Feeding variations and shape changes of a temperate reef clingfish during its early ontogeny
DOI:
https://doi.org/10.3989/scimar.04555.09AKeywords:
ecomorphology, feeding ecology, ontogeny, geometric morphometrics, GobiesocidaeAbstract
The majority of rocky reef fishes have complex life cycles, involving transition from a pelagic to a benthic environment. This means that as they grow, their morphology, behaviour and feeding habits must change. Therefore, shape changes occurring during early development of these fishes will be related to diet changes. The clingfish Sicyases sanguineus was selected for this study, because it displays a noticeable variation in shape from pelagic larvae to juvenile stage, and it is expected that diet composition will change as well. The pattern of shape changes was studied using geometric morphometrics. A set of 9 landmarks were digitized in 159 larval and juvenile fish and the same specimens were used for gut content analysis. Allometric growth was most prominent early in the ontogeny, from 4 to 12 mm. Morphology changed from a thin and hydrodynamic shape to a more robust and deeper body prior to settlement. The diet of the clingfish during larval stages showed preferences for a variety of copepod stages. As individual grows the ingested prey volume increases, but not the number and width of prey. A partial least square analysis showed low covariance between shape changes and diet composition changes in prey number and volume, suggesting that the two processes were temporally decoupled. The biggest shape changes, a lengthening of the visceral cavity and a flattening of the head, occurred up to 12 mm standard length, while the largest feeding differentiation, shifting from copepods to microalgae, occurred after 16 mm. Results suggest that shape changes precede trophic changes in this clingfish species during the transition from a pelagic to a benthic habitat.
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References
Anderson M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26: 32-46.
Balbontín F., Llanos A., Valenzuela V. 1997. Sobreposición trófica e incidencia alimentaria en larvas de peces de Chile central. Rev. Chil. Hist. Nat. 70: 381-390.
Bookstein F.L. 1991. Morphometric tools for landmark data. Geometry and Biology. Cambridge University Press, 455 pp.
Cass-Calay S.L. 2003. The feeding ecology of larval Pacific hake (Merluccius productus) in the California Current region: an updated approach using a combined OPC/MOCNESS to estimate prey biovolume. Fish. Oceanogr. 12: 34-48. https://doi.org/10.1046/j.1365-2419.2003.00206.x
Cavalcanti M.J., Monteiro L.R., Lopes P.R.D. 1999. Landmarkbased morphometric analysis in selected species of serranid fishes (Perciformes: Teleostei). Zool. Stud. 38: 287-294.
Contreras J.E., Landaeta M.F., Plaza G., et al. 2013. The contrasting hatching patterns and larval growth of two sympatric clingfishes inferred by otolith microstructure analysis. Mar. Freshw. Res. 64: 157-167. https://doi.org/10.1071/MF12232
Cortés E. 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can. J. Fish. Aquat. Sci. 54: 726-738. https://doi.org/10.1139/f96-316
Costa C., Cataudella S. 2007. Relationship between shape and trophic ecology of selected species of Sparids of the Caprolace coastal lagoon (Central Tyrrhenian sea). Environ. Biol. Fish. 78: 115-123. https://doi.org/10.1007/s10641-006-9081-9
Davis A.M., Pusey B.J., Pearson R.G. 2012. Trophic ecology of terapontid fishes (Pisces: Terapontidae): the role of morphology and ontogeny. Mar. Freshw. Res. 63: 128-141. https://doi.org/10.1071/MF11105
Dryden I.L., Mardia K.V. 1998. Statistical shape analysis. Chichester: Wiley.
Elliott J.P., Bellwood D.R. 2003. Alimentary tract morphology and diet in three coral reef fish families. J. Fish Biol. 63: 1598-1609. https://doi.org/10.1111/j.1095-8649.2003.00272.x
Farré M., Tuset V.M., Maynou F., et al. 2016. Selection of land- marks and semilandmarks in fishes for geometric morphometric analyses: a comparative study based on analytical methods. Sci. Mar. 80: 175-186. https://doi.org/10.3989/scimar.04280.15A
Frédérich B., Adriaens D., Vandewalle P. 2008. Ontogenetic shape changes in Pomacentridae (Teleostei, Perciformes) and their relationships with feeding strategies: a geometric morphometric approach. Biol. J. Linn. Soc. 95: 92-105. https://doi.org/10.1111/j.1095-8312.2008.01003.x
Frédérich B., Colleye O., Lepoint G., et al. 2012. Mismatch between shape changes and ecological shifts during the post-settlement growth of the surgeonfish, Acanthurus triostegus. Frontiers Zool. 9: 8. https://doi.org/10.1186/1742-9994-9-8 PMid:22533865 PMCid:PMC3495409
Gonçalves E.J., Barbosa M., Cabral H.N., et al. 2002. Ontogenetic shifts in patterns of microhabitat utilization in the small-headed clingfish, Apletodon dentatus (Gobiesocidae). Environ. Biol. Fish. 63: 333-339. https://doi.org/10.1023/A:1014302319622
Gould S.J. 1966. Allometry and size in ontogeny and phylogeny. Biol. Rev. 41: 587-640. https://doi.org/10.1111/j.1469-185X.1966.tb01624.x PMid:5342162
Hernández-Miranda E., Veas R., Espinoza C.V., et al. 2009. The use of otoliths and larval abundance for studying the spatial ecology of the blenny Scartichthys viridis (Valenciennes, 1836) in coastal central Chile. Rev. Biol. Mar. Oceanogr. 44: 619-633. https://doi.org/10.4067/S0718-19572009000300009
Herrel A., Joachim R., Vanhooydonck B., et al. 2006. Ecological consequences of ontogenetic changes in head shape and bite performance in the Jamaican lizard Anolis lineatopus. Biol. J. Linn. Soc. 89: 443-454. https://doi.org/10.1111/j.1095-8312.2006.00685.x
Hidalgo P., Escribano R., Vergara O., et al. 2010. Patterns of copepod diversity in the Chilean coastal upwelling system. DeepSea Res. II 57: 2089-2097. https://doi.org/10.1016/j.dsr2.2010.09.012
Hidalgo P., Escribano R., Fuentes M., et al. 2012. How coastal upwelling influences spatial patterns of size-structured diversity of copepods off central-southern Chile (summer 2009). Prog. Oceanogr. 92-95: 134-145. https://doi.org/10.1016/j.pocean.2011.07.012
Ibá-ez A.L., Cowx I.G., O'Higgins P. 2007. Geometric morphometric analysis of fish scales for identifying genera, species, and local populations within the Mugilidae. Can. J. Fish. Aquat. Sci. 64: 1091-1100. https://doi.org/10.1139/f07-075
Kerschbaumer M., Sturmbauer C. 2009. The utility of geometric morphometrics to elucidate pathways of cichlid fish evolution. Int. J. Evol. Biol. 2011: 1-8. https://doi.org/10.4061/2011/290245 PMid:21716723 PMCid:PMC3119416
Klingenberg C.P. 2011. MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour. 11: 353-357. https://doi.org/10.1111/j.1755-0998.2010.02924.x PMid:21429143
Klingenberg C.P. 2013. Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix 24: 15-24.
Klingenberg C.P. 2016. Size, shape, and form: concepts of allometry in geometric morphometrics. Dev. Genes Evol. 226: 113-137. https://doi.org/10.1007/s00427-016-0539-2 PMid:27038023 PMCid:PMC4896994
Klingenberg C.P., Ekau W. 1996. A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae). Biol. J. Linn. Soc. 59: 143-177. https://doi.org/10.1111/j.1095-8312.1996.tb01459.x
Landaeta M.F., Suárez-Donoso N., Bustos C.A., et al. 2011. Feeding habits of larval Maurolicus parvipinnis (Pisces: Sternoptychidae) in Patagonian fjords. J. Plankton Res. 33: 1813-1824. https://doi.org/10.1093/plankt/fbr081
Landaeta M.F., Bustos C.A., Contreras J.E., et al. 2015. Larval fish feeding ecology, growth and mortality from two basins with contrasting environmental conditions of an inner sea of northern Patagonia, Chile. Mar. Environ. Res. 106: 19-29. https://doi.org/10.1016/j.marenvres.2015.03.003 PMid:25756898
Lecchini D. 2005. Spatial and behavioural patterns of reef habitat settlement by fish larvae. Mar. Ecol. Prog. Ser. 301: 247-252. https://doi.org/10.3354/meps301247
Llopiz J.K. 2013. Latitudinal and taxonomic patterns in the feeding ecologies of fish larvae: A literature synthesis. J. Mar. Syst. 109-110: 69-77. https://doi.org/10.1016/j.jmarsys.2012.05.002
Lopes M., Murta A.G., Cabral H.N. 2006. Discrimination of snipefish Macroramphosus species and boardfish Capros aper morphotypes through multivariate analysis of the body shape. Helgoland Mar. Res. 60: 18-24. https://doi.org/10.1007/s10152-005-0010-7
Loy A., Mariani L., Bertelletti M., et al. 1998. Visualizing allometry: geometric morphometrics in the study of shape changes in the early stages of the two-banded sea bream, Diplodus vulgaris (Perciformes, Sparidae). J. Morph. 237: 137-146. https://doi.org/10.1002/(SICI)1097-4687(199808)237:2<137::AID-JMOR5>3.0.CO;2-Z
Loy A., Bertelleti M., Costa C., et al. 2001. Shape changes and growth trajectories in the early stages of three species of the genus Diplodus (Perciformes, Sparidae). J. Morph. 250: 24-33. https://doi.org/10.1002/jmor.1056 PMid:11599013
McCormick M.I., Makey L.J. 1997. Post-settlement transition in coral reef fishes: overlooked complexity in niche shifts. Mar. Ecol. Prog. Ser. 153: 247-257. https://doi.org/10.3354/meps153247
Mitteroecker P., Gunz P. 2009. Advances in geometric morphometrics. Evol. Biol. 36: 235-247. https://doi.org/10.1007/s11692-009-9055-x
Mitteroecker P., Gunz P., Bernhard M., et al. 2004. Comparison of cranial ontogenetic trajectories among great apes and humans. J. Hum. Evol. 46: 679-698. https://doi.org/10.1016/j.jhevol.2004.03.006 PMid:15183670
Motta P.J., Kotrschal K.M. 1992. Correlative, experimental, and comparative experimental approaches in ecomorphology. Neth. J. Zool. 42: 400-415. https://doi.org/10.1163/156854291X00414
Mu-oz A.A., Ojeda F.P. 1997. Feeding guild structure of a rocky intertidal fish assemblage in central Chile. Environ. Biol. Fish. 49: 471-479. https://doi.org/10.1023/A:1007305426073
Norton S.F. 1991. Capture success and diet of cottid fishes: the role of predator morphology and attack kinematics. Ecology 72: 1807-1819. https://doi.org/10.2307/1940980
Ochoa-Mu-oz M.J., Valenzuela C.P., Toledo S., et al. 2013. Feeding of a larval clinid fish in a microtidal estuary from southern Chile. Rev. Biol. Mar. Oceanogr. 48: 45-57. https://doi.org/10.4067/S0718-19572013000100005
Paine R., Palmer A.R. 1978. Sicyases sanguineus: A unique trophic generalist from the Chilean intertidal zone. Copeia 1: 75-81. https://doi.org/10.2307/1443824
Palmer A.R. 1979. Fish predation and the evolution of gastropod shell sculpture: experimental and geographic evidence. Evolution 33: 697-713. https://doi.org/10.1111/j.1558-5646.1979.tb04722.x PMid:28563927
Pearre S. Jr. 1986. Ratio-based trophic niche breadths of fish, the Sheldon spectrum, and the size-efficiency hypothesis. Mar. Ecol. Prog. Ser. 24: 299-314. https://doi.org/10.3354/meps027299
Pérez R. 1981. Desarrollo embrionario y larval de los pejesapos Sicyases sanguineus y Gobiesox marmoratus en la Bahía de Valparaíso, Chile, con notas sobre su reproducción (Gobiesocidae: Pisces). Invest. Mar. (Chile) 9: 1-24.
Piet G.J. 1998. Ecomorphology of a size-structured tropical freshwater fish community. Environ. Biol. Fish. 51: 67-86. https://doi.org/10.1023/A:1007338532482
Pino-Pinuer P., Escribano R., Hidalgo P., et al. 2014. Copepod community response to variable upwelling conditions off central southern Chile during 2002-2004 and 2010-2012. Mar. Ecol. Prog. Ser. 515: 83-95. https://doi.org/10.3354/meps11001
Ponton D., Carassou L., Raillard S., et al. 2013. Geometric morphometrics as a tool for identifying emperor fish (Lethrinidae) larvae and juveniles. J. Fish Biol. 83: 14-27. https://doi.org/10.1111/jfb.12138 PMid:23808689
Reiss C.S., Anis A., Taggart C.T., et al. 2002. Relationships among vertically structured in situ measures of turbulence, larval fish abundance and feeding success and copepods on Western Bank, Scotian Shelf. Fish. Oceanogr. 11: 156-174. https://doi.org/10.1046/j.1365-2419.2002.00194.x
Richard B.A., Wainright P.C. 1995. Scaling of the feeding mechanism of largemouth bass (Micropterus salmoides): kinematics of prey capture. J. Exp. Biol. 198: 419-433. PMid:9318056
Rohlf F.J., Slice D.E. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Zool. 39: 40-59. https://doi.org/10.2307/2992207
Russo T., Costa C., Cataudella S. 2007. Correspondence between shape and feeding habit change throughout ontogeny of gilthead sea bream Sparus aurata L., 1758. J. Fish Biol. 71: 629-656. https://doi.org/10.1111/j.1095-8649.2007.01528.x
Russo T., Pulcini D., O'Leary Á., et al. 2008. Relationship between body shape and trophic niche segregation in two closely related sympatric fishes. J. Fish Biol. 73: 809-828. https://doi.org/10.1111/j.1095-8649.2008.01964.x
Russo T., Pulcini D., Bruner E., et al. 2009. Shape and size variation: Growth and development of the dusky grouper (Epinephelus marginatus Lowe, 1834). J. Morphol. 270: 83-96. https://doi.org/10.1002/jmor.10674 PMid:18798248
Salas-Berríos F., Valdés-Aguilera J., Landaeta M.F., et al. 2013. Feeding habits and diet overlap of marine fish larvae from the peri-Antarctic Magellan region. Pol. Biol. 36: 1401-1414. https://doi.org/10.1007/s00300-013-1359-8
Sassa C., Kawaguchi K. 2004. Larval feeding habits of Diaphus garmani and Myctophum asperum (Pisces: Myctophidae) in the transition region of the western North Pacific. Mar. Ecol. Prog. Ser. 278: 279-290. https://doi.org/10.3354/meps278279
Sidlaukas B.L., Mol J.H., Vari R.P. 2011. Dealing with allometry in linear and geometric morphometrics: a taxonomic case study in the Leporinus cylindriformis group (Characiformes: Anostomidae) with description of a new species from Suriname. Zool. J. Linn. Soc. 162: 103-130. https://doi.org/10.1111/j.1096-3642.2010.00677.x
Sun J., Liu D. 2003. Geometric models for calculating cell biovolume and surface area for phytoplankton. J. Plankton Res. 25: 1331-1346. https://doi.org/10.1093/plankt/fbg096
Tojeira I., Faria A.M., Henriques S., et al. 2012. Early development and larval behaviour of two clingfishes, Lepadogaster purpurea and Lepadogaster lepadogaster (Pisces: Gobiesocidae). Environ. Biol. Fish. 93: 449-459. https://doi.org/10.1007/s10641-011-9935-7
Turingan R.G., Wainwright P.C., Hensley D.A. 1995. Interpopulation variation in prey use and feeding biomechanics in Caribbean triggerfishes. Oecologia 102: 296-304. https://doi.org/10.1007/BF00329796 PMid:28306840
Urho L. 2002. The importance of larvae and nursery areas for fish production. Finnish Game and Fisheries Research Institute.
Usmar N.R. 2012. Ontogenetic diet shifts in snapper (Pagrus auratus: Sparidae) within a New Zealand estuary. N. Z. J. Mar. Fresh. Res. 46: 31-46. https://doi.org/10.1080/00288330.2011.587824
Vargas C.A., Narváez D.A., Pi-ones A., et al. 2006. River plume dynamic influences transport of barnacle larvae in the inner shelf off central Chile. J. Mar. Biol. Ass. U.K. 86: 1057-1065. https://doi.org/10.1017/S0025315406014032
Vera-Duarte J., Landaeta M.F. 2016. Diet of labrisomid blenny Auchenionchus variolosus (Valenciennes, 1836) (Labrisomidae) during its larval development off central Chile (2012-2013). J. Appl. Ichthyol. 32: 46-54. https://doi.org/10.1111/jai.12935
Wainwright P.C. 1991. Ecomorphology: experimental functional anatomy for ecological problems. Amer. Zool. 31: 680-693. https://doi.org/10.1093/icb/31.4.680 https://doi.org/10.1093/icb/31.4.680
Wainwright P.C., Richard B.A. 1995. Predicting patterns of prey use from morphology of fishes. Environ. Biol. Fish. 44: 97-113. https://doi.org/10.1007/BF00005909
Weston E.M. 2003. Evolution of ontogeny in the hippopotamus skull: using allometry to dissect developmental change. Biol. J. Linn. Soc. 80: 625-638. https://doi.org/10.1111/j.1095-8312.2003.00263.x
Wimberger P.H. 1991. Plasticity of jaw and skull morphology in the neotropical cichlids Geophagus brasiliensis and G. steindachneri. Evolution 45: 1545-1563. https://doi.org/10.1111/j.1558-5646.1991.tb02662.x PMid:28564138
Zelditch M.L., Swiderski D.L., Sheets H.D. 2012. Geometric Morphometrics for Biologists: A Primer. Second Edition, Academic Press, 475 pp.
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