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Sagitta otolith of three demersal species in a tropical environment

Abstract

The objective of this study was to describe the morphology and morphometry of saggitta otoliths of Polydactylus virginicus, Menticirrhus cuiaranensis and Conodon nobilis in a tropical environment. Fishes were caught with rod and reel in competitive fishing events promoted in 2014-2015 along the coast of Sergipe. A total of 174 pairs of sagitta otoliths of P. virginicus, 181 of M. cuiaranensis and 77 of C. nobilis was extracted. In general, the sagitta otoliths of all three species analyzed here presented different morphology and shape indices. The permutational multivariate analysis of variance (PERMANOVA) demonstrated significant differences among species and ontogenetic phases within each species using morphometry and shape indices. The linear discriminant analysis (LDA) presented a 98.3% correct reclassification of the otoliths by species.

Keywords.
Conodon nobilis; Menticirrhus cuiaranensis; Polydactylus virginicus; Ontogenetic variation; Shape indices

INTRODUCTION

Otoliths are calcium carbonate precipitated primarily as aragonite structures, present in the inner ear of fishes in three pairs: sagittae, asterisci and lapilli (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. http://doi.org/10.1071/MF04267
http://doi.org/10.1071/MF04267...
). They are metabolically inert, i.e., there is no chemical alteration or reabsorption after their formation. These structures assist the hearing and perception of the external environment (Ladich & Schulz-Mirbach, 2016Ladich, F. & Schulz-Mirbach, T. 2016. Diversity in Fish Auditory Systems: One of the Riddles of Sensory Biology. Frontiers in Ecology and Evolution, 4: 1-27. http://doi.org/10.3389/fevo.2016.00028
http://doi.org/10.3389/fevo.2016.00028...
). Otoliths are excellent tools for various studies of fish populations such as: habitat use and connectivity between populations using the chemistry of the otolith (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. http://doi.org/10.3989/scimar.04218.31A
http://doi.org/10.3989/scimar.04218.31A...
; Maciel et al., 2020Maciel, T.R.; Avigliano, E.; Carvalho, B.M.; Miller, N. & Vianna, M. 2020. Population structure and habitat connectivity of Genidens genidens (Siluriformes) in tropical and subtropical coasts from Southwestern Atlantic. Estuarine, Coastal and Shelf Science, 242: 1-11. http://doi.org/10.1016/j.ecss.2020.106839
http://doi.org/10.1016/j.ecss.2020.10683...
), environmental stress indicated by the deposition of vaterita (Carvalho et al., 2019aCarvalho, B.M.; Volpedo, A.V.; Albuquerque, C.Q. & Fávaro LF. 2019a. First record of anomalous otoliths of Menticirrhus americanus in the South Atlantic. Journal of Applied Ichthyology, 35: 1286-1291. http://doi.org/10.1111/JAI.13979
http://doi.org/10.1111/JAI.13979...
; Holmberg et al., 2019Holmberg, R.J.; Wilcox-Freeburg, E.; Rhyne, A.L.; Tlusty, M.F.; Stebbins, A.; Nye, S.W.; Honig, A.; Johnston, A.E.; San Antonio, C.M.; Bourque, B. & Hannigan, R.E. 2019. Ocean acidification alters morphology of all otolith types in Clark’s anemonefish (Amphiprion clarkii). PeerJ, 7: 1-24. http://doi.org/10.7717/peerj.6152
http://doi.org/10.7717/peerj.6152...
), and age and growth (Soeth et al., 2018Soeth, M.; Fávaro, L.F.; Spach, H.L.; Daros, F.A.; Woltrich, A.E. & Correia, A.T. 2018. Age, growth, and reproductive biology of the Atlantic spadefish Chaetodipterus faber in southern Brazil. Ichthyological Research, 211: 81-90. http://doi.org/10.1007/s10228-018-0663-2
http://doi.org/10.1007/s10228-018-0663-2...
; Maciel et al., 2018Maciel, T.R.; Vaz-dos-Santos, A.M. & Vianna, M. 2018. Can otoliths of Genidens genidens (Cuvier 1829) (Siluriformes: Ariidae) reveal differences in life strategies of males and females? Environmental Biology of Fishes, 201: 1589-1598. http://doi.org/10.1007/s10641-018-0804-5
http://doi.org/10.1007/s10641-018-0804-5...
).

Many studies correlate the ontogenetic developments of otoliths to life history and changes in habitat use as distribution in the water column (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. http://doi.org/10.1111/j.1095-8649.2004.00558
http://doi.org/10.1111/j.1095-8649.2004....
; Assis et al., 2020Assis, I.O.; Silva, V.E.L; Souto-Vieira, D.; Lozano, A.P.; Volpedo, A.V. & Fabré, N.N. 2020. Ecomorphological patterns in otoliths of tropical fishes: assessing trophic groups and depth strata preference by shape. Environmental Biology of Fishes, 103: 349-361. http://doi.org/10.1007/s10641-020-00961-0
http://doi.org/10.1007/s10641-020-00961-...
). Taylor et al. (2020Taylor, M.D.; Fowler, A.M. & Suthers, I.M. 2020. Insights into fish auditory structure-function relationships from morphological and behavioural ontogeny in a maturing sciaenid. Marine Biology, 167: 1-11. http://doi.org/10.1007/s00227-019-3619-9
http://doi.org/10.1007/s00227-019-3619-9...
) correlated changes in the morphology and morphometry of the otoliths of Argyrosomus japonicus with the segregation of habitat use of juveniles and adults. The morphology and morphometry of otoliths may present sexual variation, as observed in Atherinella brasiliensis (Quoy & Gaimard, 1825), Micromesistius australis (Norman, 1937) and Porichthys notatus (Girard, 1854) (Carvalho & Correa, 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. Tropical Oceanography, 42: 54-59.; Leguá et al., 2013Leguá, 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(3): 479-489. http://doi.org/10.3856/vol41-issue3-fulltext-11
http://doi.org/10.3856/vol41-issue3-full...
; 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, 90(1): 1-15. http://doi.org/10.1111/jfb.13187
http://doi.org/10.1111/jfb.13187...
), as well as before and after the first maturity within the same species (Carvalho et al., 2020Carvalho, B.M.; Volpedo, A.V. & Fávaro, L.F. 2020. Ontogenetic and sexual variation in the sagitta otolith of Menticirrhus americanus (Teleostei; Sciaenidae) (Linnaeus, 1758) in a subtropical environment. Papéis Avulsos de Zoologia, 60: 1-12. http://doi.org/10.11606/1807-0205/2020.60.09
http://doi.org/10.11606/1807-0205/2020.6...
). The intraspecific morphologies and morphometric patterns of otoliths make them an important tool for studies of trophic ecology of ichthyophagous species (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 of Oceanography, 65: 9-18. http://doi.org/10.1590/S1679-87592017112206501
http://doi.org/10.1590/S1679-87592017112...
; Carvalho et al., 2019bCarvalho, B.M.; Spach, H.L.; Vaz-dos-Santos, A.M. & Volpedo, A.V. 2019b. Otolith shape index: Is it a tool for trophic ecology studies? Journal of the Marine Biological Association of the United Kingdom, 99(7): 1675-1682. http://doi.org/10.1017/S0025315419000729
http://doi.org/10.1017/S0025315419000729...
). Some of the species identified as preys are also exploited in artisanal and recreational fisheries (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 Pesca, 37: 247-260.; Freire et al., 2017Freire, K.M.F.; Oliveira, C.S. & da Rosa, L.C. 2017. Morphometric analysis of otoliths of juvenile crucifix sea catfish Sciades proops (Valenciennes, 1840). Journal of Applied Ichthyology, 485-490. http://doi.org/10.1111/jai.13321
http://doi.org/10.1111/jai.13321...
; Passarone et al., 2019Passarone, R.; Aparecido, K.C.; Eduardo, L.N.; Lira, A.S.; Silva, L.V.S.; Justino, A.K.S.; Craveiro, C.; Silva, E.F. & Frédou, F.L. 2019. Ecological and conservation aspects of bycatch fishes: An evaluation of shrimp fisheries impacts in Northeastern Brazil. Brazilian Journal of Oceanography, 67: 1-11. http://doi.org/10.1590/S1679-87592019029106713
http://doi.org/10.1590/S1679-87592019029...
). Polydactylus virginicus (Linnaeus, 1758), Menticirrhus cuiaranensis (Marceniuk et al., 2020Marceniuk, A.P.; Caires, R.A.; Rotundo, M.M.; Cerqueira, N.N.C.D.; Siccha-Ramirez, R.; Wosiacki, W.B. & Oliveira, C. 2020. Taxonomic revision of the Menticirrhus americanus (Linnaeus, 1758) and M. littoralis (Holbrook, 1847) (Percomorphacea: Sciaenidae) species complexes from the western Atlantic. Zootaxa, 4822(3): 301-333.) and Conodon nobilis (Linnaeus, 1758) are examples of species exploited by recreational fishers (Freire et al., 2017Freire, K.M.F.; Oliveira, C.S. & da Rosa, L.C. 2017. Morphometric analysis of otoliths of juvenile crucifix sea catfish Sciades proops (Valenciennes, 1840). Journal of Applied Ichthyology, 485-490. http://doi.org/10.1111/jai.13321
http://doi.org/10.1111/jai.13321...
) and are usually described as food items in the diet of ichthyophagous species (Tavares & Di Beneditto, 2017Tavares, M.T.M. & Di Beneditto, A.P.M. 2017. Feeding habits and behaviour of Bagre bagre and Genidens barbus, two ariid catfishes (Pisces: Siluriformes) from southeastern Brazil. Journal of Threatened Taxa, 9(10): 10771-10775. http://doi.org/10.11609/jott.3758.9.10.10771-10775
http://doi.org/10.11609/jott.3758.9.10.1...
). Those species are demersal and distributed in the Southwestern Atlantic Ocean (Menezes & Figueiredo, 1980Menezes, N.A. & Figueiredo, J.L. 1980. Manual de peixe marinhos do sudeste do Brasil Teleostei I. São Paulo, Museu de Zoologia, Universidade de São Paulo. v. 3, p. 42-59.; Froese & Pauly, 2021Froese, R. & Pauly, D. 2021. FishBase. World Wide Web electronic publication. www.fishbase.org, version (01/2021).
www.fishbase.org...
). Menticirrhus cuiaranensis and C. nobilis are benthophagous (Lira et al., 2019Lira, A.S.; Viana, A.P.; Eduardo, L.N.; Lucena-Fredóu, F. & Frédou, T. 2019. Population structure, size at first sexual maturity, and feeding ecology of Conodon nobilis (Actinopterygii: Perciformes: Haemulidae) from the coasts of Pernambuco, north-eastern Brazil. Acta Ichthyologica et Piscatoria, 49(4): 389-398. http://doi.org/10.3750/AIEP/02578
http://doi.org/10.3750/AIEP/02578...
) whereas P. virginicus is zooplanktivore (Medeiros et al., 2017Medeiros, A.P.M.; Xavier, J.H.A. & Rosa, I.M.L. 2017. Diet and trophic organization of the fish assemblage from the Mamanguape River Estuary, Brazil. Latin American Journal of Aquatic Research, 45(5): 879-890. http://doi.org/10.3856/vol45-issue5-fulltext-2
http://doi.org/10.3856/vol45-issue5-full...
).

Several studies have described the morphology and morphometry of otoliths of species important for artisanal and recreational fisheries in southeastern-southern Brazil (Siliprandi et al., 2014Siliprandi, C.C.; Rossi-Wongtschowski, C.L.D.B.; Brenha-Nunes, 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 of Oceanography, 62: 28-101. http://doi.org/10.1590/S1679-875920150988064(sp1)
http://doi.org/10.1590/S1679-87592015098...
; Brenha-Nunes et al., 2016Brenha-Nunes, M.R.; Santificetur, C.; Conversani, V.R.M.; Giaretta, M.B.; Rossi-Wongtschowski C.L.D.B. & Siliprandi C.C. 2016. Atlas of marine bony fish otoliths (sagittae) of southeastern-southern Brazil. Part IV: Perciformes (Centropomidae, Acropomatidae, Serranidae, Priacanthidae, Malacanthidae, Pomatomidae, Carangidae, Lutjanidae, Gerreidae and Haemulidae). Brazilian Journal of Oceanography, 64 (spec. 1): 23-75. http://doi.org/10.1590/s1679-87592017134306503
http://doi.org/10.1590/s1679-87592017134...
; Maciel et al., 2019Maciel, T.R.; Vaz-dos-Santos, A.M.; Barradas, J.R.D.S. & Vianna M. 2019. Sexual dimorphism in the catfish Genidens genidens (Siluriformes: Ariidae) based on otolith morphometry and relative growth. Neotropical Ichthyology, 17(1): 1-8. http://doi.org/10.1590/1982-0224-20180101
http://doi.org/10.1590/1982-0224-2018010...
; Dal Negro et al., 2021Dal Negro, T.; Santos, P.P.; Tutui, S.L.S. & Tomás, A.R.G. 2021. Coastal recreational fisheries: A case study in the southeastern Brazil. Regional Studies in Marine Science, 42: 101652. http://doi.org/10.1016/j.rsma.2021.101652
http://doi.org/10.1016/j.rsma.2021.10165...
). Conversely, few studies have been conducted in northeastern Brazil, making it impossible future studies of connectivity or fishing stocks for species with wide distribution along the Brazilian coast (Freire et al., 2017Freire, K.M.F.; Oliveira, C.S. & da Rosa, L.C. 2017. Morphometric analysis of otoliths of juvenile crucifix sea catfish Sciades proops (Valenciennes, 1840). Journal of Applied Ichthyology, 485-490. http://doi.org/10.1111/jai.13321
http://doi.org/10.1111/jai.13321...
; Assis et al., 2020Assis, I.O.; Silva, V.E.L; Souto-Vieira, D.; Lozano, A.P.; Volpedo, A.V. & Fabré, N.N. 2020. Ecomorphological patterns in otoliths of tropical fishes: assessing trophic groups and depth strata preference by shape. Environmental Biology of Fishes, 103: 349-361. http://doi.org/10.1007/s10641-020-00961-0
http://doi.org/10.1007/s10641-020-00961-...
; Bot et al., 2020Bot, R.L.N.; Carvalho, B.M.; Schwarz-Júnior, R. & Spach, H.L. 2020. Ontogenetic variation in the sagitta otolith of Centropomus undecimalis (Actinopterygii: Perciformes: Centropomidae) in a tropical estuary. Acta Ichthyologica et Piscatoria, 50(4): 433-443. http://doi.org/10.3750/AIEP/03014
http://doi.org/10.3750/AIEP/03014...
). Thus, this study was conducted with the objective of describing the morphology and morphometry of sagitta otoliths of P. virginicus, M. cuiaranensis and C. nobilis, and assessing the occurrence of ontogenetic changes to serve as basis for future studies related to diet composition and connectivity between populations.

MATERIAL AND METHODS

Samplings were performed between March 2014 and August 2015 in distinct beaches along the coast of the state of Sergipe, in northeastern Brazil (Fig. 1). Recreational fishers used rod, reel, and hook with natural bait during these events (Freire et al., 2017Freire, K.M.F.; Oliveira, C.S. & da Rosa, L.C. 2017. Morphometric analysis of otoliths of juvenile crucifix sea catfish Sciades proops (Valenciennes, 1840). Journal of Applied Ichthyology, 485-490. http://doi.org/10.1111/jai.13321
http://doi.org/10.1111/jai.13321...
). The specimens caught were identified, measured for total length and total weight (TL, in centimeters and W, in grams, respectively). Power relations were also estimated between total length and total weight (W = a∙TLb) (positive allometry, b > 3; negative allometry, b < 3; and isometry, b = 3; Froese, 2006Froese, R. & Pauly, D. 2021. FishBase. World Wide Web electronic publication. www.fishbase.org, version (01/2021).
www.fishbase.org...
). The specimens were separated into six length classes (5.1-10; 10.1-15; 15.1-20; 20.1-25; 25.1-30; 30.1-35 cm) to test for ontogenetic variation. Sagitta otoliths were washed, dried, and stored separately in small paper envelopes. Voucher specimens are deposited in the collection of the “Acervo Zoológico da Universidade Santa Cecília” under the numbers AZUSC-UNISANTA n. 5155, 5169, and 5935.

Figure 1
Map of the coastal region of the state of Sergipe showing all the beaches where samples were collected during competitive fishing events in 2014-2015.

Morphology and morphometry of otolith

The identification of otolith shape, position, type and shape of the sulcus acusticus, shape of the cauda, and ostium type was performed according to Corrêa & Vianna (1992Corrêa, M.F.M. & Viana, M.S. 1992. Catálogo dos otólitos sagitta de Sciaenidae (Osteichthyes - Perciformes) do litoral do estado do Paraná, Brasil. Nerítica, 7: 13-41.), 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. http://doi.org/10.3989/scimar.2008.72s17
http://doi.org/10.3989/scimar.2008.72s17...
), and Volpedo & Vaz-dos-Santos (2015Volpedo, A.V. & Vaz-dos-Santos, A.M. 2015. Métodos de estudios con otolitos: principios y aplicaciones. INPA CONICET UBA, Ciudad Autónoma de Buenos Aires.). The otolith length (OL, greater longitudinal distance in mm) and height (OH, greater perpendicular distance in mm) were measured (Fig. 2). Power relations were also estimated between otolith length (OL) and height (OH) and fish total length (TL): OL = a∙TLb and OH = a∙TLb. The following otolith shape indices were used to verify the ontogenetic variation as well as variation among species: OL/TL, OH/OL × 100 (Volpedo & Echeverria, 2003Volpedo, A. & Echeverría, D.D. 2003. Ecomorphological Patterns of the Sagitta in Fish on the Continental Shelf off Argentine. Fisheries Research, 60: 551-560. http://doi.org/10.1016/S0165-7836(02)00170-4
http://doi.org/10.1016/S0165-7836(02)001...
), and ellipticity [E = (OL - OH)/(OL + OH)] (Tuset et al., 2003Tuset, V.M.; Lozano, I.J.; Gonzalez, J.A.; Pertusa, J.F. & Garcia-Diaz, M.M. 2003. Shape Indices to Identify Regional Differences in Otolith Morphology of Comber, Serranus Cabrilla (L., 1758). Journal Applied Ichthyology, 19: 88-93. http://doi.org/10.1046/j.1439-0426.2003.00344.x
http://doi.org/10.1046/j.1439-0426.2003....
).

Figure 2
Length and height of sagittae otoliths for: (A) Polydactylus virginicus; (B) Menticirrhus cuiaranensis; and (C) Conodon nobilis.

Statistical analysis

The morphometry and shape indices did not meet the assumptions required for parametric tests in all three species analyzed here (Shapiro-Wilk: p < 0.05; Bartlett’s test: p < 0.05). Hence, a Permutational Analysis of Variance (PERMANOVA) was applied to verify ontogenetic differences within species and shape variation among species using the morphometry and shape indices for all three species. A linear discriminant analysis (LDA) was performed to verify the percentage of correct reclassification of otoliths among the three species analyzed (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. http://doi.org/10.1111/j.1420-9101.2004.00763.x
http://doi.org/10.1111/j.1420-9101.2004....
). All statistical analyses were performed using the R software (R Core Team, 2020The R Project for Statistical Computing (R Core Team). 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org.
https://www.r-project.org...
) 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 487 individuals of P. virginicus (TL = 7.2 to 27.5 cm; n = 229), M. cuiaranensis (TL = 12.5 to 35.5 cm; n = 182), and C. nobilis (TL = 7.4 to 33.5 cm, n = 76) were analyzed (Fig. 3). The morphological analysis of the otoliths indicated interspecific variation (Table 1), except for the shape of the sulcus acusticus and cauda, which are similar for all three species. The position and type of the sulcus acusticus are similar for P. virginicus and C. nobilis, i.e., median and ostial. Menticirrhus cuiaranensis showed on rostrum and P. virginicus and C. nobilis showed a small and underdeveloped rostrum.

Figure 3
Frequency distribution of the total length (cm) of Polydactylus virginicus, Menticirrhus cuiaranensis and Conodon nobilis sampled in a tropical environment in Southwestern Atlantic.

Table 1
Morphological classification of otoliths for Polydactylus virginicus, Menticirrhus cuiaranensis and Conodon nobilis of a tropical environment.

Morphometry and indices demonstrated ontogenetic variation within the three species analyzed here (Fig. 4). The otoliths of C. nobilis tend to be more rounded along the ontogeny and the otoliths of M. cuiaranensis and P. virginicus tend to be more elongated as the ontogenetic development occurs (Fig. 4D). The otoliths of the three species show greater growth in the anteroposterior axis along the ontogeny (Fig. 4E). The results of the PERMANOVA (F = 807.1; p < 0.0001) indicated significant differences in the morphometry of otolith and shape indices among species.

Figure 4
Box plot (mean and standard deviation) of morphometric parameters and shape indices of the otolith sagitta of Polydactylus virginicus, Menticirrhus cuiaranensis and Conodon nobilis per class of total length: (A) otolith length (OL), (B) otolith height (OH), (C) Aspect ratio OL/TL, (D) Aspect ratio (OH/OL) × 100 and (E) ellipticity.

Both P. virginicus and M. cuiaranensis presented positive body allometry when analyzing the weight-length relationship (b = 3.233 and 3.159, respectively; Fig. 5). On the other hand, C. nobilis showed body isometry (b = 3.022), with an increase in its body weight proportional to the cube of its length. At the same time, C. nobilis was the only species, among all analyzed, with otoliths presenting a strong positive allometry (b = 3.744; Fig. 5).

Figure 5
Length-weight relationship for (A) Polydactylus virginicus, (B) Menticirrhus cuiaranensis, and (C) Conodon nobilis; otolith length vs fish total length for (D) Polydactylus virginicus, (E) Menticirrhus cuiaranensis, and (F) Conodon nobilis; and otolith height vs fish total length for (G) Polydactylus virginicus, (H) Menticirrhus cuiaranensis, and (I) Conodon nobilis.

The LDA showed a variation in the shape of the sagitta otoliths: M. cuiaranensis presents otoliths distributed along axis 1 for presenting more elongated otoliths; and P. virginicus and C. nobilis are distributed along axis 2, which better explains the variability of the more rounded otoliths (Fig. 6). The LDA presented a 98.3% correct reclassification of the otoliths by species (Table 2).

Figure 6
Scatterplot of the linear discriminant analysis of morphometry and shape indices of the sagitta otolith of Polydactylus virginicus, Menticirrhus cuiaranensis and Conodon nobilis.

Table 2
Reclassification of the sagitta otoliths for Polydactylus virginicus, Menticirrhus cuiaranensis and Conodon nobilis obtained through the linear discriminant analysis (LDA).

DISCUSSION

In general, the sagitta otoliths of all three species analyzed here presented different morphology. However, similarities were observed in the shape of the sulcus acusticus and cauda for all of them, and also in the position and type of sulcus acusticus for P. virginicus and C. nobilis. Even though P. virginicus, M. cuiaranensis and C. nobilis are demersal species, the otolith shape is different among them (rectangular, bullet shaped, and oval, respectively). For Gauldie (1988Gauldie, R.W. 1988. Function, form and time-keeping properties of fish otoliths. Comparative Biochemistry and Physiology - Parte A: Molecular & Integrative Physiology, 91(2): 395-402.), it is the shape of the sulcus, and not the otolith shape, that is associated with acoustic sensitivity, which in turn depends on the habitat. However, this author did not present details on how this association works. In the present study, the shape of the sulcus acusticus was heterosulcoid for all three demersal species analyzed. The exact mechanism that relates the sulcus shape with higher acoustic sensitivity would have to be better investigated in future studies. Additionally, 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. http://doi.org/10.1111/j.1095-8649.2004.00558
http://doi.org/10.1111/j.1095-8649.2004....
) pointed out that Sciaenidae and Haemulidae families, which include M. cuiaranensis and C. nobilis, respectively, belong to groups specialized in sound production. This could be associated with relatively large otoliths for better acoustic communication.

Our study was the first to evaluate the ontogenetic variation of otoliths for P. virginicus, M. cuiaranensis and C. nobilis using shape indices. Only the OH/OL x100% demonstrated a change in trend associated with ontogenetic variation mainly for P. virginicus and C. nobilis. According to Volpedo & Echeverria (2003Volpedo, A. & Echeverría, D.D. 2003. Ecomorphological Patterns of the Sagitta in Fish on the Continental Shelf off Argentine. Fisheries Research, 60: 551-560. http://doi.org/10.1016/S0165-7836(02)00170-4
http://doi.org/10.1016/S0165-7836(02)001...
), values of aspect ratio between 21% and 96% and the absence of rostrum indicate species associated with a soft bottom. Conversely, species associated with a consolidated substrate show values between 41% and 67% and a small rostrum. The aspect ratio and the presence of a small rostrum indicate that P. virginicus and C. nobilis inhabit consolidated and soft substrates, respectively (Brenha-Nunes et al., 2016Brenha-Nunes, M.R.; Santificetur, C.; Conversani, V.R.M.; Giaretta, M.B.; Rossi-Wongtschowski C.L.D.B. & Siliprandi C.C. 2016. Atlas of marine bony fish otoliths (sagittae) of southeastern-southern Brazil. Part IV: Perciformes (Centropomidae, Acropomatidae, Serranidae, Priacanthidae, Malacanthidae, Pomatomidae, Carangidae, Lutjanidae, Gerreidae and Haemulidae). Brazilian Journal of Oceanography, 64 (spec. 1): 23-75. http://doi.org/10.1590/s1679-87592017134306503
http://doi.org/10.1590/s1679-87592017134...
; Santificetur et al., 2017Santificetur, C.; Conversani, V.R.M.; Brenha-Nunes, M.R.; Giaretta, M.B.; Siliprandi, C.C. & Rossi-Wongtschowski, C.L.D.B. 2017. Atlas of marine bony fish otoliths (sagittae) of Southeastern-Southern Brazil. Part V: Perciformes (Sparidae, Sciaenidae, Polynemidae, Mullidae, Kyphosidae, Chaetodontidae, Mugilidae, Scaridae, Percophidae, Pinguipedidae, Blenniidae, Gobiidae, Ephippidae, Sphyraenidae, Gempylidae, Trichiuridae, Scombridae, Ariommatidae, Stromateidae and Caproidae). Brazilian Journal of Oceanography, 65(2): 201-257. http://doi.org/10.1590/s1679-87592017131006502
http://doi.org/10.1590/s1679-87592017131...
). The absence of rostrum indicates that M. cuiaranensis lives in environments of unconsolidated sediment as mentioned for other species of the same genus Menticirrhus (Carvalho et al., 2020Carvalho, B.M.; Volpedo, A.V. & Fávaro, L.F. 2020. Ontogenetic and sexual variation in the sagitta otolith of Menticirrhus americanus (Teleostei; Sciaenidae) (Linnaeus, 1758) in a subtropical environment. Papéis Avulsos de Zoologia, 60: 1-12. http://doi.org/10.11606/1807-0205/2020.60.09
http://doi.org/10.11606/1807-0205/2020.6...
). Polydactylus virginicus showed a reduction in the aspect ratio in specimens larger than 15 cm TL, when this species starts the maturation process (Freire et al., 2020Freire, K.M.F.; Nascimento, F.P. & Rocha, G.R.A. 2020. Shore-based competitive recreational fisheries in southern Bahia, Brazil: A baseline study. Marine and Fishery Sciences, 33: 183-203. http://doi.org/10.47193/mafis.3322020301103
http://doi.org/10.47193/mafis.3322020301...
). This may indicate a change in habitat after maturity between juveniles and adults, or in swimming capacity associated with feeding change. On the other hand, the aspect ratio of the otoliths from C. nobilis increased until specimens were 20 cm TL long and kept stable onwards. Note that the length at first maturity for this species is about 21 cm TL in a neighboring area (da Silva et al., 2019da Silva, V.E.L.; Vieira, D.S.; Teixeira, E.C.; Ferreira, A.C.L.; Assis, I.O.; Rangely, J. & Fabré, N.N. 2019. Maturity, fecundity and reproductive cycle of Conodon nobilis (Actinopterygii: Perciformes: Haemulidae) in tropical waters of the Atlantic Ocean. Acta Ichthyologica et Piscatoria, 49(3): 235-242. http://doi.org/10.3750/AIEP/02597
http://doi.org/10.3750/AIEP/02597...
). Here, again, a change in habitat for juveniles and adults may be occurring. The otoliths of Menticirrhus are elongated (Siliprandi et al., 2014Siliprandi, C.C.; Rossi-Wongtschowski, C.L.D.B.; Brenha-Nunes, 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 of Oceanography, 62: 28-101. http://doi.org/10.1590/S1679-875920150988064(sp1)
http://doi.org/10.1590/S1679-87592015098...
; Carvalho et al., 2020Carvalho, B.M.; Volpedo, A.V. & Fávaro, L.F. 2020. Ontogenetic and sexual variation in the sagitta otolith of Menticirrhus americanus (Teleostei; Sciaenidae) (Linnaeus, 1758) in a subtropical environment. Papéis Avulsos de Zoologia, 60: 1-12. http://doi.org/10.11606/1807-0205/2020.60.09
http://doi.org/10.11606/1807-0205/2020.6...
), as also observed for M. cuiaranensis in the present study, but no change was observed in the aspect ratio for the length range analyzed here.

According to Iizuka & Katayama (2008Iizuka, K. & Katayama, S. 2008. Otolith morphology of teleost fishes of Japan. Bulletin of Fisheries Research Agency, 25: 1-222.), demersal species present otoliths within two groups defined by their external shape: elongate (or elliptical) and orbicular (or ellipsoidal). This difference was evident for the three species analyzed here, with elliptical otoliths found in P. virginicus and M. cuiaranensis, and ellipsoidal in C. nobilis. Moreover, the former two species presented a positive allometry in the relationship between body weight and length, but negative when the same relationship was estimated for the otolith. On the other hand, C. nobilis presented body isometry, but a positive otolith allometry, which is related to the ellipsoidal shape of its sagitta otolith. Hence, otoliths of C. nobilis are disproportionately heavier than the other two species. One could hypothesize that C. nobilis presents higher acoustic sensitivity based on Lychakov & Rebane (2000Lychakov, D.V. & Rebane, Y.T. 2000. Otolith regularities. Hearing Research, 143(1-2): 83-102. http://doi.org/10.1016/S0378-5955(00)00026-5
http://doi.org/10.1016/S0378-5955(00)000...
), who stated that the heavier the otolith, the higher its acoustic sensitivity in lower frequency. This higher acoustic sensitivity should be further investigated in future studies involving C. nobilis.

The otolith shape is usually species-specific, but intraspecific geographic variation may occur due to environmental factors (Santos et al., 2017Santos, R.S.; Azevedo, M.C.C.; Albuquerque, C.Q. & Araújo, F.G. 2017. Different sagitta otolith morphotypes for the whitemouth croaker Micropogonias furnieri in the Southwestern Atlantic coast. Fisheries Research, 195: 222-229. http://doi.org/10.1016/j.fishres.2017.07.027
http://doi.org/10.1016/j.fishres.2017.07...
; Maciel et al., 2020Maciel, T.R.; Avigliano, E.; Carvalho, B.M.; Miller, N. & Vianna, M. 2020. Population structure and habitat connectivity of Genidens genidens (Siluriformes) in tropical and subtropical coasts from Southwestern Atlantic. Estuarine, Coastal and Shelf Science, 242: 1-11. http://doi.org/10.1016/j.ecss.2020.106839
http://doi.org/10.1016/j.ecss.2020.10683...
). The morphology and morphometry of the otoliths from P. virginicus and C. nobilis were analyzed in previous studies carried on southeastern-southern Brazil (Brenha-Nunes et al., 2016Brenha-Nunes, M.R.; Santificetur, C.; Conversani, V.R.M.; Giaretta, M.B.; Rossi-Wongtschowski C.L.D.B. & Siliprandi C.C. 2016. Atlas of marine bony fish otoliths (sagittae) of southeastern-southern Brazil. Part IV: Perciformes (Centropomidae, Acropomatidae, Serranidae, Priacanthidae, Malacanthidae, Pomatomidae, Carangidae, Lutjanidae, Gerreidae and Haemulidae). Brazilian Journal of Oceanography, 64 (spec. 1): 23-75. http://doi.org/10.1590/s1679-87592017134306503
http://doi.org/10.1590/s1679-87592017134...
; Santificetur et al., 2017Santificetur, C.; Conversani, V.R.M.; Brenha-Nunes, M.R.; Giaretta, M.B.; Siliprandi, C.C. & Rossi-Wongtschowski, C.L.D.B. 2017. Atlas of marine bony fish otoliths (sagittae) of Southeastern-Southern Brazil. Part V: Perciformes (Sparidae, Sciaenidae, Polynemidae, Mullidae, Kyphosidae, Chaetodontidae, Mugilidae, Scaridae, Percophidae, Pinguipedidae, Blenniidae, Gobiidae, Ephippidae, Sphyraenidae, Gempylidae, Trichiuridae, Scombridae, Ariommatidae, Stromateidae and Caproidae). Brazilian Journal of Oceanography, 65(2): 201-257. http://doi.org/10.1590/s1679-87592017131006502
http://doi.org/10.1590/s1679-87592017131...
), showing similar characteristics to specimens inhabiting northeastern Brazil. The applied methodology was not the most sensitive to determine contour variations that may show latitudinal influence. Several external factors can influence the otolith shape (Torres et al., 2000Torres, G.J.; Lombarte, A. & Morales-Nin, B. 2000. Variability of the sulcus acusticus in the sagittal otolith of the genus Merluccius (Merlucciidae). Fisheries Research, 46: 5-13. http://doi.org/10.1016/S0165-7836(00)00128-4
http://doi.org/10.1016/S0165-7836(00)001...
; 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): 1-7.; Avigliano et al., 2012Avigliano, E.; Tombari, A. & Volpedo A.V. 2012. ¿El otolito de pejerrey (Odontesthes bonariensis), refleja el estrés ambiental? Biología Acuática, 27: 9-15.), including beach hydrodynamics. However, no study has been conducted in Brazil correlating these two variables. Could the differences observed in the otoliths of the three species represent a response to the beach dynamics? Future studies of the morphology and morphometry of the otoliths of such demersal coastal species should try to correlate the beach hydrodynamics with the otolith shape.

ACKNOWLEDGMENTS

All authors would like to thank the Universidade Federal de Sergipe for the scholarship provided to the first author (COPES/UFS), to all recreational fishers from the Associação Sergipana de Pesca Amadora Bons Ventos (ASPA-BV) for donating their catch from fishing competitive events to be analyzed in this study, to Rodrigo Melins, Rafael Barbosa, Ana Cláudia dos Santos, and Osmir Fabiano for helping with sample processing, and to Daniel Assis and Roberto Schwarz for their comments on an earlier version of this manuscript. B.M.C. is thankful to the National Council for Scientific and Technological Development (CNPq 153090/2019-7).

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  • Published with the financial support of the "Programa de Apoio às Publicações Científicas Períodicas da USP"

Edited by

Edited by: Murilo Nogueira de Lima Pastana

Publication Dates

  • Publication in this collection
    28 July 2021
  • Date of issue
    2021

History

  • Received
    23 Mar 2021
  • Accepted
    14 May 2021
  • Published
    04 June 2021
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