coastal habitat; fish juvenile; fish post-larvae; marine biodiversity; molecular tool
Abstract :
[en] Madagascar is a marine biodiversity hotspot. A recent checklist recorded 1689 marine or transitional water fish species, 2.5% being endemic. To date, studies in this country were mostly focused on adult fishes using morphological-based identification. The early life stages of fishes remain largely understudied. The present work aimed to improve knowledge of fish biodiversity in Madagascar by focusing on post-larval reef fishes and settled juveniles in seagrass meadows of southwest Madagascar by using either species identification keys or DNA barcoding. Up to 119,500 individuals were collected, and 1096 individuals were successfully barcoded. We identified 387 species—85 through their morphology (with 58 unsuccessfully sequenced) and 302 by using CO1 barcoding corresponding to 302 barcode index numbers (BINs). This study added 27 new BINs for the BOLD database, 120 new for Madagascar, but only 159 were assigned a precise species name. By referring to the updated checklist of Madagascar fishes, 10 new species were detected for Madagascar. This number will probably increase when all the barcoded specimens become assigned to precise species names. These preliminary findings stress our poor knowledge of marine fish biodiversity in Madagascar and demonstrate the relevance of DNA barcoding in improving this knowledge.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Jaonalison, Henitsoa ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS) ; Institut Halieutique et des Sciences Marines, Université de Toliara, Toliara, Madagascar
Durand, Jean-Dominique; MARBEC, Université Montpellier, IRD, CNRS, Ifremer, Montpellier, France
Mahafina, Jamal; Institut Halieutique et des Sciences Marines, Université de Toliara, Toliara, Madagascar
Valade, Pierre; Organisme Consultant en Environnement Aquatique, Ravine des Cabris, France
Collet, Adeline; Organisme Consultant en Environnement Aquatique, Ravine des Cabris, France
Cerqueira, Frédérique; ISEM, CNRS, University of Montpellier, IRD, EPHE, Montpellier, France
Ponton, Dominique ; ENTROPIE, IRD, Université de La Réunion, CNRS, Université de la Nouvelle-Calédonie, Ifremer, c/o Institut Halieutique et des Sciences Marines, Université de Toliara, Toliara, Madagascar
Language :
English
Title :
Application of DNA Barcoding for Monitoring Madagascar Fish Biodiversity in Coastal Areas
CEPF - Critical Ecosystem Partnership Fund Rufford Foundation WIOMSA - Western Indian Ocean Marine Science Association
Funding text :
The research was funded by the Critical Ecosystem Partnership Fund under Grant MG 66341; the Rufford foundation under Grant 2ac29a-1; Western Indian Ocean Marine Science As-sociation (WIOMSA) under MARG II Contract 1/2016; the French National Research Institute for Sustainable Development under Grant JEAI-ACOM/IH.SM/IRD, and the European Union under grant POE 2.10 POCT FED–FEDER ‘Biodiversité de l’Océan Indien’.Funding: The research was funded by the Critical Ecosystem Partnership Fund under Grant MG 66341; the Rufford foundation under Grant 2ac29a-1; Western Indian Ocean Marine Science Association (WIOMSA) under MARG II Contract 1/2016; the French National Research Institute for Sustainable Development under Grant JEAI-ACOM/IH.SM/IRD, and the European Union under grant POE 2.10 POCT FED–FEDER ‘Biodiversité de l’Océan Indien’.
MEF. Fourth National Report on Biological Diversity Convention Madagascar; Ministry of Environment and Forests: Antananarivo, Madagascar, 2009; p. 144.
Fricke, R.; Mahafina, J.; Behivoke, F.; Jaonalison, H.; Léopold, M.; Ponton, D. Annotated Checklist of the Fishes of Madagascar, Southwestern Indian Ocean, with 158 New Records. FishTaxa 2018, 3, 432.
Collet, A.; Durand, J.-D.; Desmarais, E.; Cerqueira, F.; Cantinelli, T.; Valade, P.; Ponton, D. DNA Barcoding Post-Larvae Can Improve the Knowledge about Fish Biodiversity: An Example from La Reunion, SW Indian Ocean. Mitochondrial DNA Part A 2018, 29, 905–918. [CrossRef] [PubMed]
Leis, J.M.; Carson-Ewart, B.M. The Larvae of Indo-Pacific Coastal Fishes: An Identification Guide to Marine Fish Larvae, 2nd ed.; Leiden; Brill: Boston, FL, USA, 2004; ISBN 978-90-04-11577-4.
Maamaatuaiahutapu, M.; Remoissenet, G.; Galzin, R. Guide d’identification Des Larves de Poissons Récifauxde Polynésie Française; Coral Reef Initiative for the South Pacific; Téthys: Nouméa, New Calédonie, 2006; 108p.
Juncker, M. Young Coral Reef Fish of Wallis and the Central Pacific: Identification Guide; Wallis and Futuna-Environment: Noumea, New Caledonia, 2007; 170p.
Frantine-Silva, W.; Sofia, S.H.; Orsi, M.L.; Almeida, F.S. DNA Barcoding of Freshwater Ichthyoplankton in the Neotropics as a Tool for Ecological Monitoring. Mol. Ecol. Resour. 2015, 15, 1226–1237. [CrossRef] [PubMed]
Brodeur, R.; Peterson, W.; Auth, T.; Soulen, H.; Parnel, M.; Emerson, A. Abundance and Diversity of Coastal Fish Larvae as Indicators of Recent Changes in Ocean and Climate Conditions in the Oregon Upwelling Zone. Mar. Ecol. Prog. Ser. 2008, 366, 187–202. [CrossRef]
Carassou, L.; Ponton, D.; Mellin, C.; Galzin, R. Predicting the Structure of Larval Fish Assemblages by a Hierarchical Classification of Meteorological and Water Column Forcing Factors. Coral Reefs 2008, 27, 867–880. [CrossRef]
Mahafina, J. Perception et Comportement Des Pêcheurs Pour Une Gestion Durable de La Biodiversité et de La Pêcherie Récifale Du Sud-Ouest de Madagascar. Ph.D. Thesis, Université de La Réunion et Université de Toliara, Toliara, Madagascar, 2011.
Jaonalison, H.; Mahafina, J.; Ponton, D. Fish Post-Larvae Assemblages at Two Contrasted Coral Reef Habitats in Southwest Madagascar. Reg. Stud. Mar. Sci. 2016, 6, 62–74. [CrossRef]
Chen, L.-C.; Lan, K.-W.; Chang, Y.; Chen, W.-Y. Summer Assemblages and Biodiversity of Larval Fish Associated with Hydrogra-phy in the Northern South China Sea. Mar. Coast. Fish. 2018, 10, 467–480. [CrossRef]
Grande, H.; Rezende, S.d.M.; Simon, T.E.; Félix-Hackradt, F.C.; García-Charton, J.A.; Maida, M.; Gaspar, A.L.B.; Francini-Filho, R.B.; Fredou, T.; Ferreira, B.P. Diversity of Settlement-stage Reef Fishes Captured by Light-trap in a Tropical South-west Atlantic Ocean Coastal Reef System. J. Fish Biol. 2018, 94, 210–222. [CrossRef]
Pegg, G.G.; Sinclair, B.; Briskey, L.; Aspden, W.J. MtDNA Barcode Identification of Fish Larvae in the Southern Great Barrier Reef—Australia. Sci. Mar. 2006, 70, 7–12. [CrossRef]
Trivedi, S.; Aloufi, A.A.; Ansari, A.A.; Ghosh, S.K. Role of DNA Barcoding in Marine Biodiversity Assessment and Conservation: An Update. Saudi J. Biol. Sci. 2016, 23, 161–171. [CrossRef]
Ko, H.-L.; Wang, Y.-T.; Chiu, T.-S.; Lee, M.-A.; Leu, M.-Y.; Chang, K.-Z.; Chen, W.-Y.; Shao, K.-T. Evaluating the Accuracy of Morphological Identification of Larval Fishes by Applying DNA Barcoding. PLoS ONE 2013, 8, e53451. [CrossRef] [PubMed]
Meredith, C.; Hoffman, J.; Trebitz, A.; Peterson, G.; Lietz, J.; Hatzenbuhler, C.; Pilgrim, E.; Okum, S.; Martinson, J. Development of DNA-Based Identification Methods to Track the Species Composition of Fish Larvae within Nearshore Areas of the Great Lakes; Minnesota Chapter of the American Fisheries Society: St. Cloud, MN, USA, 2017.
Leis, J.M. Taxonomy and Systematics of Larval Indo-Pacific Fishes: A Review of Progress since 1981. Ichthyol. Res. 2015, 62, 9–28. [CrossRef]
Bruggemann, J.H.; Rodier, M.; Guillaume, M.M.M.; Andréfouët, S.; Arfi, R.; Cinner, J.E.; Pichon, M.; Ramahatratra, F.; Rasoama-nendrika, F.; Zinke, J.; et al. Wicked Social-Ecological Problems Forcing Unprecedented Change on the Latitudinal Margins of Coral Reefs: The Case of Southwest Madagascar. Ecol. Soc. 2012, 17, 47. [CrossRef]
Ranaivomanana, L.N.J. Identification Des Conditions d’appropriation de La Gestion Durable Des Ressources Naturelles et Des Écosystèmes: Cas Du Grand Récif de Toliara. Ph.D. Thesis, Institut Halieutique et des Sciences Marines (IH.SM) de l’Université de Toliara, Toliara, Madagascar, 2006.
Dufour, V. Colonisation Des Recifs Coralliens Par Les Larves de Poissons. Ph.D. Thesis, Université Pierre & Marie Curie, Paris, France, 1992.
Marchetti, M.P.; Esteban, E.; Limm, M.; Kurth, R. Evaluating Aspects of Larval Light Trap Bias and Specificity in the Northern Sacramento River System: Do Size and Color Matter? Am. Fish. Soc. Symp. 2004, 39, 269–279.
Lindquist, D.C.; Shaw, R.F. Effects of Current Speed and Turbidity on Stationary Light-Trap Catches of Larval and Juvenile FIshes. Fish. Bull. 2005, 103, 438–444.
Wilson, D. Patterns of Replenishment of Coral-Reef Fishes in the Nearshore Waters of the San Blas Archipelago, Caribbean Panama. Mar. Biol. 2001, 139, 735–753. [CrossRef]
Anderson, T.W.; Bartels, C.T.; Hixon, M.A.; Bartels, E.; Carr, M.H.; Shenker, J.M. Current Velocity and Catch Efficiency in Sampling Settlement-Stage Larvae of Coral-Reef Fishes. Fish. Bull. 2002, 100, 404–413.
Laroche, J.; Ramananarivo, N. A Preliminary Survey of the Artisanal Fishery on Coral Reefs of the Tulear Region (Southwest Madagascar). Coral Reefs 1995, 14, 193–200. [CrossRef]
Raharinaivo, L.R.; Jaonalison, H.; Mahafina, J.; Ponton, D. How to Efficiently Determine the Size at Maturity of Small-sized Tropical Fishes: A Case Study Based on 144 Species Identified via DNA Barcoding from Southwestern Madagascar. J. Appl. Ichthyol. 2020, 36, 402–413. [CrossRef]
Bauchot, M.L.; Bianchi, G. Fiches FAO d’identification Des Especes Pour Les Besoins de La Peche. Guide Des Poissons Commerciaux de Madagascar (Especes Marines et d’eaux Saumatres), Avec Le Support Du Programme Des Nations Unies Pour Le Developpement (Projet RAF/79/065); FAO: Rome, Italy, 1984; 135p.
Collet, A.; Bosc, P.; Pothin, K.; Chabanet, P. Guide d’identification Des Post-Larves de Poissons Des Récifs Coralliens; ARDA et OCEA Consult’: La Réunion, France, 2013; 176p.
Werner, F.; Fröndt, R. Automated Purification of Genomic DNA from Tissue with the Macherey-Nagel NucleoMag®Tissue Kit on the EpMotion® 5075. Appl. Note 2015, 365, 1–7.
Ward, R.D.; Zemlak, T.S.; Innes, B.H.; Last, P.R.; Hebert, P.D.N. DNA Barcoding Australia’s Fish Species. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360, 1847–1857. [CrossRef] [PubMed]
Ratnasingham, S.; Hebert, P.D.N. A DNA-Based Registry for All Animal Species: The Barcode Index Number (BIN) System. PLoS ONE 2013, 8, e66213. [CrossRef] [PubMed]
R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2018.
Oksanen, J.; Blanchet, F.G.; Friendly, M.; Kindt, R.; Legendre, P.; McGlinn, D.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; et al. Vegan: Community Ecology Package. 2019. Available online: https://www.scirp.org/(S(351jmbntvnsjt1aadkposzje))/reference/ReferencesPapers.aspx?ReferenceID=1778707 (accessed on 12 October 2021).
Poulin, R. Comparison of Three Estimators of Species Richness in Parasite Component Communities. J. Parasitol. 1998, 84, 485–490. [CrossRef] [PubMed]
Meredith, M. Quick and Dirty Estimates for Wildlife Populations. 2019. Available online: http://www.r-project.org/(accessed on 12 October 2021).
Smith, E.P.; Van Belle, G. Nonparametric Estimation of Species Richness. Biometrics 1984, 40, 119–129. [CrossRef]
Pinheiro, H.T.; Rocha, L.A.; Macieira, R.M.; Carvalho-Filho, A.; Anderson, A.B.; Bender, M.G.; Di Dario, F.; Ferreira, C.E.L.; Figueiredo-Filho, J.; Francini-Filho, R.; et al. South-Western Atlantic Reef Fishes: Zoogeographical Patterns and Ecological Drivers Reveal a Secondary Biodiversity Centre in the Atlantic Ocean. Divers. Distrib. 2018, 24, 951–965. [CrossRef]
Steinke, D.; Connell, A.D.; Hebert, P.D.N. Linking Adults and Immatures of South African Marine Fishes. Genome 2016, 59, 959–967. [CrossRef]
Reid, K.; Crochelet, E.; Bloomer, P.; Hoareau, T.B. Investigating the Origin of Vagrant Dusky Groupers, Epinephelus Marginatus (Lowe, 1834), in Coastal Waters of Réunion Island. Mol. Phylogenet. Evol. 2016, 103, 98–103. [CrossRef]
Weigt, L.A.; Baldwin, C.C.; Driskell, A.; Smith, D.G.; Ormos, A.; Reyier, E.A. Using DNA Barcoding to Assess Caribbean Reef Fish Biodiversity: Expanding Taxonomic and Geographic Coverage. PLoS ONE 2012, 7, e41059. [CrossRef]
Healey, A.J.E.; McKeown, N.J.; Taylor, A.L.; Provan, J.; Sauer, W.; Gouws, G.; Shaw, P.W. Cryptic Species and Parallel Genetic Structuring in Lethrinid Fish: Implications for Conservation and Management in the Southwest Indian Ocean. Ecol. Evol. 2018, 8, 2182–2195. [CrossRef]
Ponton, D.; Carassou, L.; Raillard, S.; Borsa, P. Geometric Morphometrics as a Tool for Identifying Emperor Fish (Lethrinidae) Larvae and Juveniles. J. Fish Biol. 2013, 83, 14–27. [CrossRef]
Wibowo, A.; Wahlberg, N.; Vasemägi, A. DNA Barcoding of Fish Larvae Reveals Uncharacterised Biodiversity in Tropical Peat Swamps of New Guinea, Indonesia. Mar. Freshw. Res. 2017, 68, 1079. [CrossRef]
Durand, J.-D.; Pham, M.H.; Tran, T.T.V.; Hoang, D.H.; Van Vo, Q. Sorting the Wheat from the Chaff: A Review of BINs Associated with Groupers of Vietnam and the Implications for Species Identification from DNA Barcoding. Mar. Biodivers. 2020, 50, 38. [CrossRef]
Collins, R.A.; Cruickshank, R.H. The Seven Deadly Sins of DNA Barcoding. Mol. Ecol. Resour. 2013, 13, 969–975. [CrossRef]
Semmens, B.; Buhle, E.; Salomon, A.; Pattengill-Semmens, C. A Hotspot of Non-Native Marine Fishes: Evidence for the Aquarium Trade as an Invasion Pathway. Mar. Ecol. Prog. Ser. 2004, 266, 239–244. [CrossRef]
Blaxter, M. Imagining Sisyphus Happy: DNA Barcoding and the Unnamed Majority. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2016, 371, 20150329. [CrossRef]
