[en] Background: Many coral reef fishes undergo habitat and diet shifts during ontogeny. However, studies focusing on the physiological and morphological adaptations that may prepare them for these transitions are relatively scarce. Here, we explored the body shape variation related to ontogenetic shifts in the ecology of the surgeonfish Acanthurus triostegus (Acanthuridae) from new settler to adult stages at Moorea Island (French Polynesia). Specifically, we tested the relationship between diet and habitat shifts and changes in overall body shape during the ontogeny of A. triostegus using a combination of geometric morphometric methods, stomach contents and stable isotope analysis.
Results: After reef settlement, stable isotope composition of carbon and nitrogen revealed a change from a zooplanktivorous to a benthic algae diet. The large amount of algae (> 75% of stomach contents) found in the digestive tract of small juveniles (25–30 mm SL) suggested the diet shift is rapid. The post-settlement growth of A. triostegus is highly allometric. The allometric shape changes mainly concern cephalic and pectoral regions. The head becomes shorter and more ventrally oriented during growth. Morphological changes are directly related to the diet shift given that a small mouth ventrally oriented is particularly suited for grazing activities at the adult stage. The pectoral fin is more anteriorely and vertically positioned and its basis is larger in adults than in juveniles. This shape variation had implications for swimming performance, manoeuvrability, turning ability and is related to habitat shift. Acanthurus triostegus achieves its main transformation of body shape to an adult-like form at size of 35–40 mm SL.
Conclusion: Most of the shape changes occurred after the reef colonization but before the transition between juvenile habitat (fringing reef) and adult habitat (barrier reef). A large amount of allometric variation was observed after diet shift from zooplankton to benthic algae. Diet shift could act as an environmental factor favouring or inducing morphological changes. On the other hand, the main shape changes have to be achieved before the recruitment to adult populations and start negotiating the biophysical challenges of locomotion and feeding in wave- and current-swept outer reef habitat.
Research center :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Leis JM, McCormick MI. The biology, behaviour and ecology of the pelagic, larval stage of coral reef fishes. Coral reef fishes: dynamics and diversity in a complex ecosystem 2002, 171-199. Academic, San Diego, Sale PF.
McCormick MI, Makey LJ. Post-settlement transition in coral reef fishes: overlooked complexity in niche shifts. Marine Ecology-Progress Series 1997, 153:247-257.
McCormick MI, Makey L, Dufour V. Comparative study of metamorphosis in tropical reef fishes. Marine Biology 2002, 141:841-853.
Lecchini D. Spatial and behavioural patterns of reef habitat settlement by fish larvae. Marine Ecology-Progress Series 2005, 301:247-252.
Lecchini D, Galzin R. Spatial repartition and ontogenetic shifts in habitat use by coral reef fishes (Moorea, French Polynesia). Marine Biology 2005, 147:47-58.
Sponaugle S, Cowen RK. Larval supply and patterns of recruitment for two Caribbean reef fishes, Stegastes partitus and Acanthurus bahianus. Marine and Freshwater Research 1996, 47:433-447.
Norton SF, Luczkovich JJ, Motta PJ. The role of ecomorphological studies in the comparative biology of fishes. Environmental Biology of Fishes 1995, 44:287-304.
Wainwright PC. Ecological explanation through functional morphology: The feeding biology of sunfishes. Ecology 1996, 77:1336-1343.
Eggold BT, Motta PJ. Ontogenetic dietary shifts and morphological correlates in striped mullet, Mugil cephalus. Environmental Biology of Fishes 1992, 34:139-158.
Luczkovich JJ, Norton SF, Gilmore RG. The Influence of oral anatomy on prey selection during the ontogeny of two percoid fishes, Lagodon rhomboides and Centropomus undecimalis. Environmental Biology of Fishes 1995, 44:79-95.
Wainwright PC, Richard BA. Predicting patterns of prey use from morphology of fishes. Environmental Biology of Fishes 1995, 44:97-113.
Loy A, Bertelletti M, Costa C, Ferlin L, Cataudella S. Shape changes and growth trajectories in the early stages of three species of the genus Diplodus (Perciformes, Sparidae). Journal of Morphology 2001, 250:24-33. 10.1002/jmor.1056, 11599013.
Russo T, Costa C, Cataudella S. Correspondence between shape and feeding habit changes throughout ontogeny of gilthead sea bream Sparus aurata L., 1758. Journal of Fish Biology 2007, 71:629-656.
Russo T, Pulcini D, Bruner E, Cataudella S. Shape and Size Variation: Growth and Development of the Dusky Grouper (Epinephelus marginatus Lowe, 1834). Journal of Morphology 2009, 270:83-96. 10.1002/jmor.10674, 18798248.
Vigliola L, Harmelin-Vivien M. Post-settlement ontogeny in three Mediterranean reef fish species of the genus Diplodus. Bulletin of Marine Science 2001, 68:271-286.
Frédérich B, Adriaens D, Vandewalle P. Ontogenetic shape changes in Pomacentridae (Teleostei, Perciformes) and their relationships with feeding strategies: a geometric morphometric approach. Biological Journal of the Linnean Society 2008, 95:92-105.
Lukoschek V, McCormick MI. Ontogeny of diet changes in a tropical benthic carnivorous fish, Parupeneus barberinus (Mullidae): relationship between foraging behaviour, habitat use, jaw size, and prey selection. Marine Biology 2001, 138:1099-1113.
Bellwood DR. Ontogenetic changes in the diet of early post-settlement Scarus species (Pisces: Scaridae). Journal of Fish Biology 1988, 33:213-219.
Klingenberg CP. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews 1998, 73:79-123. 10.1017/S000632319800512X, 9569772.
Randall JE. A contribution to the biology of the convict surgeonfish of the Hawaiian Islands, Acanthurus triostegus sandoicensis. Pacific Science 1961, 15:215-272.
McCormick MI. Delayed metamorphosis of a tropical reef fish (Acanthurus triostegus): a field experiment. Marine Ecology-Progress Series 1999, 176:25-38.
Sampey A, McKinnon AD, Meekan MG, McCormick MI. Glimpse into guts: overview of the feeding of larvae of tropical shorefishes. Marine Ecology-Progress Series 2007, 339:243-257.
Frédérich B, Fabri G, Lepoint G, Vandewalle P, Parmentier E. Trophic niches of thirteen damselfishes (Pomacentridae) at the Grand Récif of Toliara, Madagascar. Ichthyological Research 2009, 56:10-17.
Lecchini D, Dufour V, Carleton J, Strand S, Galzin R. Estimating the patch size of larval fishes during colonization on coral reefs. Journal of Fish Biology 2004, 65:1142-1146.
Rohlf FJ. TpsDig (Version 1.40), a software program for landmark data acquisition 2004, Department of Ecology and Evolution, State University of New York at Stony Brook, doi:., http://life.bio.sunysb.edu/morph/
Bookstein F. Morphometric tools for landmark data: geometry and biology 1991, University Press, Cambridge.
Bookstein F. Combining the tools of geometric morphometrics. Advances in morphometrics 1996, 131-151. Plenum Press, New York, Marcus LF, Corti M, Loy A, Naylor G, Slice D.
Rohlf FJ, Marcus LF. A revolution in morphometrics. Trends in Ecology & Evolution 1993, 8:129-132. 10.1016/0169-5347(93)90024-J, 3419722, 22916142.
Zelditch ML, Swiderski DL, Sheets HD, Fink WL. Geometric morphometrics for biologists: A primer 2004, Elsevier Academic Press, San Diego.
Lawing AM, Polly PD. Geometric morphometrics: recent applications to the study of evolution and development. Journal of Zoology 2010, 280:1-7.
Rohlf FJ, Slice D. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 1990, 39:40-59.
Rohlf FJ. Relative warps analysis and an example of its application to mosquito wings. Contributions to morphometrics 1993, 131-159. Monografias del Museo Nacional de Ciencias Naturales, CSIC, Madrid, Marcus LF, Bello E, G-V A.
Thompson DAW. On growth and form 1917, Cambridge University Press, .
Sheets HD. Regress6: calculation of regressions between shape variables and a dependant variable 2003, Department of Physics, Canisius College, Buffalo, doi:., http://www2.canisius.edu/~sheets/morphsoft.html
Sheets HD. PCAGen6: Principal Component Analysis of shape variables 2001, Department of Physics, Canisius College, Buffalo, doi:., http://www2.canisius.edu/~sheets/morphsoft.html
Wilson S, Bellwood DR. Cryptic dietary components of territorial damselfishes (Pomacentridae, Labroidei). Marine Ecology-Progress Series 1997, 153:299-310.
McCormick MI. Ontogeny of diet shifts by a microcarnivorous fish, Cheilodactylus spectabilis: relationship between feeding mechanics, microhabitat selection and growth. Marine Biology 1998, 132:9-20.
Youson JH. First metamorphosis. Fish physiology 1988, 135-196. Academic, New York, Hoar WS, Randall DJ.
Victor BC. Settlement strategies and biogeography of reef fishes. The ecology of fishes on coral reefs 1991, 231-260. Academic, San Diego, Sale PF.
Frédérich B, Lecchini D, Vandewalle P. Evidence of an original scale development during the settlement phase of a coral reef fish (Acanthurus triostegus). Journal of Applied Ichthyology 2010, 26:176-178.
Sweeting CJ, Jennings S, Polunin NVC. Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory. Functional Ecology 2005, 19:777-784.
Caut S, Angulo E, Courchamp F. Discrimination factors (δ15N and δ13C) in an omnivorous consumer: Effect of diet isotopic ratio. Functional Ecology 2008, 22:255-263.
de la Moriniere EC, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, van der Velde G. Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Marine Ecology-Progress Series 2003, 246:279-289.
Lepoint G, Frédérich B, Gobert S, Parmentier E. Isotopic ratios and elemental contents as indicators of seagrass C processing and sewage influence in a tropical macrotidal ecosystem (Madagascar, Mozambique Channel). Scientia Marina 2008, 72:109-117.
Konow N, Bellwood DR, Wainwright PC, Kerr AM. Evolution of novel jaw joints promote trophic diversity in coral reef fishes. Biological Journal of the Linnean Society 2008, 93:545-555.
Purcell SW, Bellwood DR. A functional analysis of food procurement in two surgeonfish species, Acanthurus nigrofuscus and Ctenochaetus striatus (Acanthuridae). Environmental Biology of Fishes 1993, 37:139-159.
Fulton CJ. Swimming speed performance in coral reef fishes: Field validations reveal distinct functional groups. Coral Reefs 2007, 26:217-228.
Webb PW. The biology of fish swimming. Mechanics and physiology of animal swimming 1994, 45-62. Cambridge University Press, Cambridge, Maddock L, Bone Q, Rayner JMV.
Blake RW. Fish functional design and swimming performance. Journal of Fish Biology 2004, 65:1193-1222.
Webb PW, LaLiberte GD, Schrank AJ. Does body and fin form affect the maneuverability of fish traversing vertical and horizontal slits?. Environmental Biology of Fishes 1996, 46:7-14.
Gerstner CL. Maneuverability of four species of coral-reef fish that differ in body and pectoral-fin morphology. Canadian Journal of Zoology 1999, 77:1102-1110.
Nakamura Y, Shibuno T, Lecchini D, Kawamura T, Watanabe Y. Spatial variability in habitat associations of pre- and post-settlement stages of coral reef fishes at Ishigaki Island, Japan. Marine Biology 2009, 156:2413-2419.