Coral Reefs

pp 1–11 | Cite as

Deep reef fishes in the world’s epicenter of marine biodiversity

  • Hudson T. PinheiroEmail author
  • Bart Shepherd
  • Cristina Castillo
  • Rene A. Abesamis
  • Joshua M. Copus
  • Richard L. Pyle
  • Brian D. Greene
  • Richard R. Coleman
  • Robert K. Whitton
  • Emma Thillainath
  • Abner A. Bucol
  • Matthew Birt
  • Dave Catania
  • Mauritius V. Bell
  • Luiz A. Rocha


The Philippines is often highlighted as the global epicenter of marine biodiversity, yet surveys of reef-associated fishes in this region rarely extend beyond shallow habitats. Here, we improve the understanding of fish species diversity and distribution patterns in the Philippines by analyzing data from mesophotic coral ecosystems (MCEs; 30–150 m depth) obtained via mixed-gas rebreather diving and baited remote underwater video surveys. A total of 277 fish species from 50 families was documented, which includes thirteen newly discovered and undescribed species. There were 27 new records for the Philippines and 110 depth range extensions, indicating that many reef fishes have a broader geographic distribution and greater depth limits than previously reported. High taxonomic beta-diversity, mainly associated with family and genus turnover with depth, and significant effects of traits such as species body size, mobility and geographic range with maximum recorded depth, were observed. These results suggest that MCEs are characterized by unique assemblages with distinct ecological and biogeographic traits. A high proportion (60.5%) of the fish species are targeted by fishing, suggesting that Philippine MCEs are as vulnerable to overfishing as shallow reefs. Our findings support calls to expand conservation efforts beyond shallow reefs and draw attention to the need to explicitly include deep reefs in marine protected areas to help preserve the unique biodiversity of MCEs in the Philippines.


Mesophotic coral ecosystems Twilight zone Checklist Coral triangle Philippines Conservation 



This work was funded by the generous support of donors who endorsed the California Academy of Sciences’ Hope for Reefs Initiative, and through grants from the National Science Foundation to T. Gosliner, R. Mooi, G. Williams and L.A. Rocha (DEB 12576304), and Brian W. Bowen (OCE-15-58852), and a grant from the Seaver Institute to Brian W. Bowen and Richard L. Pyle. We also thank the Australian Research Council Center of Excellence for Coral Reef Studies at James Cook University, the Oceans Institute and School of Biological Sciences at University of Western Australia, G.R. Russ, A.C. Alcala and T. Langlois for support. We are grateful to many colleagues who helped in the field and with discussions: M. Bell, E. Jessup, M. Lane, N. Nazarian, T. Phelps, B. Bowen, C. Ka‘apu-Lyons, S. Longo. Hollis, Poseidon and Anilao Beach Club provided gear and logistical support. HTP thanks CNPq for his PhD fellowship (Ciência sem Fronteiras; GDE 202475/2011-5). Philippines research and collecting permits (GP-0072-13, GP-0077-14, and GP-0085-15) were provided by the Department of Agriculture-Bureau of Fisheries and Aquatic Resources. Additional permits were provided by Apo Island Protected Area Management Board. This is a collaborative research initiative with key Philippine partners including: former Secretary of Agriculture P. J. Alcala; former Philippine Consul General M. Paynor and the Consular staff in San Francisco; former BFAR Director A. G. Perez; BFAR colleagues, especially A. Vitug and L. Labe; and NFRDI colleagues especially, Acting Director D. Bayate and N. Romena.

Supplementary material

338_2019_1825_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)
338_2019_1825_MOESM2_ESM.pdf (126 kb)
Supplementary material 2 (PDF 125 kb)


  1. Abesamis RA, Langlois T, Birt M, Thillainath E, Bucol AA, Arceo HO, Russ GR (2018) Benthic habitat and fish assemblage structure from shallow to mesophotic depths in a storm-impacted marine protected area. Coral Reefs 37:81–97CrossRefGoogle Scholar
  2. Alcala A, Bucol A, Nillos-Kleiven P (2008) Directory of marine reserves in the Visayas, PhilippinesGoogle Scholar
  3. Alcala AC, Russ GR (2006) No-take marine reserves and reef fisheries management in the Philippines: a new people power revolution. Ambio 35:245–254CrossRefGoogle Scholar
  4. Allen G (2008) Conservation hotspots of biodiversity and endemism for Indo-Pacific coral reef fishes. Aquat Conserv Mar Freshw Ecosyst 18:541–556CrossRefGoogle Scholar
  5. Allen GR, Erdmann MV (2012) Reef fishes of the East Indies, vol I-III. Tropical Reef Research, PerthGoogle Scholar
  6. Allen GR, Werner TB (2002) Coral reef fish assessment in the ‘coral triangle’ of southeastern Asia. Environ Biol Fishes 65:209–214CrossRefGoogle Scholar
  7. Anderson WD, Greene BD, Rocha LA (2016) Grammatonotus brianne, a new callanthiid fish from Philippine waters, with short accounts of two other Grammatonotus from the Coral Triangle. Zootaxa 4173:289–295CrossRefGoogle Scholar
  8. Arango BG, Pinheiro HT, Rocha C, Greene BD, Pyle RL, Copus JM, Shepherd B, Rocha LA (2019) Three new species of Chromis (Teleostei, Pomacentridae) from mesophotic coral ecosystems of the Philippines. Zookeys 835:1–15CrossRefGoogle Scholar
  9. Baldwin CC, Tornabene L, Robertson DR (2018) Below the Mesophotic. Sci Rep 8:4920CrossRefGoogle Scholar
  10. Barwell LJ, Isaac NJB, Kunin WE (2015) Measuring β—diversity with species abundance data. J Anim Ecol 84:1112–1122CrossRefGoogle Scholar
  11. Baselga A, Orme CDL (2012) Betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812CrossRefGoogle Scholar
  12. Bejarano I, Appeldoorn RS, Nemeth M (2014) Fishes associated with mesophotic coral ecosystems in La Parguera, Puerto Rico. Coral Reefs 33:313–328CrossRefGoogle Scholar
  13. Bellwood DR, Meyer CP (2009) Searching for heat in a marine biodiversity hotspot. J Biogeogr 36:569–576CrossRefGoogle Scholar
  14. Bellwood DR, Wainwright PC (2002) The history and biogeography of fishes on Coral Reels. Coral Reef Fishes. Academic Press, San Diego, pp 5–32CrossRefGoogle Scholar
  15. 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
  16. Bowen BW, Rocha LA, Toonen RJ, Karl SA (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366CrossRefGoogle Scholar
  17. Cabral RB, Aliño PM, Balingit ACM, Alis CM, Arceo HO, Nanola CL Jr, Geronimo RC, Partners MSN (2014) The Philippine marine protected area (MPA) database. Philipp Sci Lett 7:300–308Google Scholar
  18. Carpenter KE, Niem VH. FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. FAO, RomeGoogle Scholar
  19. Carpenter KE, Springer VG (2005) The center of the center of marine shore fish biodiversity: the Philippine Islands. Environ Biol Fishes 72:467–480CrossRefGoogle Scholar
  20. Christensen RHB (2013) Package “Ordinal”: regression models for ordinal data. Denmark, CopenhagenGoogle Scholar
  21. Coleman RR, Copus JM, Coffey DM, Whitton RK, Bowen BW (2018) Shifting reef fish assemblages along a depth gradient in Pohnpei, Micronesia. PeerJ 6:e4650CrossRefGoogle Scholar
  22. Craig MT, Hastings PA (2007) A molecular phylogeny of the groupers of the subfamily Epinephelinae (Serranidae) with a revised classification of the Epinephelini. Ichthyol Res 54:1–17CrossRefGoogle Scholar
  23. Eschmeyer, Fong J (2018) Species by family/subfamily in the catalog of fishesGoogle Scholar
  24. Froese R, Pauly D (2018) Fishbase. World Wide Web electronic publication., version (06/2018)
  25. Fukunaga A, Kosaki RK, Wagner D (2017) Changes in mesophotic reef fish assemblages along depth and geographical gradients in the Northwestern Hawaiian Islands. Coral Reefs 36:785–790CrossRefGoogle Scholar
  26. Gaither MR, Rocha LA (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. J Biogeogr 40:1638–1648CrossRefGoogle Scholar
  27. Goetze JS, Langlois TJ, Egli DP, Harvey ES (2011) Evidence of artisanal fishing impacts and depth refuge in assemblages of Fijian reef fish. Coral Reefs 30:507–517CrossRefGoogle Scholar
  28. Herre AW (1953) Checklist of Philippine fishes. U.S. Printing Office. 119., Washington, DCGoogle Scholar
  29. 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
  30. Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep 5:12407CrossRefGoogle Scholar
  31. Honda K, Nakamura Y, Nakaoka M, Uy WH, Fortes MD (2013) Habitat use by fishes in coral reefs, seagrass beds and mangrove habitats in the Philippines. PLoS ONE 8:e65735CrossRefGoogle Scholar
  32. Horigue V, Pressey RL, Mills M, Brotánková J, Cabral R, Andréfouët S (2015) Benefits and challenges of scaling up expansion of marine protected area networks in the Verde Island Passage, Central Philippines. PLoS One 10:e0135789CrossRefGoogle Scholar
  33. IUCN (2017) The IUCN red list of threatened species.
  34. Joseph Quimpo TR, Cabaitan PC, Dionnie Olavides RD, Dumalagan EE, Munar J, Siringan FP (2018) Preliminary observations of macrobenthic invertebrates and megafauna communities in the upper mesophotic coral ecosystems in Apo Reef Natural Park, Philippines. Raffles Bull Zool 7600:1–11Google Scholar
  35. Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275CrossRefGoogle Scholar
  36. 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
  37. Koleff P, Gaston K, Lennon J (2003) Measuring beta diversity for presence–absence data. J Anim Ecol 72:367–382CrossRefGoogle Scholar
  38. Kulbicki M, Parravicini V, Bellwood DR, Arias-Gonzàlez E, Chabanet P, Floeter SR, Friedlander A, McPherson J, Myers RE, Vigliola L, Mouillot D (2013) Global biogeography of reef fishes: a hierarchical quantitative delineation of regions. PLoS ONE 8:e81847CrossRefGoogle Scholar
  39. Langlois TJ, Harvey ES, Fitzpatrick B, Meeuwig JJ, Shedrawi G, Watson DL (2010) Cost-efficient sampling of fish assemblages: comparison of baited video stations and diver video transects. Aquat Biol 9:155–168CrossRefGoogle Scholar
  40. Lavides MN, Molina EPV, De Rosa GE (2016) Patterns of coral-reef finfish species disappearances inferred from fishers’ knowledge in global epicentre of marine shorefish diversity. PLoS ONE 11:e0155752CrossRefGoogle Scholar
  41. Lindfield SJ, Harvey ES, Halford AR, McIlwain JL (2016) Mesophotic depths as refuge areas for fishery-targeted species on coral reefs. Coral Reefs 35:125–137CrossRefGoogle Scholar
  42. Lindfield SJ, McIlwain JL, Harvey ES (2014) Depth refuge and the impacts of SCUBA spearfishing on coral reef fishes. PLoS ONE 9:e92628CrossRefGoogle Scholar
  43. Loya Y, Eyal G, Treibitz T, Lesser MP, Appeldoorn R (2016) Theme section on mesophotic coral ecosystems: advances in knowledge and future perspectives. Coral Reefs 35:1–9CrossRefGoogle Scholar
  44. Luiz OJ, Madin JS, Robertson DR, Rocha LA, Wirtz P, Floeter SR (2012) Ecological traits influencing range expansion across large oceanic dispersal barriers: insights from tropical Atlantic reef fishes. Proc R Soc B Biol Sci 279:1033–1040CrossRefGoogle Scholar
  45. Luiz OJ, Woods RM, Madin EMP, Madin JS (2016) Predicting IUCN extinction risk categories for the world’s data deficient groupers (Teleostei: Epinephelidae). Conserv Lett 9:342–350CrossRefGoogle Scholar
  46. Maypa AP, White AT, Caňares E, Martinez R, Eisma-Osorio RL, Aliňo P, Apistar D (2012) Marine protected area management effectiveness: progress and lessons in the Philippines. Coast Manag 40:510–524CrossRefGoogle Scholar
  47. Mora C, Chittaro PM, Sale PF, Kritzer JP, Ludsin SA (2003) Patterns and processes in reef fish diversity. Nature 421:933–936CrossRefGoogle Scholar
  48. Motomura H, Alama UB, Muto N, Babaran RP, Ishikawa S (2017) Commercial and bycatch market fishes of Panay Island, Republic of the Philippines. The Kagoshima University Museum, Kagoshima, University of the Philippines Visayas, Iloilo, and Research Institute for Humanity and Nature, KyotoGoogle Scholar
  49. Nacorda HME, Dizon RM, Menez LAB, Nanola CL, Roa-Chio PBL, De Jesus DO, Hernandez HB, Quimpo FTR, Licuanan WRY, Alino PM, Villanoy CL (2017) Beneath 50 m of NW Pacific water: coral reefs on the Benham Bank Seamount off the Philippine Sea. J Environ Sci Manag 20:110–121Google Scholar
  50. Nañola CL, Aliño PM, Carpenter KE (2011) Exploitation-related reef fish species richness depletion in the epicenter of marine biodiversity. Environ Biol Fishes 90:405–420CrossRefGoogle Scholar
  51. Pinheiro HT, Goodbody-Gringley G, Jessup ME, Shepherd B, Chequer AD, Rocha LA (2016) Upper and lower mesophotic coral reef fish communities evaluated by underwater visual censuses in two Caribbean locations. Coral Reefs 35:139–151CrossRefGoogle Scholar
  52. Pinheiro HT, Mazzei E, Moura RL, Amado-Filho GM, Carvalho-Filho A, Braga AC, Costa PAS, Ferreira BP, Ferreira CEL, Floeter SR, Francini-Filho RB, Gasparini JL, Macieira RM, Martins AS, Olavo G, Pimentel CR, Rocha LA, Sazima I, Simon T, Teixeira JB, Xavier LB, Joyeux J-C (2015) Fish biodiversity of the Vitória-Trindade Seamount Chain, southwestern Atlantic: an updated database. PLoS ONE 10:e0118180CrossRefGoogle Scholar
  53. Pyle R (2000) Assessing undiscovered fish biodiversity on deep coral reefs using advanced self-contained diving technology. Mar Technol Soc J 34:82–91CrossRefGoogle Scholar
  54. Pyle RL, Boland R, Bolick H, Bowen BW, Bradley CJ, Kane C, Kosaki RK, Langston R, Longenecker K, Montgomery A, Parrish FA, Popp BN, Rooney J, Smith CM, Wagner D, Spalding HL (2016) A comprehensive investigation of mesophotic coral ecosystems in the Hawaiian Archipelago. PeerJ 4:e2475CrossRefGoogle Scholar
  55. Pyle RL, Kosaki RK (2016) Prognathodes basabei, a new species of butterflyfish (Perciformes, Chaetodontidae) from the Hawaiian Archipelago. Zookeys 614:137–152CrossRefGoogle Scholar
  56. Ramos DAE, Aragones LV, Rollon RN (2015) Linking integrity of coastal habitats and fisheries yield in the Manta lip Reef System. Ocean Coast Manag 111:62–71CrossRefGoogle Scholar
  57. Randall JE (1998) Zoogeography of shore fishes of the indo-pacific region. Zool Stud 37:227–268Google Scholar
  58. Roberts CM, Mcclean CJ, Veron JEN, 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 80(295):1280–1284CrossRefGoogle Scholar
  59. Rocha LA, Pinheiro HT, Shepherd B, Papastamatiou YP, Luiz OJ, Pyle RL, Bongaerts P (2018) Mesophotic coral ecosystems are threatened and ecologically distinct from shallow water reefs. Science 80(361):281–284CrossRefGoogle Scholar
  60. Rocha LA, Pinheiro HT, Wandell M, Rocha CR, Shepherd B (2017) Roa rumsfeldi, a new butterflyfish (Teleostei, Chaetodontidae) from mesophotic coral ecosystems of the Philippines. Zookeys 709:127–134CrossRefGoogle Scholar
  61. Rosa MR, Alves AC, Medeiros DV, Coni EOC, Ferreira CM, Ferreira BP, de Souza Rosa R, Amado-Filho GM, Pereira-Filho GH, de Moura RL, Thompson FL, Sumida PYG, Francini-Filho RB (2016) Mesophotic reef fish assemblages of the remote St. Peter and St. Pauls Archipelago, Mid-Atlantic Ridge, Brazil. Coral Reefs 35:113–123CrossRefGoogle Scholar
  62. Russ GR, Alcala AC (1999) Management histories of Sumilon and Apo Marine Reserves, Philippines, and their influence on national marine resource policy. Coral Reefs 18:307–319CrossRefGoogle Scholar
  63. Russ GR, Miller KI, Rizzari JR, Alcala AC (2015) Long-term no-take marine reserve and benthic habitat effects on coral reef fishes. Mar Ecol Prog Ser 529:233–248CrossRefGoogle Scholar
  64. Sanciangco JC, Carpenter KE, Etnoyer PJ, Moretzsohn F (2013) Habitat availability and heterogeneity and the Indo-Pacific warm pool as predictors of marine species richness in the tropical Indo-Pacific. PLoS One 8:e56245CrossRefGoogle Scholar
  65. Semmler RF, Hoot WC, Reaka ML (2016) Are mesophotic coral ecosystems distinct communities and can they serve as refugia for shallow reefs? Coral Reefs 36:433–444CrossRefGoogle Scholar
  66. Shepherd B, Pinheiro HT, Rocha LA (2018) Ephemeral aggregation of the benthic ctenophore Lyrocteis imperatoris on a mesophotic coral ecosystem in the Philippines. Bull Mar Sci 94:101–102CrossRefGoogle Scholar
  67. Simon T, Pinheiro HT, Moura RL, Carvalho-Filho A, Rocha LA, Martins AS, Mazzei EF, Francini-Filho RB, Amado-Filho GM, Joyeux J-C (2016) Mesophotic fishes of the Abrolhos Shelf, the largest reef ecosystem in the South Atlantic. J Fish Biol 89:990–1001CrossRefGoogle Scholar
  68. Slattery M, Lesser MP, Brazeau D, Stokes MD, Leichter JJ (2011) Connectivity and stability of mesophotic coral reefs. J Exp Mar Bio Ecol 408:32–41CrossRefGoogle Scholar
  69. Smith DG, Williams JT (1999) The great Albatross Philippine expedition and its fishes. Mar Fish Rev 61:31–41Google Scholar
  70. Tornabene L, Van Tassell JL, Robertson DR, Baldwin CC (2016) Repeated invasions into the twilight zone: evolutionary origins of a novel assemblage of fishes from deep Caribbean reefs. Mol Ecol 25:3662–3682CrossRefGoogle Scholar
  71. Turner JA, Babcock RC, Hovey R, Kendrick GA (2017) Deep thinking: a systematic review of mesophotic coral ecosystems. ICES J Mar Sci 74:2309–2320CrossRefGoogle Scholar
  72. 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
  73. Weeks R, Russ GR, Alcala AC, White AT (2010) Effectiveness of marine protected areas in the Philippines for biodiversity conservation. Conserv Biol 24:531–540CrossRefGoogle Scholar
  74. Westneat MW, Alfaro ME (2005) Phylogenetic relationships and evolutionary history of the reef fish family Labridae. Mol Phylogenet Evol 36:370–390CrossRefGoogle Scholar
  75. White AT, Gomez E, Alcala AC, Russ G (2007) Evolution and lessons from fisheries and coastal management in the Philippines. In: McClanahan TR, Castilla JC (eds) Fisheries management: progress towards sustainability. Blackwell Publishing Ltd, Chapter 5Google Scholar
  76. White AT, Vogt HP, Arin T (2000) Philippine Coral Reefs under threat: the economic losses caused by reef destruction. Mar Pollut Bull 40:598–605CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.California Academy of SciencesSan FranciscoUSA
  2. 2.Silliman University–Angelo King Center for Research and Environmental ManagementDumaguetePhilippines
  3. 3.Hawai’i Institute of Marine BiologyKaneoheUSA
  4. 4.Department of BiologyUniversity of Hawai‘i at MānoaHonoluluUSA
  5. 5.Bernice P. Bishop MuseumHonoluluUSA
  6. 6.The UWA Oceans Institute and School of Biological SciencesThe University of Western AustraliaCrawleyAustralia
  7. 7.Australian Institute of Marine ScienceCrawleyAustralia

Personalised recommendations