, Ka‘apu-Lyons C, Pyle RL (2015b) Luzonichthys seaver, a new species of Anthiinae (Perciformes, Serranidae) from Pohnpei, Micronesia. Biodivers Data J 3:e4902CrossRefPubMedGoogle Scholar
  17. Costello MJ, Marta Coll, Danovaro R, Halpin P, Ojaveer H, Miloslavich P (2010) A census of marine biodiversity knowledge, resources, and future challenges. PLoS One 5:e12110PubMedCentralCrossRefPubMedGoogle Scholar
  18. Edmondson CH (1954) Hawaiian Portunidae. Occasional Papers of Bernice P. Bishop Museum, Honolulu, Hawai‘i 21:217–274Google Scholar
  19. Edmondson CH (1959) Hawaiian Grapsidae. Occasional Papers of Bernice P. Bishop Museum, Honolulu, Hawai‘i 22:153–202Google Scholar
  20. Edmondson CH (1962) Xanthidae of Hawaii. Occasional Papers of Bernice P. Bishop Museum, Honolulu, Hawai‘i 22:1–309Google Scholar
  21. Engstrom NA (1984) Depth limitation of a tropical intertidal xanthid crab, Cataleptodius floridanus, and a shallow-water majid, Pitho aculeate: results of a caging experiment. J Crustacean Biol 4:55–62CrossRefGoogle Scholar
  22. Fautin D, Dalton P, Incze LS, Leong JAC, Pautzke C, Rosenberg A, Sandifer P, Sedberry G, Tunnell JW Jr, Abbott I, Brainard RE, Brodeur M, Eldredge LG, Feldman M, Moretzsohn F, Vroom PS, Wainstein M, Wolff N (2010) An overview of marine biodiversity in United States waters. PLoS One 5:e11914PubMedCentralCrossRefPubMedGoogle Scholar
  23. Garth JS, Haig J, Knudsen JW (1987) Crustacea Decapoda (Brachyura and Anomura) of Enewetak Atoll. In: Devaney DM, Reese ES, Burch BL, Helfrich P (eds) The natural history of Enewetak Atoll. Volume II, Biogeography and systematics. US Department of Energy Office of Scientific and Technical Information, Oak Ridge, TN, pp 235–261Google Scholar
  24. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 2:495–509CrossRefGoogle Scholar
  25. Goreau TF, Goreau NI (1973) The ecology of Jamaican coral reefs II. Geomorphology, zonation and sedimentary phases. Bull Mar Sci 23:299–464Google Scholar
  26. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  27. Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on “Mesophotic coral ecosystems: characterization, ecology, and management”. Coral Reefs 29:247–251CrossRefGoogle Scholar
  28. Hortal J, Borges PAV, Gaspar C (2006) Evaluating the performance of species richness estimators: sensitivity to sample grain size. J Anim Ecol 75:274–287CrossRefPubMedGoogle Scholar
  29. Jokiel PL (1987) Ecology, biogeography and evolution of corals in Hawaii. Trends Ecol Evol 2:179–182CrossRefPubMedGoogle Scholar
  30. Kahng SE, Maragos JE (2006) The deepest, zooxanthellate scleractinian corals in the world? Coral Reefs 25:254–254CrossRefGoogle Scholar
  31. Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa on a deep photosynthetic reef (50–140 m) in the Au’au Channel, Hawaii. Coral Reefs 26:679–687CrossRefGoogle Scholar
  32. Kahng SE, Copus JM, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems. Curr Opin Environ Sustain 7:72–81CrossRefGoogle Scholar
  33. Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein LM, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275CrossRefGoogle Scholar
  34. Kane C, Kosaki RK, Wagner D (2014) High levels of mesophotic reef fish endemism in the northwestern Hawaiian Islands. Bull Mar Sci 90:693–703CrossRefGoogle Scholar
  35. Kay EA (ed) (1994) A natural history of the Hawaiian Islands: selected readings II. University of Hawai‘i Press, Mānoa, HIGoogle Scholar
  36. Knowlton N, Brainard RE, Fisher R, Moews M, Plaisance L, Caley MJ (2010) Coral reef biodiversity. In: McIntyre AD (ed) Life in the world’s oceans. Wiley-Blackwell Publishing Ltd, Chichester, UK, pp 65–77CrossRefGoogle Scholar
  37. Knudsen JW (1960) Aspects of the ecology of the California xanthid crabs. Ecol Monogr 30:165–185CrossRefGoogle Scholar
  38. Lai JCY, Mendoza JCE, Guinot D, Clark PF, Ng PKL (2011) Xanthidae MacLeay, 1838 (Decapoda: Brachyura: Xanthoidea) systematics: A multi-gene approach with support from adult and zoeal morphology. Zool Anz 250:407–448CrossRefGoogle Scholar
  39. Lasley RM Jr, Klaus S, Ng PKL (2014) Phylogenetic relationships of the ubiquitous coral reef crab subfamily Chlorodiellinae (Decapoda, Brachyura, Xanthidae). Zoo Scr 44:165–178CrossRefGoogle Scholar
  40. Leray M, Knowlton N (2015) DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proc Natl Acad Sci U S A 112:2076–2081PubMedCentralCrossRefPubMedGoogle Scholar
  41. Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Bio Ecol 375:1–8CrossRefGoogle Scholar
  42. Liddell WD, Avery WE (2000) Temporal change in hard substrate communities 10–250 m, the Bahamas. Proc 10th Int Coral Reef Symp 1:437–442Google Scholar
  43. Liddell WD, Avery WE, Ohlhorst SL (1997) Patterns of benthic community structure, 10–250 m, the Bahamas. Proc 8th Int Coral Reef Symp 1:437–442Google Scholar
  44. Luck DG, Forsman ZH, Toonen RJ, Leicht SJ, Kahng SE (2013) Polyphyly and hidden species among Hawai‘i’s dominant mesophotic coral genera, Leptoseris and Pavona (Scleractinia: Agariciidae). PeerJ 1:e132PubMedCentralCrossRefPubMedGoogle Scholar
  45. Maragos JE, Jokiel PL (1986) Reef corals of Johnston Atoll: one of the world’s most isolated reefs. Coral Reefs 4:141–150CrossRefGoogle Scholar
  46. Moberg F, Folke C (1999) Ecological goods and services of coral reef ecosystems. Ecol Econ 29:215–233CrossRefGoogle Scholar
  47. Monteforte M (1987) The decapod reptantia and stomatopod crustaceans of a typical high island coral reef complex in French Polynesia (Tiahura, Moorea Island): zonation, community composition and trophic structure. Atoll Res Bull 309:1–37CrossRefGoogle Scholar
  48. Ng PKL, Guinot D, Davie PJF (2008) Systema Brachyororum: Part I. An annotated checklist of extant brachyuran crabs of the world. Raffles Bull Zool 17:1–286Google Scholar
  49. Paulay G, Kropp R, Ng PKL, Eldredge LG (2003) The crustaceans and pycnogonids of the Mariana Islands. Micronesica 35–36:456–513Google Scholar
  50. Petrescu I, Chatterjee T, Schizas NV (2012) New genus and new species of Cumacea (Crustacea: Peracarida) from the mesophotic coral ecosystem of SW Puerto Rico, Caribbean Sea. Zootaxa 3476:55–61Google Scholar
  51. Petrescu I, Chatterjee T, Schizas NV (2013) Two new species of the genus Cumella (Crustacea: Cumacea: Nannastacidae) associated with mesophotic reefs of Puerto Rico and St. Croix, Caribbean Sea. Cah Biol Mar 54:257–262Google Scholar
  52. Plaisance L, Knowlton N, Paulay G, Meyer C (2009) Reef-associated crustacean fauna: biodiversity estimates using semi-quantitative sampling and DNA barcoding. Coral Reefs 28:977–986CrossRefGoogle Scholar
  53. Plaisance L, Caley MJ, Brainard RE, Knowlton N (2011) The diversity of coral reefs: what are we missing? PLoS One 6:e25026PubMedCentralCrossRefPubMedGoogle Scholar
  54. Pochon X, Forsman ZH, Spalding HL, Padilla-Gamiño JL, Smith CM, Gates RD (2015) Depth specialization in mesophotic corals (Leptoseris spp.) and associated algal symbionts in Hawai’i. R Soc Open Sci 2:140351PubMedCentralCrossRefPubMedGoogle Scholar
  55. Poupin J (1996) Crustacea Decapoda of French Polynesia (Astacidea, Palinuridea, Anomura, Brachyura). Atoll Res Bull 442:1–114Google Scholar
  56. Pyle RL (2000) Assessing undiscovered fish biodiversity on deep coral reefs using advanced self-contained diving technology. Mar Technol Soc J 34:82–91CrossRefGoogle Scholar
  57. Pyle RL, Earle JL, Greene BD (2008) Five new species of the damselfish genus Chromis (Perciformes: Labroidei: Pomacentridae) from deep coral reefs in the tropical western Pacific. Zootaxa 1671:3–31Google Scholar
  58. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  59. Rezak R, Bright TJ, McGrail DW (1985) Reefs and banks of the Northwestern Gulf of Mexico: their geological, biological, and physical dynamics. Wiley, New YorkGoogle Scholar
  60. Rathbun MJ (1906) The brachyura and macrura of the Hawaiian Islands. Bulletin of the United States Fish Commission 23:827–930Google Scholar
  61. Roberts CM, McClean CJ, Veron JE, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284CrossRefPubMedGoogle Scholar
  62. Rooney J, Donham E, Montgomery A, Spalding H, Parrish F, Boland R, Fenner D, Gove J, Vetter O (2010) Mesophotic coral ecosystems in the Hawaiian Archipelago. Coral Reefs 29:361–367CrossRefGoogle Scholar
  63. Small A, Adey A, Spoon D (1998) Are current estimates of coral reef biodiversity too low? The view through the window of a microcosm. Atoll Res Bull 458:1–20CrossRefGoogle Scholar
  64. Wagner D, Kosaki RK, Spalding HL, Whitton RK, Pyle RL, Sherwood AR, Tsuda RT, Calcinai B (2014) Mesophotic surveys of the flora and fauna at Johnston Atoll, Central Pacific Ocean. Mar Biodivers Rec 7:e68CrossRefGoogle Scholar
  65. Wainwright PC, Bellwood DR (2002) Ecomorphology of feeding in coral reef fishes. In: Sale PF (ed) coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 33–55CrossRefGoogle Scholar
  66. Walther BA, Moore JL (2005) The concepts of bias, precision and accuracy, and their use in testing the performance of species richness estimators, with a literature review of estimator performance. Ecography 28:815–829CrossRefGoogle Scholar
  67. Wellington GM (1982) Depth zonation of corals in the Gulf of Panama: control and facilitation by resident reef fishes. Ecol Monogr 3:224–241Google Scholar
  68. White KN, Ohara T, Fujii T, Kawamura I, Mizuyama M, Montenegro J, Shikiba H, Naruse T, McClelland T, Denis V, Reimer JD (2013) Typhoon damage on a shallow mesophotic reef in Okinawa, Japan. PeerJ 1:e151PubMedCentralCrossRefPubMedGoogle Scholar
  69. Willis TJ, Anderson MJ (2003) Structure of cryptic reef fish assemblages: relationships with habitat characteristics and predator density. Mar Ecol Prog Ser 257:209–221CrossRefGoogle Scholar
  70. Yarnall JL (1969) Aspects of the behavior of Octopus cyanea Gray, 1849. Anim Behav 17:747–754CrossRefGoogle Scholar
  71. Ziegler AC (2002) Hawaiian natural history, ecology, and evolution. University of Hawai‘i Press, MānoaGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.The Hawai‘i Institute of Marine BiologyUniversity of Hawai‘i at MānoaKaneoheUSA
  2. 2.Joint Institute for Marine and Atmospheric ResearchUniversity of Hawai‘i at MānoaHonoluluUSA
  3. 3.Ecosystem Sciences Division, Pacific Islands Fisheries Science CenterNational Oceanic and Atmospheric AdministrationHonoluluUSA
  4. 4.Office of National Marine Sanctuaries, Papahānaumokuākea Marine National MonumentNational Oceanic and Atmospheric AdministrationHonoluluUSA
  5. 5.Brooklyn CollegeBrooklynUSA

Personalised recommendations