An approach to unraveling the coexistence of snappers (Lutjanidae) using otolith morphology

Authors

  • Zahra Sadighzadeh Marine Biology Department, Graduate school of Marine Science and Technology, Science and Research Branch, Islamic Azad University
  • Jose Luís Otero-Ferrer Universidade de Vigo, Departamento de Ecología y Biología Animal
  • Antoni Lombarte Institut de Ciéncies del Mar (CSIC)
  • Mohammad R. Fatemi Marine Biology Department, Graduate school of Marine Science and Technology, Science and Research Branch, Islamic Azad University
  • Víctor Manuel Tuset Institut de Ciéncies del Mar (CSIC)

DOI:

https://doi.org/10.3989/scimar.03982.16C

Keywords:

otolith, morphology, biodiversity, functional ecology, snappers, Lutjanidae

Abstract


The sagittae otolith morphology of marine fishes has been used in many ecomorphological studies to explain certain ecological adaptations of species to habitat. Our study compares the sagittal otolith shapes of ten species of snappers (Family Lutjanidae) inhabiting the Persian Gulf. We used a morphometric analysis of the otolith measurements (length, height, perimeter, area and weight) and of the ratio between the area of the sulcus acusticus and the area of the otolith (S:O). The otolith contour was also analysed using wavelets as a mathematical descriptor. Morphological variations in the otoliths were associated with the morphology and external colouration of snappers as well as ecological traits. An analysis of the interspecific S:O ratio suggested that the highest ratios occurred in snappers inhabiting shallower waters. A categorical multivariate analysis, including morphological, ecological and otolith size factors, showed that the species adapted to dim light conditions had a greater otolith perimeter. An analysis of variance of the otolith contour revealed zones with a higher interspecific variability, although only the antero-dorsal zone showed differing patterns. Although the otolith patterns appear to have a phylogenetic component, they might also be related to diel activity rhythms or to the light conditions in the habitat. The results of the study showed that variation in otolith morphology can be used to explain the coexistence of sympatric species.

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References

Aguirre H., Lombarte A. 1999. Ecomorphological comparisons of sagittae in Mullus barbatus and M. surmuletus. J. Fish. Biol. 55: 105-114.

Aguzzi J., Sbragaglia V., Santamaría G., et al. 2013. Daily activity rhythms in temperate coastal fishes: insights from cabled observatory video monitoring. Mar. Ecol. Prog. Ser. 486: 223-236. http://dx.doi.org/10.3354/meps10399

Aiken K.A. 1993. Jamaica in Marine Fishery Resources of the Lesser Antilles, Puerto Rico & Hispaniola. FAO Fish. Tech. Pap. 326: 1160 -1180.

Allen G.R. 1985. FAO Species Catalogue. Snappers of the world. An annotated and illustrated catalogue of lutjanid species known to date. FAO Fish. Syn. 125: 1-208.

Assadi H., Dehghani P.R. 1997. Atlas of the Persian Gulf and the Sea of Oman Fishes. Iranian Fisheries Research and Training Organization, 226 pp.

Assis C.A. 2003. The lagenar otoliths of teleosts: their morphology and its application in species identification, phylogeny and systematics. J. Fish Biol. 62: 1268-1295. http://dx.doi.org/10.1046/j.1095-8649.2003.00106.x

Assis C.A. 2005. The utricular otoliths, lapilli, of teleosts: their morphology and relevance for species identification and systematics studies. Sci. Mar. 69: 259-273.

Appeldoorn R.S., Meyers S. 1993. Puerto Rico and Hispaniola. FAO Fish. Tech. Pap. 326: 99-159.

Atema J., Fay R.R., Popper A.N., et al. 1988. Sensory Biology of Aquatic Animals. Springer Verlag, 936 pp. http://dx.doi.org/10.1007/978-1-4612-3714-3

Azzurro E., Aguzzi J., Maynou F., et al. 2013. Diel rhythms in shallow Mediterranean rocky-reef fishes: a chronobiological approach with the help of trained volunteers. J. Mar. Biol. Assoc. U.K. 93: 461-470. http://dx.doi.org/10.1017/S0025315412001166

Baisre J.A. 2000. Chronicle of Cuban marine fisheries (1935-1995). Trend analysis and fisheries potential. FAO Fish. Tech. Pap. 394: 1-26.

Blacker R.W. 1969. Chemical composition of the zones in cod (Gadus morhua L.) otoliths. J. Cons. Int. Explor. Mer 33: 107-108. http://dx.doi.org/10.1093/icesjms/33.1.107

Carlström D. 1963. A crystalographic study of vertebrate otoliths. Biol. Bull. 125: 441-463. http://dx.doi.org/10.2307/1539358

Cerme-o P., Morales-Nin B., Uriarte A. 2006. Juvenile European anchovy otolith microstructure. Sci. Mar. 70: 553-557.

Cervigón F. 1993. Los peces marinos de Venezuela. Volume 2. Fundación Científica Los Roques, Caracas, Venezuela, 954 pp.

Claro R., Lindeman K.C., Parenti L.R. 2001. Ecology of the marine fishes of Cuba. Smithsonian Institution Press, Washington, 253 pp. PMCid:PMC1621142

Cocheret de la Moriniére E., Pollux B.Y.A., Nagelkerken I., et al. 2003. Diet shifts Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuar. Coast. Shelf Sci. 57: 1079-1089. http://dx.doi.org/10.1016/S0272-7714(03)00011-8

Collar D.C., Wainwright P.C. 2009. Ecomorphology of centrarchid fishes. In: Cook S.J., Philipp D.P. (eds), Centrarchid fishes: diversity, biology and conservation. Blackwell Scientific Press, pp. 70-89. http://dx.doi.org/10.1002/9781444316032.ch3

Colmenero A.I., Aguzzi J., Lombarte A., et al. 2010. Sensory constraints in temporal segregation in two species of anglerfish, Lophius budegassa and L. piscatorius. Mar. Ecol. Prog. Ser. 416: 255-265. http://dx.doi.org/10.3354/meps08766

Cruz A., Lombarte A. 2004. Otolith size and its relationship with colour patterns and sound production. J. Fish Biol. 65: 1512-1525. http://dx.doi.org/10.1111/j.0022-1112.2004.00558.x

Cuesta-Albertos J.A., Febrero-Bande M. 2010. A simple multiway ANOVA for functional data. Test 19: 537-557. http://dx.doi.org/10.1007/s11749-010-0185-3

Degens E.T., Deuser W.G., Haedrich R.L. 1969. Molecular structure and composition of fish otoliths. Mar. Biol. 2: 105-113. http://dx.doi.org/10.1007/BF00347005

Deng X., Wagner H.J., Popper A.N. 2011. The inner ear and its coupling to the swim bladder in the deep-sea fish Antimora rostrata (Teleostei: Moridae). Deep Sea Res. Part I Oceanogr. Res. Pap. 58: 27-37. http://dx.doi.org/10.1016/j.dsr.2010.11.001 PMid:21532967 PMCid:PMC3082141

Deng X., Wagner H.J. Popper A.N. 2013. Interspecific variations of inner ear structure in the deep-sea fish family Melamphaidae. Anat. Rec. 296: 1064-1082. http://dx.doi.org/10.1002/ar.22703 PMid:23625740

Druzhinin A.D. 1970. The range and biology of snappers (Family Lutjanidae). J. Ichthyol. 10: 717-736.

Febrero-Bande M., Oviedo de la Fuente M. 2011. fda.usc: Functional Data Analysis and Utilities for Statistical Computing (fda.usc). R package version 0.9.5.

Fox R.J., Bellwood D.R. 2011. Unconstrained by the clock? Plasticity if diel activity rhythm in a tropical reef fish, Siganus lineatus. Funct. Ecol. 25: 1096-1105. http://dx.doi.org/10.1111/j.1365-2435.2011.01874.x

Froese R., Pauly D. 2011. FishBase. World Wide Web electronic publication.

Gauldie R.W. 1988. Function, form and time-keeping properties of fish otoliths. Comp. Biochem. Physiol. Part A 91: 395-402. http://dx.doi.org/10.1016/0300-9629(88)90436-7

Gauldie R.W., Crampton J.S. 2002. An ecomorphological explication of individual variability in the shape of the fish otolith: comparison of the otolith of Hoplostethus atlanticus with other species by depth. J. Fish Biol. 60: 1221-1240. http://dx.doi.org/10.1111/j.1095-8649.2002.tb01715.x

Holt S.A. 2002. Intra- and inter-day variability in sound production by red drum (Sciaenidae) at a spawning site. Bioacoustics 12: 227-229. http://dx.doi.org/10.1080/09524622.2002.9753704

Jonsson B., Jonsson N. 2001. Polymorphism and speciation in Arctic charr. J. Fish Biol. 58: 605-638. http://dx.doi.org/10.1111/j.1095-8649.2001.tb00518.x

Kuiter R.H., Tonozuka T. 2001. Pictorial guide to Indonesian reef fishes. Part 1 eels-snappers, Muraenidae-Lutjanidae. Zoonetics, Australia, 302 pp.

Lombarte A. 1992 Changes in otolith area:sensory area ratio with body size and depth. Environ. Biol. Fish. 33: 405-410. http://dx.doi.org/10.1007/BF00010955

Lombarte A., Cruz A. 2007. Otolith size trends in marine fish communities from different depth strata. J. Fish Biol. 71: 53-76. http://dx.doi.org/10.1111/j.1095-8649.2007.01465.x

Lombarte A., Fortu-o J.M. 1992. Differences in morphological features of the sacculus of the inner ear of two hakes (Merluccius capensis and M. paradoxus, Gadiformes) inhabits from different depth of sea. J. Morphol. 214: 97-107. http://dx.doi.org/10.1002/jmor.1052140107

Lombarte A., Lleonart J. 1993. Otolith size changes related with body growth, habitat depth and temperature. Environ. Biol. Fish. 37: 297-306. http://dx.doi.org/10.1007/BF00004637

Lombarte A., Palmer M., Matallanas J., et al. 2010. Ecomorphological trends and phylogenetic inertia of otolith sagittae in Nototheniidae. Environ. Biol. Fish. 89: 607-618. http://dx.doi.org/10.1007/s10641-010-9673-2

Luczkovich J.J., Norton S.R., Gilmore R.G. 1995. The influence of oral anatomy on prey selection during the ontogeny of two percoid fishes, Lagodon rhomboides and Centropomus undecimalis. Environ. Biol. Fish. 44: 79-95. http://dx.doi.org/10.1007/BF00005908

Luczkovich J.J., Sprague M.W., Johnson S.E., et al. 1999. Delimiting spawning areas of weakfish Cynoscion regalis (Family Sciaenidae) in Pamlico Sound, North Carolina using passive hydroacoustic surveys. Bioacoustics 10: 143–160. http://dx.doi.org/10.1080/09524622.1999.9753427

Lychakov D.V., Rebane Y.T. 2000. Otolith regularities. Hear. Res. 143: 83-102. http://dx.doi.org/10.1016/S0378-5955(00)00026-5

Mallat S. 1991. Zero-crossings of a wavelet transform. IEEE Trans. Inform. Theory 37: 1019-1033. http://dx.doi.org/10.1109/18.86995

Martinez-Andrade F. 2003. A comparison of life histories and ecological aspects among snappers (Pisces: Lutjanidae). PhD thesis, Lousiana State University, 194 pp.

Meakin C., Qin J. 2011. Growth, behaviour and colour changes of juvenile King George whiting (Silaginodes punctata) mediated by light intensities. New Zealand J. Mar. Freshw. Res. 46: 111-123. http://dx.doi.org/10.1080/00288330.2011.608687

Meulman J.J., Heiser W.J. 2005. Categories 14.0. CD Rom. SPSS Inc., Chicago.

Miller T.L., Cribb T.H. 2007. Phylogenetic relationships of some common Indo-Pacific snappers (Perciformes: Lutjanidae) based on mitochondrial DNA sequences with comments on the taxonomic position of the Caesioninae. Mol. Phyl. Evol. 44: 450-460. http://dx.doi.org/10.1016/j.ympev.2006.10.029 PMid:17188002

Mittelbach G.G. 1984. Predation and resource partitioning in two sunfishes (Centrarchidae). Ecology 65: 499-513. http://dx.doi.org/10.2307/1941412

Montgomery J.C., Pankhurst N.W. 1997. Sensory physiology. In: Randall D.J., Farrell A.P. (eds), Deep-sea Fishes. Academic Press, pp. 325-349. http://dx.doi.org/10.1016/S1546-5098(08)60233-2

Myrberg A.A. Jr. 1980. Fish bioacoustics: its relevance to the 'not so silent world'. Environ. Biol. Fish. 5: 297-304. http://dx.doi.org/10.1007/BF00005184

Nagelkerken I., Kleijnen S., Klop T., et al. 2001. Dependence of Caribbean reef fishes on mangroves and seagrass beds as nursery habitats: a comparison of fish faunas between bays with and without mangroves/seagrass beds. Mar. Ecol. Prog. Ser. 214: 225-235. http://dx.doi.org/10.3354/meps214225

Nolf D. 1985. Otolithi piscium. In: H.P. Schultze (ed.), Handbook of Paleoichthyology. Gustav Fischer Verlag, pp. 1-10.

Pakkasmaa S., Piironen J. 2000. Water velocity shapes juvenile salmonids. Evol. Ecol. 14: 721-730. http://dx.doi.org/10.1023/A:1011691810801

Parisi-Baradad V., Lombarte A., Garcia-Ladona E., et al. 2005. Otolith shape contour analysis using affine transformation invariant wavelet transforms and curvature scale space representation. Mar. Freshw. Res. 56: 795-804. http://dx.doi.org/10.1071/MF04162

Parisi-Baradad V., Manjabacas A., Lombarte A., et al. 2010. Automated Taxon Identification of Teleost fishes using an otolith online database. Fish. Res. 105: 13-20. http://dx.doi.org/10.1016/j.fishres.2010.02.005

Paxton J.R. 2000. Fish otoliths: do sizes correlate with taxonomic group, habitat and/or luminescence? Phil. Trans. Roy. Soc. London Ser. B 355: 1299-1303. http://dx.doi.org/10.1098/rstb.2000.0688 PMid:11079419 PMCid:PMC1692828

Platt C., Popper A.N. 1981. Fine structure and function of the ear. In: Tavolga W.N., Popper A.N., Ray R.R. (eds), Hearing and Sound Communication in Fishes. Springer Verlag, pp. 1-36. http://dx.doi.org/10.1007/978-1-4615-7186-5_1

Popper A.N., Coombs S. 1982. The morphology and evolution of the ear in actinopterygian fishes. Amer. Zool. 22: 311-328.

Popper A.N., Fay R.R. 1993. Sound detection and processing by fish: critical review and major research questions. Brain Beh. Evol. 41: 14-38. http://dx.doi.org/10.1159/000113821 PMid:8431753

Popper A.N., Lu Z. 2000. Structure-function relationships in fish otolith organs. Fish. Res. 46: 15-25. http://dx.doi.org/10.1016/S0165-7836(00)00129-6

Popper A.N., Fay R.R., Platt C., et al. 2003. Sound detection mechanisms and capabilities of teleost fishes. In: Tavolga W.N., Popper A.N., Ray R.R. (eds), Hearing and Sound Communication in Fishes. Springer Verlag, pp. 3-38.

Popper A.N., Ramcharitar J., Campana S.E. 2005. Why otoliths? Insights from inner ear physiology and fisheries biology. Mar. Freshw. Res. 56: 497-504. http://dx.doi.org/10.1071/MF04267

Pulcini D., Costa C., Aguzzi J., et al. 2008. Light and shape: A contribution to demonstrate morphological differences in diurnal and nocturnal Teleosts. J. Morph. 269:375-385. http://dx.doi.org/10.1002/jmor.10598 PMid:17972269

Ramcharitar J., Gannon D.P., Popper A.N. 2006. Bioacoustics of the family Sciaenidae (croakers and drumfishes). Trans. Amer. Fish. Soc. 135: 1409-1431. http://dx.doi.org/10.1577/T05-207.1

Reichenbacher B., Sienknecht U., Ku.chenhoff H., et al. 2007. Combined otolith morphology and morphometry for assessing taxonomy and diversity in fossil and extant killifish (Aphanius, †Prolebias). J. Morph. 268: 898-915. http://dx.doi.org/10.1002/jmor.10561 PMid:17674357

Robinson B.W., Wilson D.S. 1994. Character release and displacement in fishes: a neglected literature. Amer. Naturalist 144: 596-627. http://dx.doi.org/10.1086/285696

Sadighzadeh S., Tuset V.M., Valinassab T., et al. 2012. Comparison of different otolith shape descriptors and morphometrics in the identification of closely related species of Lutjanus spp. from the Persian Gulf. Mar. Biol. Res. 8: 802-814. http://dx.doi.org/10.1080/17451000.2012.692163

Schulz-Mirbach T., Heß M., Plath M. 2011. Inner ear morphology in the Atlantic Molly Poecilia mexicana - First detailed microanatomical study of the inner ear of a Cyprinodontiform species. PLoS One 6(11): e27734. http://dx.doi.org/10.1371/journal.pone.0027734 PMid:22110746 PMCid:PMC3217005

Sisneros J.A., Bass A.H. 2003. Seasonal plasticity of peripheral auditory frequency sensitivity. J. Neurosci. 23: 1049-1058. PMid:12574435

Teimori A., Jawad L.A.J., Al-Kharusi L.H., et al. 2012. Late Pleistocene to Holocene diversification and historical zoogeography of the Arabian killifish (Aphanius dispar) inferred from otolith morphology. Sci. Mar. 76(4): 637-645.

Thayer G.W., Chester A.J. 1989. Distribution and abundance of fishes among basin and channel habitats in Florida Bay. Bull. Mar. Sci. 44: 200-219.

Tuset V.M., Piretti S., Lombarte A., et al. 2010. Using sagittal otoliths and eye diameter for ecological characterization of deep-sea fish: Aphanopus carbo and A. intermedius from NE Atlantic waters. Sci. Mar. 74: 807-814. http://dx.doi.org/10.3989/scimar.2010.74n4807

Valinassab T., Adjeer M., Momeni M. 2010. Biomass estimation of demersal fishes in the Persian Gulf and Oman Sea by swept area method. Iranian Fisheries Research Organization Press, 356 pp.

Volpedo A.V., Echeverría D.D. 2003. Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fish. Res. 60: 551-560. http://dx.doi.org/10.1016/S0165-7836(02)00170-4

Wainwright P.C. 1996. Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 77: 1336-1343. http://dx.doi.org/10.2307/2265531

Wainwright P.C., Bellwood D.R. 2002. Ecomorphology of feeding in coral reef fishes. In: Sale P.F. (ed.), Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, pp. 33-55. http://dx.doi.org/10.1016/B978-012615185-5/50004-9 PMid:12204315

Wainwright P.C., Ferry-Graham L.A., Waltzek T.B., et al. 2001. Evaluating the use of ram and suction during prey capture by cichlid fishes. J. Exp. Biol. 204: 3039-3051. PMid:11551992

Weissburg M.J. 2005. Sensory biology: linking the internal and external ecologies of marine organisms. Mar. Ecol. Prog. Ser. 287: 263-265. http://dx.doi.org/10.3354/meps287263

Winn H.E. 1967. Vocal facilitation and biological significance of toadfish sounds. In: Tavolga W.N (ed), Marine Bio-Acoustics II. Pergamon Press, pp. 283-303.

Published

2014-09-30

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1.
Sadighzadeh Z, Otero-Ferrer JL, Lombarte A, Fatemi MR, Tuset VM. An approach to unraveling the coexistence of snappers (Lutjanidae) using otolith morphology. Sci. mar. [Internet]. 2014Sep.30 [cited 2024Mar.28];78(3):353-62. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1537

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