Abstract
Mesophotic reefs, defined as reefs between 30 m and 150 m, have been less investigated than their shallower counterparts. Yet, more protected from human activities and bleaching events, they could be refuge zones allowing the resilience of shallow reefs. However, it is currently unknown if their role as refugia for species diversity also extends to functional diversity and thus potentially ecosystem functioning. Using an extensive video field surveys from Mayotte Island in the Western Indian Ocean, we analyzed how taxonomic diversity and functional diversity of coral reef fishes changed along a depth gradient from 10 to 100 m. We found that shallow and mesophotic reefs host different species, but that these dissimilar assemblages share similar richness combinations of traits values. However, when accounting for biomass of species, it appears that functional structure of assemblages differs along the depth gradient, with, for instance, herbivorous fishes being very scarce in deep reefs while large-bodied carnivorous are more abundant. Therefore, surveys of mesophotic fishes should assess not only species, but also trait composition, abundance and biomass. Overall, our results support the claim that extending marine protected areas to mesophotic reefs is required to maximize the protection of both species and functional diversities to eventually maintain coral reef ecosystem functioning and associated services across the broader seascape.
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References
Allgeier JE, Valdivia A, Cox C, Layman CA (2016) Fishing down nutrients on coral reefs. Nat Commun 7:12461
Assis J, Coelho NC, Lamy T, Valero M, Alberto F, Serrão EÁ (2016) Deep reefs are climatic refugia for genetic diversity of marine forests. J Biogeogr 43:833–844
Audzijonyte A, Pecl GT (2018) Deep impact of fisheries. Nat Ecol Evol 2:1348–1349
Bacheler NM, Shertzer KW, Runde BJ, Rudershausen PJ, Buckel JA (2021) Environmental conditions, diel period, and fish size influence the horizontal and vertical movements of red snapper. Sci Rep 11:1–16
Bellwood DR, Streit RP, Brandl SJ, Tebbett SB (2019) The meaning of the term ‘function’ in ecology: a coral reef perspective. Funct Ecol 33:948–961
Bivand RS, Pebesma EJ, Gómez-Rubio V, Pebesma EJ (2008) Applied spatial data analysis with R. Springer
Bongaerts P, Ridgway T, Sampayo E, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327
Bosch NE, Monk J, Goetze J, Wilson S, Babcock RC, Barrett N, Langlois TJ (2022a) Effects of human footprint and biophysical factors on the body-size structure of fished marine species. Conserv Biol 36(2):e13807
Bosch NE, McLean M, Zarco-Perello S, Bennett S, Stuart-Smith RD, Vergés A, Wernberg T (2022b) Persistent thermally driven shift in the functional trait structure of herbivorous fishes: evidence of top-down control on the rebound potential of temperate seaweed forests? Glob Change Biol 28:2296–2311
Brandl SJ, Rasher DB, Côté IM, Casey JM, Darling ES, Lefcheck JS, Duffy JE (2019) Coral reef ecosystem functioning: eight core processes and the role of biodiversity. Front Ecol Environ 17:445–454
Brazo A, Marques R, Zimmermann M, Aspillaga E, Hereu B, Saragoni G, Mercière A, Crec’Hriou R, Mercader M, Verdoit-Jarraya M, (2021) Seasonal influence on the bathymetric distribution of an endangered fish within a marine protected area. Sci Rep 11:1–16
Breheny P, Burchett W (2017) Visualization of regression models using visreg. R J 9:56
Brown SC, Wigley TM, Otto-Bliesner BL, Rahbek C, Fordham DA (2020) Persistent Quaternary climate refugia are hospices for biodiversity in the Anthropocene. Nat Clim Chang 10:244–248
Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci 105:16201–16206
Cabral RB, Bradley D, Mayorga J, Goodell W, Friedlander AM, Sala E, Costello C, Gaines SD (2020) A global network of marine protected areas for food. Proc Natl Acad Sci 117:28134–28139
Carrington VG, Papa Y, Beese CM, Hall J, Covain R, Horn P, Ladds MA, Rogers A, Yeo D (2021) How functionally diverse are fish in the deep? A comparison of fish communities in deep and shallow-water systems. Divers Distrib 27(7):1208
Chao A, Chiu CH, Villéger S, Sun IF, Thorn S, Lin YC, Chiang JM, Sherwin WB (2019) An attribute-diversity approach to functional diversity, functional beta diversity, and related (dis) similarity measures. Ecol Monogr 89:e01343
Cinner JE, Huchery C, MacNeil MA, Graham NA, McClanahan TR, Maina J, Maire E, Kittinger JN, Hicks CC, Mora C (2016) Bright spots among the world’s coral reefs. Nature 535:416–419
Cinner JE, Zamborain-Mason J, Gurney GG, Graham NA, MacNeil MA, Hoey AS, Mouillot D (2020) Meeting fisheries, ecosystem function, and biodiversity goals in a human-dominated world. Science 368(6488):307–311
Coleman RR, Copus JM, Coffey DM, Whitton RK, Bowen BW (2018) Shifting reef fish assemblages along a depth gradient in Pohnpei. Micronesia Peerj 6:e4650
Costello MJ, Chaudhary C (2017) Marine biodiversity, biogeography, deep-sea gradients, and conservation. Curr Biol 27:R511–R527
Cure K, Currey-Randall L, Galaiduk R, Radford B, Wakeford M, Heyward A (2021) Depth gradients in abundance and functional roles suggest limited depth refuges for herbivorous fishes. Coral Reefs 40:365–379
Doherty B, Herfaut J, Le Manach F, Harper S, Zeller D (2015) Reconstructing domestic marine fisheries in Mayotte from 1950–2010. Fisheries Catch Reconstructions in the Western Indian Ocean, eds F Le Manach and D Pauly (Vancouver: University of British Columbia):53–65
Eddy TD, Lam VW, Reygondeau G, Cisneros-Montemayor AM, Greer K, Palomares MLD, Bruno JF, Ota Y, Cheung WW (2021) Global decline in capacity of coral reefs to provide ecosystem services. One Earth 4:1278–1285
Edgar GJ, Cooper A, Baker SC, Barker W, Barrett NS, Becerro MA, Bates AE, Brock D, Ceccarelli DM, Clausius E (2020) Reef Life Survey: establishing the ecological basis for conservation of shallow marine life. Biol Cons 252:1–14
Ellis D (1995) Evaluation of video camera technique for indexing abundances of juvenile pink snapper pristipomoides filamentosus, and other Hawaiian insular shelf fishes. Fish Bull 93:67–77
Eyal G, Laverick JH, Bongaerts P, Levy O, Pandolfi JM (2021) Mesophotic coral ecosystems of the great barrier reef are understudied and underexplored. Front Mar Sci 8:83
Ferrier S, Manion G, Elith J, Richardson K (2007) Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers Distrib 13:252–264
Genevier LG, Jamil T, Raitsos DE, Krokos G, Hoteit I (2019) Marine heatwaves reveal coral reef zones susceptible to bleaching in the Red Sea. Glob Change Biol 25:2338–2351
Goetze JS, Wilson S, Radford B, Fisher R, Langlois TJ, Monk J, Knott NA, Malcolm H, Currey-Randall LM, Ierodiaconou D (2021) Increased connectivity and depth improve the effectiveness of marine reserves. Glob Change Biol 27(15):3432
Gower JC, Legendre P (1986) Metric and Euclidean properties of dissimilarity coefficients. J Classif 3:5–48
Hijmans RJ, Van Etten J, Cheng J, Mattiuzzi M, Sumner M, Greenberg JA, Lamigueiro OP, Bevan A, Racine EB, Shortridge A (2015) Package ‘raster’. R package 734
Hollarsmith JA, Winquist R-O, T, Velasco-Lozano M, DuBois K, Reyes-Bonilla H, Neumann KC, Grosholz ED, (2020) Habitats and fish communities at mesophotic depths in the Mexican Pacific. J Biogeogr 47:1552–1563
Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637
Jankowski M, Graham N, Jones G (2015) Depth gradients in diversity, distribution and habitat specialisation in coral reef fishes: implications for the depth-refuge hypothesis. Mar Ecol Prog Ser 540:203–215
Kahng S, Copus JM, Wagner D (2017) Mesophotic coral ecosystems. Marine animal forests: the ecology of benthic biodiversity hotspots:185-206
Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AG, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21:393–404
Langlois T, Goetze J, Bond T, Monk J, Abesamis RA, Asher J, Harvey ES (2020) A field and video annotation guide for baited remote underwater stereo-video surveys of demersal fish assemblages. Method Ecol Evol 11:1401–1409
Lefcheck JS, Innes-Gold AA, Brandl SJ, Steneck RS, Torres RE, Rasher DB (2019) Tropical fish diversity enhances coral reef functioning across multiple scales. Sci Adv 5(3):eavve6420
Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8
Letessier TB, Juhel J-B, Vigliola L, Meeuwig JJ (2015) Low-cost small action cameras in stereo generates accurate underwater measurements of fish. J Exp Mar Biol Ecol 466:120–126
Lindfield SJ, Harvey ES, Halford AR, McIlwain JL (2016) Mesophotic depths as refuge areas for fishery-targeted species on coral reefs. Coral Reefs 35:125–137
Loiseau N, Legras G, Kulbicki M, Mérigot B, Harmelin-Vivien M, Mazouni N, Galzin R, Gaertner J-C (2017) Multi-component β-diversity approach reveals conservation dilemma between species and functions of coral reef fishes. J Biogeogr 44:537–547
MacNeil MA, Graham NA, Cinner JE, Wilson SK, Williams ID, Maina J, Newman S, Friedlander AM, Jupiter S, Polunin NV (2015) Recovery potential of the world’s coral reef fishes. Nature 520:341–344
Magneville C, Loiseau N, Albouy C, Casajus N, Claverie T, Escalas A, Leprieur F, Maire E, Mouillot D, Villéger S (2022) mFD: an R package to compute and illustrate the multiple facets of functional diversity. Ecography. https://doi.org/10.1111/ecog.05904
Mallet D, Pelletier D (2014) Underwater video techniques for observing coastal marine biodiversity: a review of sixty years of publications (1952–2012). Fish Res 154:44–62
Manion G, Lisk M, Ferrier S, Nieto-Lugilde D, Fitzpatrick M (2016) gdm: functions for generalized dissimilarity modeling. Rpackage version 1
Marie C-V, Breton D, Crouzet M (2018) More than half of all adults living in Mayotte were born elsewhere. Popul Soc 10:1–4
Maxwell SL, Cazalis V, Dudley N, Hoffmann M, Rodrigues AS, Stolton S, Visconti P, Woodley S, Kingston N, Lewis E (2020) Area-based conservation in the twenty-first century. Nature 586:217–227
McLean M et al (2021) Trait similarity in reef fish faunas across the world’s oceans. Proc Natl Acad Sci 118(12):e2012318118
Medeiros APM, Ferreira BP, Alvarado F, Betancur RR, Soares MO, Santos BA (2021) Deep reefs are not refugium for shallow-water fish communities in the southwestern Atlantic. Ecol Evol 11:4413–4427
Morais RA, Bellwood DR (2020) Principles for estimating fish productivity on coral reefs. Coral Reefs 39:1221–1231
Mouillot D, Villéger S, Parravicini V, Kulbicki M, Arias-González JE, Bender M, Chabanet P, Floeter SR, Friedlander A, Vigliola L (2014) Functional over-redundancy and high functional vulnerability in global fish faunas on tropical reefs. Proc Natl Acad Sci 111:13757–13762
Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J Biogeogr 26:867–878
Neuswanger JR, Wipfli MS, Rosenberger AE, Hughes NF (2016) Measuring fish and their physical habitats: versatile 2D and 3D video techniques with user-friendly software. Can J Fish Aquat Sci 73:1861–1873
Oliver EC, Donat MG, Burrows MT, Moore PJ, Smale DA, Alexander LV, Benthuysen JA, Feng M, Gupta AS, Hobday AJ, Holbrook NJ, Perkins-Kirkpatrick SE, Scannell HA, Straub SC, Wernberg T (2018) Longer and more frequent marine heatwaves over the past century. Nat Commun 9(1):1–12
Olivier D, Loiseau N, Petatán-Ramírez D, Millán OT, Suárez-Castillo AN, Torre J, Munguia-Vega A, Reyes-Bonilla H (2018) Functional-biogeography of the reef fishes of the islands of the Gulf of California: integrating functional divergence into marine conservation. Global Ecol Conserv 16:e00506
Ordonez A, Svenning JC (2015) Geographic patterns in functional diversity deficits are linked to glacial-interglacial climate stability and accessibility. Glob Ecol Biogeogr 24:826–837
Pebesma E, Heuvelink G (2016) Spatio-temporal interpolation using gstat. RFID J 8:204–218
Pellissier L, Leprieur F, Parravicini V, Cowman PF, Kulbicki M, Litsios G, Olsen SM, Wisz MS, Bellwood DR, Mouillot D (2014) Quaternary coral reef refugia preserved fish diversity. Science 344:1016–1019
Piacenza SE, Barner AK, Benkwitt CE, Boersma KS, Cerny-Chipman EB, Ingeman KE, Kindinger TL, Lee JD, Lindsley AJ, Reimer JN (2015) Patterns and variation in benthic biodiversity in a large marine ecosystem. PLoS ONE 10:e0135135
Price A, Keeling M, O’callaghan C (1999) Ocean-scale patterns of ‘biodiversity’of Atlantic asteroids determined from taxonomic distinctness and other measures. Biol J Lin Soc 66:187–203
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 361:281–284
Sala E, Mayorga J, Bradley D, Cabral RB, Atwood TB, Auber A, Cheung W, Costello C, Ferretti F, Friedlander AM (2021) Protecting the global ocean for biodiversity, food and climate. Nature 592:397–402
Sale PF (2013) The ecology of fishes on coral reefs. Elsevier
Spalding M, Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. Univ of California Press
Stefanoudis PV, Gress E, Pitt JM, Smith SR, Kincaid T, Rivers M, Andradi-Brown DA, Rowlands G, Woodall LC, Rogers AD (2019) Depth-dependent structuring of reef fish assemblages from the shallows to the rariphotic zone. Front Mar Sci 6:307
Venegas RM, Oliver T, Liu G, Heron SF, Clark SJ, Pomeroy N, Young C, Eakin CM, Brainard RE (2019) The rarity of depth refugia from coral bleaching heat stress in the western and central Pacific Islands. Sci Rep 9:1–12
Villéger S, Brosse S, Mouchet M, Mouillot D, Vanni MJ (2017) Functional ecology of fish: current approaches and future challenges. Aquat Sci 79:783–801
Weijerman M, Grüss A, Dove D, Asher J, Williams ID, Kelley C, Drazen JC (2019) Shining a light on the composition and distribution patterns of mesophotic and subphotic fish communities in Hawai ‘i. Mar Ecol Prog Ser 630:161–182
Wickel J, Jamon A, Pinault M, Durville P, Chabanet P (2014) Composition et structure des peuplements ichtyologiques marins de l’île de Mayotte (sud-ouest de l’océan Indien). Cybium: Revue Internationale d’Ichtyologie 38:179–203
Acknowledgements
This research was funded by the CUFR of Mayotte, by the second Research Consortium Iles eparse 2017–2020 (project MAPOR), by the French Foundation for Research on Biodiversity and its partners (FRB-www.fondationbiodiversite.fr) and by ANR (The French National Research Agency) under the “investissement d’avenir” program with the reference ANR-16-IDEX-0006. The authors thank Priscilla Dupont and Julien Wikel for helping with fish ID on videos and Yann Mercky and Elliott Sucre for their help on field operation.
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Loiseau, N., Villéger, S., Le Bozec, C. et al. Mesophotic reefs are not refugia for neither taxonomic nor functional diversity of reef fishes. Coral Reefs 42, 63–75 (2023). https://doi.org/10.1007/s00338-022-02311-1
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DOI: https://doi.org/10.1007/s00338-022-02311-1