Ontogenetic and sexual variation in the sagitta otolith of Menticirrhus americanus (Teleostei; Sciaenidae) (Linnaeus, 1758) in a subtropical environment

Barbara Maichak de Carvalho Alejandra Vanina Volpedo Luís Fernando Fávaro About the authors

Abstract

This study aimed to verify variations in the form of the sagitta otolith of Menticirrhus americanus as to their ontogeny, sex and stage of such structure. Ontogenetically were found significant differences (p < 0.05) for all shape indices (aspect ratios, shape factor, rectangularity, ellipticity, relative surface of sulcus acusticus) and also in the wavelet of the otolith. The CVA presented a 98.6% correct reclassification of the otolith between interval class. Sexual variations were found in the wavelet and in the relative surface of sulcus acusticus index. Between adult females and young females, differences were not detected in the wavelet and rectangularity, but significant differences were found in all other shape indices. The CVA presented a 79.6% correct reclassification of the otolith of the sexes and stages of life sampled. Young females and adults females showed highest correct percentage of classification. The results of this study demonstrate for the first time the influence of the ontogenetic variation and sexual in the form of the otoliths.

Key-Words.
Dimorphism; Otolith; Shape indices; Stage of life; Wavelet

INTRODUCTION

Otoliths are calcium carbonate precipitated primarily as aragonite structures. Present in the inner ear in three pairs: sagittae, asteriscus and lapillus (Popper et al., 2005Popper, A.N.; Ramcharitar, J. & Campana, S.E. 2005. Why otoliths? Insights from inner ear physiology and fisheries biology. Marine and Freshwater Research, 56: 497-504.). Their morphological patterns make them an important tool (Volpedo & Echeverría, 2000Volpedo, A.V. & Echeverría, D.D. 2000. Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. Buenos Aires, Editorial Dunken. 90p.; Volpedo et al., 2017Volpedo, A.V.; Thomposn, G.A. & Avigliano, E. 2017. Atlas de Otolitos de peces de Argentina. Buenos Aires, CAFP-BA-PIESCI. 321p.). In this way, they are useful in studies of trophic ecology of ichthyophagous (Bustos et al., 2012Bustos, L.R.; Daneri, G.A.; Harrington, A.; Varela, E. & Volpedo, A.V. 2012. The diet of the South American tarsea lion (Otaria flavescens) at Río Negro, Patagonia, Argentina, during the winter-spring period. Iheringia, Série Zoológica, 102: 394-340.; Miotto et al., 2017Miotto, M.; Carvalho, B.M. & Spach, H.L. 2017. Does the closed fishing season influence the ichthyofauna consumed by Larus dominicanus? Brazilian Journal Oceanography, 65: 9-18.), in the identification of fish stocks through morphology and morphometry (Avigliano et al., 2015Avigliano, E.; Comte, G.; Rosso, J.J.; Mabragaña, E.; Paola, D.R.; Sanchez, S.; Volpedo, A.; Rosso, F.D. & Schenone, N.F. 2015. Identificación de stocks pesqueros de la corvina de río (Plagioscion ternetzi) de los ríos Paraguay y Paraná, mediante el análisis morfométrico de sus otólitos. Latin American Journal of Aquatic Research, 43(3): 718-725.; Zischke et al., 2016Zischke, M.T.; Litherland, L.; Tilyard, B.R.; Strarford, N.J.; Jones, E.L. & Wang, Y.G. 2016. Otolith morphology of four mackerel species (Scomberomorus spp.) in Australia: Species differentiation and prediction for fisheries monitoring and assessment. Fisheries Research, 176: 39-47.), habitat use (Avigliano et al., 2014Avigliano, E.; Martinez, C.F.R. & Volpedo, A.V. 2014. Combined use of otolith microchemistry and morphometry as indicators of the habitat of the silverside (Odontesthes bonariensis) in a freshwater-estuarine environment. Fisheries Research, 149: 55-60.; Carvalho et al., 2017Carvalho, B.M.; Volpedo, A.V.; Vaz-dos-Santos, A.M. & Spach, H.L. 2017. Use of otolith microchemistry as an indicator of the habitat of Anchoa tricolor (Spix & Agassiz, 1829) in a subtropical estuary. Latin American Journal of Aquatic Research, 45: 457-465.), connectivity between populations (Teimori et al., 2012Teimori, A.; Jawad, L.A.J.; Al-Kharusi, L.H.; Al-Mamry, J.M. & Reichenbacher, B. 2012. Late Pleistocene to Holocene diversification and historical zoogeography of the Arabian killifish (Aphanius dispar) inferred from otolith morphology. Scientia Marina, 76: 637-645.; Tanner et al., 2013Tanner, S.E.; Reis-Santos, P.; Vasconcelos, R.P.; Fonseca, V.F.; França, S.; Cabral, H.N. & Thorrold, S.R. 2013. Does otolith geochemistry record ambient environmental conditions in a temperate tidal estuary? Journal of Experimental Marine Biology and Ecology, 441: 7-15.; Davoren & Halden, 2014Davoren, G.K. & Halden, N.M. 2014. Connectivity of capelin (Mallotus villosus) between regions and spawning habitats in Newfoundland inferred from otolith chemistry. Fisheries Research, 159: 95-104.) and age and growth (Vaz-dos-Santos & Rossi-Wongtschwski, 2007Vaz-dos-Santos, A.M. & Rossi-Wongtschwski, C.L.D.B. 2007. Age and growth of the Argentine hake Merluccius hubbsi Marini, 1933 in the Brazilian South-Southeast Region during 1996-2001. Neotropical Ichthyology, 3: 375-386.; Egbert & Rulifson, 2017Egbert, M.E. & Rulifson, R.A. 2017. Age and growth, reproductive biology, and histology in Atlantic needlefish (Strongylura marina) in a coastal freshwater lake. Marine and Freshwater Research, 68(7):1325-1335.).

Although otoliths have interspecific patterns among species, some morphological changes may occur influenced by various physiological or external factors (Volpedo & Echeverría, 1999Volpedo, A.V. & Echeverría, D.D. 1999. Morfología de los otolitos sagittae de juveniles y adultos de Micropogonias furnieri (Desmarest, 1823) (Sciaenidae). Revista Ciências Marina Thalassas, 15: 19-24.). Reproduction is one of the physiological factors that may influence the morphology of otoliths (Tombari et al., 2005Tombari, A.D.; Volpedo, A.V. & Echeverría, D.D. 2005. Desarrollo de la sagitta en juveniles y adultos de Odontesthes argentinensis (Valenciennes, 1835) y O. bonariensis (Valenciennes, 1835) de la provincia de Buenos Aires, Argentina (Teleostei: Atheriniformes). Revista Chilena de História Natural, 78: 623-633.; Carvalho & Corrêa, 2014Carvalho, B.M. & Corrêa, M.F.M. 2014. Morphometry of the sagitta otolith from Atherinella brasiliensis (Quoy and Gaimard, 1824) (Actinopterygii: Atherinopsidae), at the coast of Paraná. Revista Tropical Oceanography, 42: 54-59.). Some species of the family Atheronipsidae after the onset of the reproductive process develop a dorsal depression in the sagitta otolith (Tombari et al., 2005Tombari, A.D.; Volpedo, A.V. & Echeverría, D.D. 2005. Desarrollo de la sagitta en juveniles y adultos de Odontesthes argentinensis (Valenciennes, 1835) y O. bonariensis (Valenciennes, 1835) de la provincia de Buenos Aires, Argentina (Teleostei: Atheriniformes). Revista Chilena de História Natural, 78: 623-633.; Carvalho & Corrêa, 2014Carvalho, B.M. & Corrêa, M.F.M. 2014. Morphometry of the sagitta otolith from Atherinella brasiliensis (Quoy and Gaimard, 1824) (Actinopterygii: Atherinopsidae), at the coast of Paraná. Revista Tropical Oceanography, 42: 54-59.). In addition to morphological differences between young and adult, it is also possible to identify variations in otolith growth rates before and after the first maturity (Carvalho et al., 2015Carvalho, B.M.; Vaz-dos-Santos, A.M.; Spach, H.L. & Volpedo, A.V. 2015. Ontogenetic development of the sagitta otolith of the anchovy, Anchoa tricolor, in a subtropical estuary. Scientia Marina, 79: 409-418.). Food availability may also differentiate otolith morphology among species (Gagliano & McCormick, 2004Gagliano, M. & McCormick, M.I. 2004. Feeding history influence otolith shape in tropical fish. Marine Ecology Progress Series, 278: 291-296.).

Also, in some species, the biomineralization of otoliths causes morphological and morphometric variations between the sexes (Légua et al., 2013Légua, J.; Plaza, G.; Pérez, D. & Arkhiphin, A. 2013. Otolith shape analysis as a tool for stock identification of the southern blue whiting, Micromesistius australis. Latin American Journal of Aquatic Research, 41: 479-489.; Mille et al., 2015Mille, T.; Mahe, K.; Villanueva, M.C.; De Pontual, H. & Ernande, B. 2015. Sagitta otolith morphogenesis asymmetry in marine fishes. Journal of Fish Biology, 87: 646-663.; Bose et al., 2016Bose, A.P.H.; Adragna, J.B. & Balshine, S. 2016. Otolith morphology varies between populations, sexes and male alternative reproductive tactics in a vocal toadfish Porichthys notatus. Journal of Fish Biology, 1-15.). Different sex growth rates may also influence the morphological and morphometric patterns of otoliths; this change was observed in Micropogonias furnieri (Bervian et al., 2006Bervian, G.; Fontoura, N.F. & Haimovici, M. 2006. Statistical model of variable allometric growth: otolith growth in Micropogonias furnieri (Actinopterygii, Sciaenidae). Journal of Fish Biology, 68: 196-208.) and Anchoa tricolor (Carvalho et al., 2015Carvalho, B.M.; Vaz-dos-Santos, A.M.; Spach, H.L. & Volpedo, A.V. 2015. Ontogenetic development of the sagitta otolith of the anchovy, Anchoa tricolor, in a subtropical estuary. Scientia Marina, 79: 409-418.) on the subtropical Southwestern Atlantic Ocean.

In addition to the physiological factors cited above, environmental factors may influence the morphology and morphometry of otoliths. The depth is related to alterations in the sulcus acusticus area allowing a greater sound perception (Torres et al., 2000Torres, G.J.; Lombarte, A. & Morales-Nin, B. 2000. Variability of the sulcus acusticus in the sagitta otolith of the genus Merluccius (Merlucciidae). Fisheries Research, 46: 5-13.; Cruz & Lombarte, 2004Cruz, A. & Lombarte, A. 2004. Otolith size and its relationship with colour patterns and sound production. Journal of Fish Biology, 65: 1512-1525.). Salinity influences the otolith shape of Odontesthes bonariensis and it is possible to identify processes of environmental salinization or habitat change (Avigliano et al., 2012Avigliano, E.; Tombari, A. & Volpedo, A.V. 2012. ¿EL otolito de pejerrey (Odontesthes bonariensis), refleja el estrés ambiental? Biología Acuática, 1-7.; Avigliano et al., 2014Avigliano, E.; Martinez, C.F.R. & Volpedo, A.V. 2014. Combined use of otolith microchemistry and morphometry as indicators of the habitat of the silverside (Odontesthes bonariensis) in a freshwater-estuarine environment. Fisheries Research, 149: 55-60.), the same process of habitat change was identified for Anguilla anguilla (Capoccioni et al., 2011Capoccioni, F.; Costa, C.; Aguzzi, J.; Menesatti, P.; Lombarte, A. & Ciccotti, E. 2011. Ontogenetic and environmental effects on otolith shape variability in three Mediterranean European eel (Anguilla anguilla, L.) local stocks. Journal of Experimental Marine Biology and Ecology, 397: 1-7.). Thermal amplitudes in water bodies also modify the shape of otoliths in populations exposed to this factor (Lombarte & Lleonart, 1993Lombarte, A. & Lleonart, J. 1993. Otolith size changes related with body grotwh, habitat depth and temperature. Environmental Biology of Fishes, 37: 297-306.; Légua et al., 2013Légua, J.; Plaza, G.; Pérez, D. & Arkhiphin, A. 2013. Otolith shape analysis as a tool for stock identification of the southern blue whiting, Micromesistius australis. Latin American Journal of Aquatic Research, 41: 479-489.).

Some methods can be used to describe the morphology and morphometry of otoliths (Lombarte & Tuset, 2015Lombarte, A. & Tuset, V.M. 2015. Morfolmetria de otólitos. In: Volpedo & Vaz-dos-Santos. Métodos de estudos com otólitos: princípios e aplicações. Buenos Aires, CAFP-BA-PIESCI. p. 59-91.). Shape indeces contribute in understanding the morphometric relationships between fish and otoliths (Volpedo & Echeverría, 1999Volpedo, A.V. & Echeverría, D.D. 1999. Morfología de los otolitos sagittae de juveniles y adultos de Micropogonias furnieri (Desmarest, 1823) (Sciaenidae). Revista Ciências Marina Thalassas, 15: 19-24.; Tuset et al., 2003Tuset, V.M.; Lozano, I.J.; Gonzalez, J.A. 2003. Shape indices to identify regional differences in otolith morphology of comber, Serranus cabrilla (L., 1758). Journal of Applied Ichthyology, 19: 88-93.; Carvalho et al., 2015Carvalho, B.M.; Vaz-dos-Santos, A.M.; Spach, H.L. & Volpedo, A.V. 2015. Ontogenetic development of the sagitta otolith of the anchovy, Anchoa tricolor, in a subtropical estuary. Scientia Marina, 79: 409-418.). The evaluation of the contour of the otoliths can be done through different methods such as: polar coordinates (Lombarte & Tuset, 2015Lombarte, A. & Tuset, V.M. 2015. Morfolmetria de otólitos. In: Volpedo & Vaz-dos-Santos. Métodos de estudos com otólitos: princípios e aplicações. Buenos Aires, CAFP-BA-PIESCI. p. 59-91.), landmarks (Monteiro et al., 2005Monteiro, L.R.; Di Beneditto, A.P.M.; Guillermo, L.H. & Rivera, L.A. 2005. Allometric changes and shape differentiation of sagitta otoliths in sciaenid fishes. Fisheries Research, 74: 288-299.; Carvalho et al., 2015Carvalho, B.M.; Vaz-dos-Santos, A.M.; Spach, H.L. & Volpedo, A.V. 2015. Ontogenetic development of the sagitta otolith of the anchovy, Anchoa tricolor, in a subtropical estuary. Scientia Marina, 79: 409-418.), fourier harmonics (Libungan et al., 2015Libungan, L.A.; Óskarsson, G.J.; Slotte, A.; Jacobsen, J.A. & Pálsson, S. 2015. Otolith shape: a population marker for Atlantic herring Clupea harengus. Journal of Fish Biology, 86:1377-1395.; Bose et al., 2016Bose, A.P.H.; Adragna, J.B. & Balshine, S. 2016. Otolith morphology varies between populations, sexes and male alternative reproductive tactics in a vocal toadfish Porichthys notatus. Journal of Fish Biology, 1-15.) and wavelets (Sadighzadeh et al., 2014Sadighzadeh, Z.; Valinassa, T.; Vosugi, G.; Motallebi, A.A.; Fatemi, M.R.; Lombarte, A. & Tuset, V.M. 2014. Use of otolith shape for stock identification of John’s snapper, Lutjanus johnii (Pisces: Lutjanidae), from the Persian Gulf and the Oman Sea. Fisheries Research, 155: 59-63.; Tuset et al., 2015Tuset, V.M.; Imondi, R.; Aguado, G.; Otero-Ferrer, J.L.; Santschi, L.; Lombarte, A. & Love, M. 2015. Otolith Patterns of Rockfishes from the Northeastern Pacific. Journal of Morphology, 276: 458-469.). According Sadighzadeh et al. (2012Sadighzadeh, Z.; Tuset, V.M.; Valinassab, T.; Dadpour, M.R. & Lombarte, A. 2012. Comparison of different otolith shape descriptors and morphometrics for the identification of closely related species of Lutjanus spp. from the Persian Gulf. Marine Biology Research, 8: 802-814.), the fourier harmonics present better results in phylogenetically distant species while wavelets are more efficient in the differentiation of nearby species and identify intraspecific variations.

The morphology and morphometry of the sagitta otolith of sciaenids has been described by several studies (Corrêa & Vianna, 1992Corrêa, M.F.M. & Viana, M.S. 1992. Catálogo dos otólitos sagitta de Sciaenidae (Ostheichthys ‐ Perciformes) do litoral do estado do Paraná, Brasil. Nerítica, 7: 13-41.; Volpedo & Echeverría, 1999Volpedo, A.V. & Echeverría, D.D. 1999. Morfología de los otolitos sagittae de juveniles y adultos de Micropogonias furnieri (Desmarest, 1823) (Sciaenidae). Revista Ciências Marina Thalassas, 15: 19-24., 2000Volpedo, A.V. & Echeverría, D.D. 2000. Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. Buenos Aires, Editorial Dunken. 90p.; Waessle et al., 2003Waessle, J.A.; Lasta, C.A. & Favero, M. 2003. Otolith morphology and body size relationships for juvenile Sciaenidae in the Río de la Plata estuary (35-36°S). Scienta Marina, 67: 233-240.; Siliprandi et al., 2014Siliprandi, C.C.; Rossi-Wongtschowski, C.L.D.B.; Brenha, M.R.; Gonsales, S.A.; Santificetur, C. & Vaz-Dos-Santos, A.M. 2014. Atlas of marine bony fish otoliths (sagittae) of southeastern - southern Brazil Part II: Perciformes (Carangidae, Sciaenidae, Scombridae and Serranidae). Brazilian Journal Oceanography, 62: 28-101.). Menticirrhus americanus is a species belonging to the family Sciaenidae widely distributed in the Southwestern Atlantic Ocean between latitude 41°N and 51°S (Chao et al., 2015Chao, N.L.; Frédou, F.L.; Haimovici, M.; Peres, M.B.; Polidoro, B.; Raseira, M.; Subirá, R. & Carpenter, K. 2015. A popular and potentially sustainable fishery resource under pressure-extinction risk and conservation of Brazilian Sciaenidae (Teleostei: Perciformes). Global Ecology and Conservation, 1-10.). It is a demersal species with benthophagous habits (Froese & Paully, 2017Froese, R. & Pauly, D. 2017. FishBase. World Wide Web electronic publication. www.fishbase.org, version 06/2017.
www.fishbase.org...
; Haluch et al., 2009Haluch, C.F.; Freitas, M.O.; Corrêa, M.F.M. & Abilhoa, V. 2009. Variação sazonal e mudanças ontogênicas na dieta de Menticirrhus americanus (Linnaeus, 1758) (Teleostei, Sciaenidae) na baía de Ubatuba-Enseada, Santa Catarina, Brasil. Pan-American Journal of Aquatic Sciences, 4: 347-356.). Previous studies made brief morphological and morphometric descriptions of the sagitta otolith of Menticirrhus americanus (Volpedo & Echeverría, 2000Volpedo, A.V. & Echeverría, D.D. 2000. Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. Buenos Aires, Editorial Dunken. 90p.; Siliprandi et al., 2014Siliprandi, C.C.; Rossi-Wongtschowski, C.L.D.B.; Brenha, M.R.; Gonsales, S.A.; Santificetur, C. & Vaz-Dos-Santos, A.M. 2014. Atlas of marine bony fish otoliths (sagittae) of southeastern - southern Brazil Part II: Perciformes (Carangidae, Sciaenidae, Scombridae and Serranidae). Brazilian Journal Oceanography, 62: 28-101.; Volpedo et al., 2018Volpedo, A.V.; Biolé, F.G.; Callicó, Fortunato, R.G.; Tombari, A.D. & Thompson, G.A. 2018. Otolitos de peces de la costa bonaerense. In: Volpedo, A.V.; Thompson, G.A. & Avigliano, E. Atlas de otólitos de peces de Argentina. Buenos Aires, CAFP-BA-PIESCI. p. 181-248.). But these studies not testing the ontogenetic, sexual and life stage variations in the shape of the otolith. Due to this lack of knowledge in this study we will verify possible ontogenetic, sexual and life stage variations (young females and small adult females) in the shape of otolith sagitta de Menticirrhus americanus.

MATERIAL AND METHODS

Area of study and sampling

Bimonthly samplings were performed between August 2015 and February 2016 in two beaches. Initially, in an internal estuarine beach (P1) using gillnets of different mesh sizes (2.5, 4 and 5 cm) and was also used to obtain copies of fishing with hook. On the beach outside the estuary (P2), specimens of artisanal fishing using gillnets of different mesh sizes (6, 7 and 9 cm). Samplings were carried out at the mouth of an estuary and an adjacent beach in the subtropical Southwestern Atlantic Ocean of Brazil (25°28′-25°36′S, 48°20′-48°28′W, Paranaguá Bay, Fig. 1), considered a transition region between tropical and temperate climate (Spalding et al., 2007Spalding, M.D.; Fox, H.E.; Allen, G.R.; Davidson, N.; Ferdaña, Z.A.; Finlayson, M.; Halpern, B.S.; Jorge, M.A.; Lombana, A.; Lourie, S.A.; Martin, K.D.; Mcmanus, E.; Molnar, J.; Recchia, C.A. & Robertson, J. 2007. Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas. BioScience, 57: 573-584.).

Figure 1
Sampling sites of Menticirrhus americanus in estuarine areas (P1) and a beach adjacent (P2) to the estuary in the Subtropical Southwestern Atlantic.

The specimens caught were identified, measured for total length and total weight (TL, in millimeters and TW, in grams, respectively) and separated into five interval classes (110-150; 160-200; 210-250; 260-300; 310-350 mm). Sagitta otoliths were extracted. Gonads were removed, the sex and maturity stage were determined by microscopic analysis according to the procedure described in Possamai & Fávaro (2015Possamai, B. & Fávaro, L.F. 2015. Using mariculture as a breeding site: reproduction of Hypleurochilus fissicornis (Actinopterygii: Blenniidae). Scientia Marina, 79: 1-10.).

Morphometry of otolith

Only the right otolith was photographed, and the morphology of the internal face was classified according to Tuset et al. (2008Tuset, V.M.; Lombarte, A.; Assis, C.A. 2008. Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Scientia Marina, 72: 7-198.). Measurements of the right otoliths were taken using the ImageJ program, namely: length (OL, greater longitudinal distance in mm) and height (OH, greater perpendicular distance in mm) and area (A) of the otolith, area (mm²) of the sulcus acusticus (AS) and otolith perimeter (P, in mm) (Fig. 2).

Figure 2
Scheme of linear morphometry applied to the right otolith of Menticirrhus americanus collected in a subtropical environment: OL = maximum longitudinal length, OH = maximum perpendicular height, A = area of the otolith and AS = area of the sulcus acusticus, Pe = perimeter of the otolith and PeS = perimeter of the sulcus acusticus.

In order to verify the ontogenetic, sexual and in the stages of life variations, the following shape indices were applied as described: OL/TL and OH/OL% Aspect Ratios (Volpedo & Echeverría, 2003Volpedo, A.V. & Echeverría, D.D. 2003. Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fisheries Research, 60: 551-560.), Form Factor [FF = (4π*A) OS-1], Rectangularity [Rc = (A/(OL×OH)), Ellipticity [E = (OL-OH/OL+OH)] (Tuset et al., 2003Tuset, V.M.; Lozano, I.J.; Gonzalez, J.A. 2003. Shape indices to identify regional differences in otolith morphology of comber, Serranus cabrilla (L., 1758). Journal of Applied Ichthyology, 19: 88-93.) and Relative surface of the sulcus acusticus [Rss = AS/A] (Lombarte, 1992Lombarte, A. 1992. Changes in otolith area: sensory area ratio with body size and depth. Environmental Biology of Fishes, 33: 405-410.).

Contour of otolith

The otolith contour reconstruction was done using the wavelets. Wavelets are the result of the expansion of a signal in a family of functions that represent the dilations and translations of a mother function (Mallat, 1991Mallat, S. 1991. Zero crossings of a wavelet transform. IEEE Transaction on Information Theory, 37(4): 1019-1033.): Ψs(x) = 1/sΨ(φ/s), where: Ψ is the function with local support in a limited amplitude on the abscissa axis; φ is the lower pitch filter; s is the scale parameter. The wavelet analysis allows to identify morphological similarities and/or differences as well as at which position of the otolith they are found, since the functions are elaborated from 512 Cartesian coordinates projected at points equidistant along the otolith (Lombarte & Tuset, 2015Lombarte, A. & Tuset, V.M. 2015. Morfolmetria de otólitos. In: Volpedo & Vaz-dos-Santos. Métodos de estudos com otólitos: princípios e aplicações. Buenos Aires, CAFP-BA-PIESCI. p. 59-91.). The wavelet acquisition was performed as described by Parisi-Baradad et al. (2010Parisi-Baradad, V.; Manjabacas, A.; Lombarte, A.; Olivella, R.; Chic, O.; Piera, J. & García-Ladona, E. 2010. Automatic Taxon Identification of Teleost fishes in an otolith online database. Fisheries Research, 105: 13-20.) in site AFORO (http://isis.cmima.csic.es/aforo/index.jsp).

Statistical analysis

The data (shape indices and wavelet) did not meet the assumptions of parametric analysis (Shapiro-Wilk; p < 0.05 and Bartlett, p < 0.05). In this way, the Kruskal-Wallis test was applied to check for differences in shape indices between class intervals and the Conover post-hoc test was applied to identify between which class intervals the indices varied significantly (Pohlert, 2016Pohlert, T. 2016. The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR). R package. http://CRAN.R-project.org/package=PMCMR.
http://CRAN.R-project.org/package=PMCMR...
).

In order to test the sexual differences and in the life stages (young and young females) among the indexes of form were selected specimens collected exclusively in P1. Specimens of similar lengths of females were selected (n = 30; TL mean = 230 ± 12 mm) and adults males (n = 30; TL mean = 222 ± 16 mm), young females (n = 29; TL mean = 144 ± 16 mm) and small young females (n = 29; TL mean = 175 ± 16 mm) this similar size selection between groups is to avoid the effect of allometry on the data. The Wilcoxon Mann-Whitney test was used to test possible variations in the shape indices between males and females and between young females and small young females.

The Permutational Analysis of Variance (PERMANOVA) was used to identify variations in the contour between class intervals. The Bonferroni test was used to identify between which intervals the interactions were significant (p < 0.005). A principal component analysis (PCA) was used to verify the shape variation between the class intervals of the otoliths obtained. Later, with the main components (PCs), a canonical variable analysis (CVA) was performed to verify the percentage of correct reclassification of otoliths between class intervals (Linde et al., 2004Linde, M.; Palmer, M. & Gomez-Zurita, J. 2004. Differential correlates of diet and phylogeny on the shape of the premaxilla and anterior tooth in sparid fishes (Perciformes: Sparidae). Journal of Evolutionary Biology, 17: 941-952.).

A principal component analysis (PCA) was also performed to identify sexual variations and life stages in wavelets obtained from selected otoliths. The CVA to verify the percentage of correct reclassification of the otoliths between the sexes and between young females and young adults with com PCs. The Bonferroni test was used to verify between which parameters these interactions were significant (p < 0.05). Statistical analyses were performed using the R software and Past (Hammer et al., 2001Hammer, Ø.; Harper D.A.T. & Ryan, P.D. 2001. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4: 1-9.).

RESULTS

A total of 291 specimens of M. americanus (TL range: 120 and 345 mm; TW range: 15.33 and 291 g) were analyzed, which were distributed in five length class intervals to describe the ontogeny (Fig. 4). Were used for sexual variation a total 60 specimens of which 30 females (TL mean = 230 ± 12 mm) and 30 males (TL mean = 222 ± 16 mm). Also, were used for life stage variations 29 young females (TL mean = 144 ± 16 mm) and 29 small young females (TL mean = 175 ± 16 mm).

Figure 3
Otolith contour using 512 equidistant point in the otolith the Menticirrhus americanus para a in a subtropical environment: D = dorsal region of otolith, V = ventral region of otolith, A = anterior region of otolith and P = posterior region of otolith.

Figure 4
Frequency distribution of the total length (mm) of the Menticirrhus americanus in two environments in the Subtropical Southwestern Atlantic.

The morphological classification of the otolith showed that some characteristics were constant along the ontogeny such as: absent rostrum and excisura, pseudo-ostial type of sulcus acusticus, the anterior region was round, the posterior region was peak and the external face had calcareous concretions at all class intervals (Fig. 5).

Figure 5
Micrograph of the inner face of the right sagitta otolith of Menticirrhus americanus throughout its ontogenetic development: (A) 132 mm interval 110-150 magnification 52x, (B) 169 mm interval 160-200 magnification 42x, (C) 214 mm interval 210-250 magnification 36x, (D) 285 mm interval 260-300 magnification 42x and (E) 333 mm interval 310-350 magnification 26x.

The length and height of the otolith and the ellipticity and SRS indices presented a positive and direct relationship with TL (Figs. 6A, B, G and H). In contrast, the inverse was observed between TL and the OL/TL aspect ratio, OH/OL% aspect ratio and the form factor (Figs. 6C, D and E). The rectangularity index showed a tendency to increase only for the intervals 110-150 and 160-200 mm, and this upward trend was not found in the upper intervals (Fig. 6F).

Figure 6
Box plot (mean and confidence interval) of morphometric parameters and morphometric indices of the otolith sagitta of Menticirrhus americanus per class interval: (A) otolith length (OL), (B) otolith height (OH), (C) OL/TL aspect ratio, (D) OH/OL% aspect ratio, (E) form factor, (F) rectangularity, (G) ellipticity and (H) surface of the sulcus acusticus (SRS). Circles indicate outliers.

The Kruskal-Wallis test between the morphometric parameters (OL and OH) and all shape indices between the class intervals indicated significant differences (p < 0.001), suggesting ontogenetic variations along the growth of M. americanus. The Bonferroni correction of the Conover post-hoc test interactions are shown in Table 1.

Table 1
Values of probability obtained through the Conover post-hoc test applied to Bonferroni correction between the class intervals and the morphometric indices and the length and height of the sagitta otolith of Menticirrhus americanus from a subtropical Southwestern Atlantic. Values p < 0.05 and p < 0.001 were considered significant.

In the Table 2, the morphometric parameters of the fish and otoliths analyzed together with the otolith shape indices, separated by sex and life stage. Due to size selection the averages of Table 2 are similar for both males and females and young females and small adult females.

Table 2
Morphometric parameters and shape indices (mean ± standard deviation) of Menticirrhus americanus from a subtropical environment were: males (M, n = 30), females (F, n = 30), young females (Y, n = 29) and small females (A, n = 29).

The Wilcoxon Mann-Whitney test evidence significant differences (W = 545, p = 0.0002) only for SRS between males and females. For small adult females and young females, the Wilcoxon Mann-Whitney test among all otolith parameters was significant (p < 0.005), except for the rectangularity (W = 546, p = 0.09) and SRS (W = 530, p = 0.15) indices.

Reconstruction of the contour of the otoliths along the ontogeny showed a high variability in the contour between the different intervals (Fig. 8). From PERMANOVA, significant differences were detected between the contours of the class intervals (F = 3.32; p < 0.0001). The Bonferroni test identified significant variation between all interactions (Table 3).

Figure 7
Scatterplot of the principal component analysis of the contour of the sagitta otolith of Menticirrhus americanus along its ontogeny sampled in two subtropical environments in the Southwestern Atlantic.

Figure 8
Decomposition of the contour of the sagitta otoliths throughout the ontogeny of Menticirrhus americanus, on the x-axis there are 512 Cartesian coordinates of the contour, y-axis, the means of the points. Interval class: dark blue 110-150 mm, orange 160-200 mm, grey 210-250 mm, yellow 260-300 mm and light blue 310-350 mm.

Table 3
Values of probability obtained through the PERMANOVA with the Bonferroni correction applied in the contour of the Menticirrhus americanus otoliths among the class intervals. Values p < 0.05 and p < 0.001 were considered significant.

From the Fig. 7, there is a high variability of contour of the otoliths throughout their ontogeny. The otoliths distributed along PC1 tend to be rounded to elongated, being represented by the smaller intervals in the negative values of PC1 (interval class 110-150 and 160-200) and in the positive values of PC1 are distributed more elliptic otoliths represented by the range 260-300 with pointed posterior region. In PC2, there are the elongated, higher otoliths represented by the intervals 210-250 and 310-350 with a rounded posterior region (Fig. 7).

The CVA presented 98.6% of correct reclassification of the otoliths among the class intervals sampled (Table 4).

Table 4
Correct reclassification of the contour of the otolith Menticirrhus americanus among the class intervals obtained through the analysis of canonical variables (CVA). The number in parentheses corresponds to the frequency of reclassification.

The contour of the otoliths of young and adult females shows a variability in the wavelet 1, wavelet 4, wavelet 5 and wavelet 6 (Fig. 9). The wavelets of males and females are distinguished mainly in the wavelet 4 (Fig. 10). With PERMANOVA, significant differences were identified between the contours of the sexes and life stages (F = 4.53; p = 0.0031). The Bonferroni test identified significant variation between the sexes only (Table 5).

Figure 9
Decomposition of the contour of the sagitta otoliths of males and females of Menticirrhus americanus, on the x-axis there are 512 Cartesian coordinates of the contour, y-axis, the means of the points. Females are black lines and males are gray lines. Circle in wavelet 4 to highlight more discrepant region between males and females.

Figure 10
Decomposition of the contour of the sagitta otoliths of adult and young females of Menticirrhus americanus, on the x-axis there are 512 Cartesian coordinates of the contour, y-axis, the means of the points. Young females are the black lines and adult females, the gray lines.

Table 5
Values of probability obtained through the PERMANOVA with the Bonferroni correction applied in the contour of the Menticirrhus americanus otoliths among the sex (M = males and F= females) and stage of life. Values p < 0.05 and p < 0.001 were considered significant.

The PCA of contour of otoliths between sexes and stages of life demonstrates a high variability of shape of otoliths. Females have peak posterior region (Figs. 11A, C, D) and males have a more rounded posterior region (Fig. 11B). Young females and small young females present more rounded otoliths (Figs. 11C, D).

Figure 11
Scatterplot of the principal component analysis of the contour of the sagitta otolith of males (blue circles), females (red circles), young females (green square) Menticirrhus americanus in an estuarine beach of a subtropical environments in the Subtropical Southwestern Atlantic.

The CVA presented 79.6% of correct reclassification of the otoliths between the sexes and life stages sampled. Young females and small young females had the highest correct percentage of classification (Table 6).

Table 6
Correct reclassification of the contour of the otolith Menticirrhus americanus among the sex and stage of life obtained through the analysis of canonical variables (CVA). The number in parentheses corresponds to the frequency of reclassification.

DISCUSSION

The morphological features of otoliths of M. americanus evaluated during their ontogenetic development, such as: absence of rostrum and excisura, heterosulcoid sulcus acusticus and round anterior region, can be considered diagnostic characteristics of this species, as also described in other studies (Volpedo & Echeverría, 2000Volpedo, A.V. & Echeverría, D.D. 2000. Catálogo y claves de otolitos para la identificación de peces del Mar Argentino. Buenos Aires, Editorial Dunken. 90p.; Siliprandi et al., 2014Siliprandi, C.C.; Rossi-Wongtschowski, C.L.D.B.; Brenha, M.R.; Gonsales, S.A.; Santificetur, C. & Vaz-Dos-Santos, A.M. 2014. Atlas of marine bony fish otoliths (sagittae) of southeastern - southern Brazil Part II: Perciformes (Carangidae, Sciaenidae, Scombridae and Serranidae). Brazilian Journal Oceanography, 62: 28-101.; Volpedo et al., 2017Volpedo, A.V.; Thomposn, G.A. & Avigliano, E. 2017. Atlas de Otolitos de peces de Argentina. Buenos Aires, CAFP-BA-PIESCI. 321p.).

The absence of rostrum and excisura indicates that M. americanus poorly uses water column to move, being a species associated with the substrate after the settlement. These characteristics of the otolith allow to differentiate M. americanus from species that use the water column, since these have a well-developed rostrum and excisura (Volpedo & Echeverría, 2003Volpedo, A.V. & Echeverría, D.D. 2003. Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fisheries Research, 60: 551-560.; Carvalho et al., 2015Carvalho, B.M.; Vaz-dos-Santos, A.M.; Spach, H.L. & Volpedo, A.V. 2015. Ontogenetic development of the sagitta otolith of the anchovy, Anchoa tricolor, in a subtropical estuary. Scientia Marina, 79: 409-418.).

The otolith of M. americanus showed ontogenetic variations in the same way as other authors observed for other marine species (Volpedo & Echeverría, 1999Volpedo, A.V. & Echeverría, D.D. 1999. Morfología de los otolitos sagittae de juveniles y adultos de Micropogonias furnieri (Desmarest, 1823) (Sciaenidae). Revista Ciências Marina Thalassas, 15: 19-24.; Vignon, 2012Vignon, M. 2012. Ontogenetic trajectories of otolith shape during shift in habitat use: Interaction between otolith growth and environment. Marine Ecology Progress Series, 411: 231-241.; Carvalho et al., 2015Carvalho, B.M.; Vaz-dos-Santos, A.M.; Spach, H.L. & Volpedo, A.V. 2015. Ontogenetic development of the sagitta otolith of the anchovy, Anchoa tricolor, in a subtropical estuary. Scientia Marina, 79: 409-418.). Menticirrhus americanus is a species of isometric positive growth (b > 3) (Dias et al., 2014Dias, J.F.; Fernandez, W.S. & Schmidt, T.C.S. 2014. Length-weight relationship of 73 fish species caught in the southeastern inner continental shelf region of Brazil. Latin American Journal of Aquatic Research, 42: 127-136.; Froese & Pauly, 2017Froese, R. & Pauly, D. 2017. FishBase. World Wide Web electronic publication. www.fishbase.org, version 06/2017.
www.fishbase.org...
), this characteristic is corroborated by the otolith growth change, which stops growing in the dorsoventral axis and begins to grow in the anteroposterior axis as also observed for Paralonchurus brasiliensis, another species belonging to the family Sciaenidae (Oliveira et al., 2009Oliveira, M.A.; Di Beneditto, A.P.M. & Monteiro, L.R. 2009. Variação geográfica na forma e nas relações alométricas dos otólitos sagitta da maria-luiza Paralonchurus brasiliensis (Steindachner, 1875) (Teleostei, Sciaenidae) no litoral norte do Rio de Janeiro (21°S-23°S), Brasil. Boletim do Instituto de Pesca, 35: 3 475-485.). According to Avigliano et al. (2012Avigliano, E.; Tombari, A. & Volpedo, A.V. 2012. ¿EL otolito de pejerrey (Odontesthes bonariensis), refleja el estrés ambiental? Biología Acuática, 1-7.), elliptic otoliths are correlated with species that inhabit more saline environments, as is the case of the M. americanus otolith that has elliptic otoliths and has a preferential environment estuarine mouths and shallow internal shelf (Barletta et al., 2008Barletta, M.; Saint-Paul, U.; Amaral, C.S.; Corrêa, M.F.M.; Guebert, F.; Dantas, D.V. & Lorenzi, L. 2008. Factors affecting seasonal variations in fish assemblages at an ecocline in a tropical-subtropical mangrove fringed estuary. Journal of Fish Biology, 73: 1314-1336.).

Ontogenetic variations of otoliths indicate important characteristics of the ecology of M. americanus. According to Volpedo & Echeverría (2003Volpedo, A.V. & Echeverría, D.D. 2003. Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fisheries Research, 60: 551-560.), values in the aspect ratio (OH/OL%) between 30 and 50 indicate species associated with unconsolidated substrates (composed of silt, clay and sand), the values of M. americanus for this index varied between 35 and 45, reflecting that this species throughout its ontogeny is associated with unconsolidated substrates. This preference of M. americanus during all stages of life for this type of substrate is corroborated by its presence in the accompanying fauna in the Atlantic seabob (Xiphopenaeus kroyeri) shrimp fishery (Bernardo et al., 2011Bernardo, C.; Spach, H.L.; Schwarz Junior, R.; Stoiev, S.B. & Cattani, A.P. 2011. A captura incidental de cienídeos em arrasto experimental com rede-de-portas utilizada na pesca do camarão-sete-barbas, Xiphopenaeus kroyeri, no estado do Paraná, Brasil. Arquivos de Ciências do Mar, 44: 98-105.; Cattani et al., 2011Cattani, A.P.; Santos, L.O.; Spach, H.L.; Budel, B.R. & Gondim Guanais, J.H.D. 2011. Avaliação da ictiofauna da fauna acompanhante da pesca do camarão sete-barbas do município de Pontal do Paraná, litoral do Paraná, Brasil. Boletim do Instituto de Pesca, 37: 247-260.).

According to Volpedo et al. (2008Volpedo, A.V.; Tombari, A.D. & Echeverría, D.D. 2008. Eco-morphological patterns of the sagitta of Antarctic. Polar Biology, 31: 1-6.), the SRS index describes how much of the otolith surface comes into contact with the macular nerve through the sulcus acusticus. From this relation, it is possible to suggest the auditory capacity of fish; M. americanus presented higher values of this index than species of the genus Cynoscion (Aguirre, 2003Aguirre, W.E. 2003. Allometric growth of the sulcus in Cynoscion spp. (Sciaenidae). Journal of Fish Biology, 63: 1341-1346.), suggesting a greater auditory capacity of M. americanus in relation to the species of this genus. These observed differences are the result of several ecological factors. First, species of the genus Cynoscion forage in the water column (Rondineli et al., 2007Rondineli, G.R.; Braga, F.M.S.; Tutui, S.L.S. & Bastos, G.C.C. 2007. Dieta de Menticirrhus americanus (Linnaeus, 1758) e Cynoscion jamaicensis (Vaillant e Bocourt, 1883) (Pisces, Sciaenidae) no sudeste do Brasil, Estado de São Paulo. Boletim do Instituto de Pesca, 33: 221-228.) requiring greater visual acuity and may have a lower auditory capacity, while M. americanus is a benthivorous species (Rondineli et al., 2007Rondineli, G.R.; Braga, F.M.S.; Tutui, S.L.S. & Bastos, G.C.C. 2007. Dieta de Menticirrhus americanus (Linnaeus, 1758) e Cynoscion jamaicensis (Vaillant e Bocourt, 1883) (Pisces, Sciaenidae) no sudeste do Brasil, Estado de São Paulo. Boletim do Instituto de Pesca, 33: 221-228.) associated with environments with higher turbidity, thus requiring a greater auditory than visual capacity. Another factor is the detection of predators by hearing (Popper et al., 2005Popper, A.N.; Ramcharitar, J. & Campana, S.E. 2005. Why otoliths? Insights from inner ear physiology and fisheries biology. Marine and Freshwater Research, 56: 497-504.), as M. americanus is prey to several species of top predators, including marine mammals (Di Beneditto & Siciliano, 2007Di Beneditto, A.P.M. & Siciliano, S. 2007. Stomach contents of the marine tucuxi dolphin (Sotalia guianensis) from Rio de Janeiro, south-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom, 87: 253-254.; Bornatowski et al., 2014Bornatowski, H.; Braga, R.R.; Abilhôa, V. & Corrêa, M.F.M. 2014. Feeding ecology and trophic comparisons of six shark species in a coastal ecosystem off southern Brazil. Journal of Fish Biology, 85: 246-263.; Miotto et al., 2017Miotto, M.; Carvalho, B.M. & Spach, H.L. 2017. Does the closed fishing season influence the ichthyofauna consumed by Larus dominicanus? Brazilian Journal Oceanography, 65: 9-18.) its keen hearing favors its escape. Finally, a greater auditory capacity facilitates intraspecific recognition for mating, essential for M. americanus that forms reproductive aggregates through vocalization (Ramcharitar et al., 2006Ramcharitar, J.; Gannon, D.P. & Popper, A.N. 2006. Bioacoustics of Fishes of the Family Sciaenidae (Croakers and Drums. Transactions of the American Fisheries Society, 135: 1409-1431.).

Otoliths of males and females of M. americanus showed a sexual dimorphism in both the contour and the SRS index. The species of the family Sciaenidae are known to have the ability to vocalize, and this vocalization may be for defense of the territory or for reproduction (Montie et al., 2015Montie, E.W.; Vega, S. & Powell, M. 2015. Seasonal and spatial patterns of fish sound production in the May River, South Carolina. Transactions of the American Fisheries Society, 144: 705-716.). In some species, male and female vocalize, but in the reproductive age, males increase the intensity of vocalization (Tellechea et al., 2011Tellechea, J.S.; Norbis, W.; Olsson, D. & Fine, M.L. 2011. Calls of the black drum (Pogonias cromis: Sciaenidae): geographical differences in sound production between northern and southern hemisphere populations. Journal of Experimental Zoology, 315: 48-55.; Parmentier et al., 2014Parmentier, E.; Tock, J.; Falguiére, J.C. & Beauchaud, M. 2014. Sound production in Sciaenops ocellatus: Preliminary study for the development of acoustic cues in aquaculture. Aquaculture, 432: 204-211.). In addition to the behavioral differences, there is a morphological distinction in the size of the sound muscle between the sexes (Ramcharitar et al., 2006Ramcharitar, J.; Gannon, D.P. & Popper, A.N. 2006. Bioacoustics of Fishes of the Family Sciaenidae (Croakers and Drums. Transactions of the American Fisheries Society, 135: 1409-1431.; Tellechea & Norbis, 2012Tellechea, J.S. & Norbis, W. 2012. Sexual Dimorphism in Sound Production and Call Characteristics in the Striped Weakfish Cynoscion guatucupa. Zoological Studies, 51: 946-955.). The sexual dimorphism in otoliths of M. americanus may be a result of the need to capture sound since females are attracted to males for mating by their vocalization. Species that form reproductive aggregates become more susceptible to fishing in this period, causing impacts for future cuts to withdrawals from individuals able to spawn.

As well as M. americanus, other species of demersal fish have demonstrated sexual dimorphism in the sagitta otolith contour (Mille et al., 2015Mille, T.; Mahe, K.; Villanueva, M.C.; De Pontual, H. & Ernande, B. 2015. Sagitta otolith morphogenesis asymmetry in marine fishes. Journal of Fish Biology, 87: 646-663.; Bose et al., 2016Bose, A.P.H.; Adragna, J.B. & Balshine, S. 2016. Otolith morphology varies between populations, sexes and male alternative reproductive tactics in a vocal toadfish Porichthys notatus. Journal of Fish Biology, 1-15.). However, the small number of studies that verify the existence or not of sexual dimorphism in the otoliths of demersal species makes it impossible to conclude that this is a characteristic of demersal fish.

Both shape indices and contour analysis demonstrated significant differences in otoliths between young females and small adult females of M. americanus. With these analyses, the influence of the reproductive process on the otolith shape of the females of M. americanus is confirmed by the reduction of energy invested in somatic growth for the formation of oocytes and a change in the rates of calcium deposition on the otolith, once this element is of great importance for oocyte formation.

From the results of this study it is possible to conclude that M. americanus presents an ontogenetic variation of the otolith shape. There is a sexual dimorphism between female and male otoliths, suggesting that these sexual variations are related to sound uptake into the formation of reproductive aggregates. Stages of life also showed differences in the shape of otoliths suggesting an influence of reproduction and somatic growth in this structure.

ACKNOWLEDGMENTS

The authors are grateful for funding from the project CAFP-BA/SPU and 292/14 UFPR/Fundação Araucária. They also thank CONICET (PIP112-20120100543CO), Universidad de Buenos Aires (UBACYT 20020150100052BA), Agencia Nacional de Promoción Científica y Técnica (ANPCyT PICT 2015-1823); CNPQ for the PhD degree scholarship to the first author (CNPQ 141267/2015-1), LAFMA (CEM-UFPR) for the stereomicroscope and the Olympus DP71 camera and the Centro de Microscopia Eletrônica (CME-UFPR) for the micrographs. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES) - Finance Code 001.

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  • 1
    Edited by: Fernando César Paiva Dagosta
  • Published with the financial support of the “Programa de Apoio às Publicações Científicas Periódicas da USP”

Publication Dates

  • Publication in this collection
    16 Mar 2020
  • Date of issue
    2020

History

  • Received
    21 May 2019
  • Accepted
    16 Dec 2019
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