Abstract
Important morphological and ecological modifications occur during the transition between pelagic and demersal phases in marine fish. However, it is still unknown how fast these shape changes may occur. We studied the shape changes of a common cryptobenthic fish, the triplefin Helcogrammoides chilensis (Cancino, 1960) during the shift from pelagic larvae to recently settled individuals, along rocky shores in central Chile during the austral summers of 2020 and 2021. The working hypothesis was that larval stages would show more allometry and faster shape changes in the head and the paired fins insertion than benthic juveniles, in preparation for their new environment. Shape changes were analyzed utilizing landmark-based geometric morphometrics, while age was estimated using sagittal otolith microstructure analysis. There was an important overlap in the size (length and weight) between older larvae and recently settled individuals (between 20 and 25 mm SL, and 0.08–0.17 g), nonetheless, the head shape and paired fins were clearly different between stages. Pelagic larvae (46–88 days post hatch) had a shorter pectoral fin base, a frontal mouth opening, and eyes located at the level of the tip of the upper jaw. Meanwhile, recently settled individuals (80–112 days post hatch) had wider, vertically positioned pectoral fins, mouths displaced to a vertical position, and eyes located upper and forward the head. Larvae experienced faster growth rates than settlers (0.24 vs. 0.02 mm day−1, respectively), and the pattern of ontogenetic shape changes decreased two orders of magnitude after settlement. It is plausible that after the pelagic–demersal shift most of the fish’s energy was used in body structure rearrangement and incrementing body pigmentation, as an adaptation of cryptobenthic juvenile to the rocky reef.
Similar content being viewed by others
Data availability
Raw coordinates of the geometric morphometric analysis are available as Supplementary Material. Data of otolith microstructure will be available upon reasonable request.
Code availability
Not applicable.
References
Bellwood, D. R., C. H. R. Goatley, S. J. Brandl & O. Bellwood, 2014. Fifty million years of herbivory on coral reefs: fossils, fish and functional innovations. Proceedings of the Royal Society B: Biological Sciences 281: 20133046. https://doi.org/10.1098/rspb.2013.3046.
Bernal-Durán, V. & M. F. Landaeta, 2017. Feeding variations and shape changes of a temperate reef clingfish during its early ontogeny. Scientia Marina 81: 205–215. https://doi.org/10.3989/scimar.04555.09A.
Bernal-Durán, V., N. Jahnsen-Guzman & M. F. Landaeta, 2017. Sharing morphospaces: early ontogenetic shape changes in two clingfish larvae (Pisces: Gobiesocidae) from the south-east Pacific Ocean. Journal of Fish Biology 91: 1510–1516. https://doi.org/10.1111/jfb.13451.
Berríos, V. & M. Vargas, 2004. Estructura trófica de la asociación de peces intermareales de la costa rocosa del norte de Chile. Revista de Biología Tropical 52: 201–212.
Bookstein, F. L., 1991. Morphometric Tools for Landmark Data. Cambridge University Press, Cambridge: 435.
Brandl, S. J., C. H. R. Goatley, D. R. Bellwood & L. Tornabene, 2018. The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs. Biological Reviews 93: 1846–1873. https://doi.org/10.1111/brv.12423.
Caiger, P. E., C. Croq & K. D. Clements, 2021. Environmentally induced morphological variation in the temperate reef fish, Forsterygion lapillum (F. Tripterygiidae). Marine Biology 168: 131. https://doi.org/10.1007/s00227-021-03939-3.
Cancino, J. M. & J. C. Castilla, 1988. Emersion behaviour and foraging ecology of the common Chilean clingfish Sicyases sanguineus (Pisces: Gobiesocidae). Journal of Natural History 22: 249–261. https://doi.org/10.1080/00222938800770191.
Cancino, C., K. Farías, S. Lampas, B. González & V. Cuevas, 2010. Descripción de los complejos estructurales óseos en Helcogrammoides chilensis (Blennioidei: Tripterygiidae) de la zona central de Chile. Revista de Biología Marina y Oceanografía 45: 671–682. https://doi.org/10.4067/S0718-19572010000400011.
Chen, Y., W. Wang, W. Zhou, F. Hu & M. Wu, 2022. Shifting feeding habits during settlement among small yellow croackers (Larimichthys polyactis). Frontiers in Marine Science 8: 786724. https://doi.org/10.3389/fmars.2021.786724.
Depczynski, M. & D. R. Bellwood, 2003. The role of cryptobenthic reef fishes in coral reef trophodynamics. Marine Ecology Progress Series 256: 183–191. https://doi.org/10.3354/meps256183.
Dryden, I. L. & K. V. Mardia, 1998. Statistical Analysis of Shape. Wiley, Chichester.
Frédérich, B., O. Colleye, G. Lepoint & D. Lecchini, 2012. Mismatch between shape changes and ecological shifts during the post-settlement growth of the surgeonfish, Acanthurus triostegus. Frontiers in Zoology 9: 8. https://doi.org/10.1186/1742-9994-9-8.
Hernández-Miranda, E., A. T. Palma & F. P. Ojeda, 2003. Larval fish assemblages in nearshore coastal waters off central Chile: temporal and spatial patterns. Estuarine, Coastal and Shelf Science 56: 1075–1092. https://doi.org/10.1016/S0272-7714(02)00308-6.
Jensen, M., P. J. Nielsen & G. G. Wilson, 2023. Links between the timing of life history transitions and dietary and morphological variation during early life history in the sand goby, Pomatoschistus minutus. Journal of Fish Biology. https://doi.org/10.1111/jfb.15477.
Kaufman, L., J. Ebersole, J. Beets & C. C. McIvor, 1992. A key phase in the recruitment dynamics of coral reef fishes: post-settlement transition. Environmental Biology of Fishes 34: 109–118. https://doi.org/10.1007/BF00002386.
Kingsford, M. J. & J. H. Choat, 1989. Horizontal distribution patterns of presettlement reef fish: are they influenced by the proximity of reef? Marine Biology 101: 285–297.
Klingenberg, C. P., 1998. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews 73: 79–123. https://doi.org/10.1017/S000632319800512X.
Klingenberg, C. P., 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11: 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.
Landaeta, M. F., V. Nowajewski, L. D. Paredes & C. A. Bustos, 2019a. Early life history traits of the blenny Aunchenionchus crinitus (Teleostei: Labrisomidae) off northern Chile. Journal of the Marine Biological Association of the United Kingdom 99: 963–974. https://doi.org/10.1017/S0025315418000619.
Landaeta, M. F., V. Bernal-Durán, M. I. Castillo, M. Díaz-Astudillo, B. Fernández-General & P. Núñez-Acuña, 2019b. Nearshore environmental conditions influence larval growth and shape changes for a temperate rocky reef fish. Hydrobiologia 839: 159–176. https://doi.org/10.1007/s10750-019-04004-3.
Landaeta, M. F., Y. Figueroa-González, G. Moyano, J. Vera-Duarte, A. Pérez-Matus & G. Plaza, 2022. Mismatch between shape changes, early growth, and condition for a temperate reef fish from an oceanic island. Marine and Freshwater Research 73(5): 624–636. https://doi.org/10.1071/MF21084.
Leis, J. M., 1991. The pelagic stage of reef fishes: the larval biology of coral reef fishes. In Sale, P. F. (ed.), The Ecology of Fishes on Coral Reefs Academic Press, San Diego, CA: 183–230.
Leis, J. M. & M. I. McCormick, 2002. The biology, behavior and ecology of the pelagic, larval stage of coral reef fishes. In Sale, P. F. (ed.), Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem Academic Press, San Diego, CA: 171–199.
Loy, A., L. Mariani, M. Bertelletti & L. Tunesi, 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). Journal of Morphology 237: 137–146. https://doi.org/10.1002/(SICI)1097-4687(199808)237:2%3c137::AID-JMOR5%3e3.0.CO;2-Z.
Mansur, L., D. Catalán, G. Plaza, M. F. Landaeta & F. P. Ojeda, 2013. Validations of the daily periodicity of increment deposition in rocky intertidal fish otoliths of the south-eastern Pacific Ocean. Revista de Biología Marina y Oceanografía 48: 629–633. https://doi.org/10.4067/S0718-19572013000300019.
Mansur, L., G. Plaza, M. F. Landaeta & F. P. Ojeda, 2014. Planktonic duration in fourteen species of intertidal rocky fishes from the south-eastern Pacific Ocean. Marine and Freshwater Research 65: 901–909. https://doi.org/10.1071/MF13064.
Marliave, J. B., 1986. Lack of planktonic dispersal of rocky intertidal fish larvae. Transactions of the American Fisheries Society 115: 149–154.
Martínez-Leiva, L., J. M. Landeira, E. Fatira, J. Díaz-Pérez, S. Hernández-León, J. Roo & V. M. Tuset, 2023. Energetic implications of morphological changes between fish larval and juvenile stages using geometric morphometrics of body shape. Animals 13: 370. https://doi.org/10.3390/ani13030370.
McCormick, M. I., 1993. Development and changes at settlement in the barbel structure on the reef fish, Upeneus tragula (Mullidae). Environmental Biology of Fishes 37: 269–282. https://doi.org/10.1007/BF00004634.
McCormick, M. I. & L. Makey, 1997. Post-settlement transition in coral reef fishes: overlooked complexity in niche shifts. Marine Ecology Progress Series 153: 247–257.
McCormick, M. I., L. Makey & V. Dufour, 2002. Comparative study of metamorphosis in tropical reef fishes. Marine Biology 141: 841–853. https://doi.org/10.1007/s00227-002-0883-9.
Monteiro, L. R. 1999. Multivariate regression models and geometric morphometrics: The search for causal factors in the analysis of shape. Systematic Biology 48: 192–199.
Palacios-Fuentes, P., M. F. Landaeta, G. Muñoz, G. Plaza & F. P. Ojeda, 2012. The effects of a parasitic copepod on the recent larval growth of a fish inhabiting rocky coasts. Parasitology Research 111: 1661–1671. https://doi.org/10.1007/s00436-012-3005-8.
Palacios-Fuentes, P., M. F. Landaeta, N. Jahnsen-Guzmán, G. Plaza & F. P. Ojeda, 2014. Hatching patterns and larval growth of a triplefin from central Chile inferred by otolith microstructure analysis. Aquatic Ecology 48: 259–266. https://doi.org/10.1007/s10452-014-9481-4.
Palacios-Fuentes, P., M. Díaz-Astudillo, M. A. Reculé, F. P. Ojeda & M. F. Landaeta, 2020. Presettlement schooling behaviour of a rocky fish in a shallow area. Is it related to local environmental conditions? Scientia Marina 84: 243–252. https://doi.org/10.3989/scimar.05043.19A.
Pérez, R., 1979. Desarrollo postembrionario de Tripterygion chilensis Cancino 1955, en la Bahía de Valparaíso (Tripterygiidae: Perciformes). Revista de Biología Marina 16: 319–329.
Plaza, G., M. F. Landaeta, C. V. Espinoza & F. P. Ojeda, 2013. Daily growth patterns of six species of young-of-the-year of Chilean intertidal fishes. Journal of the Marine Biological Association of the United Kingdom 93: 389–395. https://doi.org/10.1017/s00253154120000859.
Polanco-Pérez, J., F. V. Search, P. Winckler, M. J. Ochoa-Muñoz & M. F. Landaeta, 2021. Unexpected effects of coastal storms on trophic ecology of two rocky reef fish species. Marine Biology 168: 20. https://doi.org/10.1007/s00227-021-03827-w.
Primost, M. A., G. Bigatti & F. Marquez, 2015. Shell shape as indicator of pollution in marine gastropods affected by imposex. Marine and Freshwater Research 67: 1948–1954. https://doi.org/10.1071/MF15233.
Raventos, N., H. Torrado, R. Arthur, T. Alcoverro & E. Macpherson, 2021. Temperature reduces fish dispersal as larvae grow faster to their settlement size. Journal of Animal Ecology 90: 1419–1432. https://doi.org/10.1111/1365-2656.13435.
Rossi, A., M. Levaray, C. Paillon, E. D. H. Durieux, V. Pasqualini & S. Agostini, 2019. Relationship between swimming capacities and morphological traits of fish larvae at settlement stage: a study of several coastal Mediterranean species. Journal of Fish Biology 95: 348–356. https://doi.org/10.1111/jfb.13955.
Schaefer, K. & F. L. Bookstein, 2009. Does geometric morphometrics serve the needs of plasticity research? Journal of Bioscience 34: 589–599. https://doi.org/10.1007/s12038-009-0076-5.
Smith, A. C. & J. S. Shima, 2011. Variation in the effects of larval history on juvenile performance on a temperate reef fish. Austral Ecology 36: 830–838. https://doi.org/10.1111/j.1442-9993.2010.02223.x.
Solomon, F. N., D. Rodrigues, E. J. Gonçalves, E. A. Serrão & R. Borges, 2017. Larval development and allometric growth of the black-faced blenny Tripterygion delaisi. Journal of Fish Biology 90: 2239–2254. https://doi.org/10.1111/jfb.13286.
Stimson, J. S., 1990. Density dependent recruitment in the reef fish Chaetodon miliaris. Environmental Biology of Fishes 29: 1–13. https://doi.org/10.1007/BF00000563.
Thorrold, S. R. & M. J. Milicich, 1990. Comparison of larval duration and pre- and post-settlement growth in two species of damselfish, Chromis atripectoralis and Pomacentrus coelestis (Pisces, Pomacentridae), from the Great Barrier Reef. Marine Biology 105: 375–384. https://doi.org/10.1007/BF01316308.
Tupper, M. & R. G. Boutilier, 1997. Effects of habitat on settlement, growth, predation risk and survival of a temperate reef fish. Marine Ecology Progress Series 151: 225–236. https://doi.org/10.3354/meps151225.
Vera-Duarte, J., C. A. Bustos & M. F. Landaeta, 2017. Diet and body shape changes of paroko Kelloggella disalvoi (Gobiidae) from intertidal pools of Easter Island. Journal of Fish Biology 91: 1319–1336. https://doi.org/10.1111/jfb.13450.
Victor, B., 1991. Settlement strategies and biogeography of reef fishes. In Sale, P. (ed.), The Ecology of Fishes on Coral Reefs. Academic Press, San Diego.
Webb, J., 1999. Larvae in fish development and evolution. In Hall, B. K. & M. H. Wake (eds), The Origin and Evolution of Larval Forms. Academic Press, San Diego.
Williams, J. T. & V. G. Springer, 2001. Review of the South American-Antarctic triplefin genus Helcogrammoides (Perciformes: Tripterygiidae). Revista de Biologia Tropical 40(Suppl. 1): 117–123.
Acknowledgements
We thank Javier Polanco-Pérez, Andrés Castro, Pablo Lorca, and all the team at LABITI, for their help and support in the field collection at Montemar, Valparaíso, and the collaboration by Jorge E. Contreras and José Agreda in the otolith microstructure analysis. Two anonymous reviewers and the editor improved an early version of the ms. We also thank Fran Search for the English revision. HAB would like to thank ANID Grant – Millennium Science Initiative Program – ICN2021_002.
Funding
This work was partially funded by the Chilean Antarctic Institute project INACH RT_08-18 Grant to MFL, Centro COSTA-R (Project CIDI 12 Universidad de Valparaíso), and Project RED21992, Sistema articulado de investigación en Cambio Climático y Sustentabilidad en zonas costeras de Chile.
Author information
Authors and Affiliations
Contributions
FP-C digitized the landmarks, extracted and mounted otoliths, and performed data analysis; YF-G took photographs of fish specimens, and extracted and mounted otoliths; GP performed otolith data analyses; FP-C, HAB, and MFL performed geometric morphometric analyses; MFL designed the collection and methodology, and wrote the first version of the manuscript; the whole team wrote the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no financial or proprietary interests in any material discussed in this article.
Additional information
Handling editor: Ian Nagelkerken
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Páez-Collao, F., Figueroa-González, Y., Plaza, G. et al. Fast shape changes prior to settlement for a temperate cryptobenthic fish: an approach using geometric morphometrics and otoliths. Hydrobiologia 851, 527–539 (2024). https://doi.org/10.1007/s10750-023-05341-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-023-05341-0