Discriminating Scleromystax barbatus (Siluriformes: Callichthyidae) populations from Atlantic Rainforest streams employing otolith shape

Roger Henrique Dalcin¹ and Vinicius Abilhoa^1,2

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Abstract​

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Introduction​

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Atlantic Rainforest rivers and streams harbor a high taxonomic and functional fish fauna diversity (Abilhoa et al., 2011). Many fish species within this biome display restricted distributions, associated to the high number of independent hydrological drainages that arise in high altitudes and flow towards the Atlantic Ocean (Menezes et al., 2007). Both geological and ecological conditions have influenced the unique diversification patterns, genetic population structuring and high number of endemic fish species noted in this region (Torres, Ribeiro, 2009; Thomaz et al., 2015).

The Brazilian Atlantic Rainforest biome is one of the most biologically rich, albeit threatened, biodiversity hotspot (Myers et al., 2000). Despite their wide geographical range throughout the Brazilian coast at almost 30° of latitude, after five centuries of human occupation less than 7% of original forests remain, now comprising only fragments surrounded by open-habitat matrices, such as agricultural and urban landscapes (Ribeiro et al., 2009).

Due to the isolating effect of mountain ranges on the geographic distribution of fishes that occur coastal Atlantic Rainforest rivers, several dispersal-vicariance mechanisms and hypotheses based on headwater stream capture and isolation/connection due to marine transgressions and regressions have been proposed (Ribeiro, 2006; Roxo et al., 2014; Thomaz, Knowles, 2018). Paleodrainage connections between coastal drainages have been used to explain the current distribution and genetic diversity of many fish populations in this region (Lima et al., 2016; Thomaz et al., 2017; Pio, Carvalho, 2021; Souto-Santos et al., 2022).

Species belonging to the Scleromystax Günther, 1864 genus (Siluriformes, Callichthyidae, Corydoradinae), popularly known as banded coridoras, are geographically widespread throughout coastal Atlantic Rainforest rivers (Britto, 2003; Britto et al., 2016). This monophyletic genus includes six species of small armored-catfish, namely S. barbatus (Quoy & Gaimard, 1824), S. macropterus (Regan, 1913), S. prionotos (Nijssen & Isbrücker, 1980), S. salmacis Britto & Reis, 2005, S. reisi Britto, Fukakusa & Malabarba, 2016 and S. virgulatus (Nijssen & Isbrücker, 1980). The banded coridoras S. barbatus exhibits a relatively broad distribution area through coastal rivers basins off southern and southeastern Brazil, from the Paraíba do Sul River basin to the Itapocu River basin (Menezes et al., 2007). This species differs from its congeners by the presence of dark brown blotches, often coalesced, extending from almost the entire dorsolateral body plates towards the base of caudal fin, displaying irregular small dark brown blotches distributed over the head (Oyakawa et al., 2006). It is mostly found in small groups inhabiting shallow stream portions, feeding on benthic invertebrates while moving and probing the substrate (Aranha et al., 1998; Gonçalves, Cestari, 2013). Molecular genetic variations within S. barbatus populations in southern Brazil indicate that this species is an interesting model for phylogeographic studies (Tschá et al., 2017).

Studies concerning evolutionary and biogeographic history effects on Atlantic Rainforest freshwater fish distributions have revealed that many widely distributed species display high genetic divergences (Torres, Ribeiro, 2009; Thomaz et al., 2017; Souza et al., 2018), often with low morphological variations between geographically isolated populations, indicating that the ichthyofauna in this region is much more diverse than previously thought. Therefore, an ongoing need to explore additional methodological approaches to address issues such as species identification, speciation, geographic variation, structured genetic variation, and phylogeny, is paramount (Padial et al., 2010; Garavello et al., 2021; Ibañez et al., 2022).

Otoliths, commonly known as earstones, are calcareous structures positioned in the inner ear of teleost fish, in close association with the sensorial macula, whose main functions comprise hearing and gravity perception (Platt, Popper, 1981). Three pairs of otoliths are present, the sagittae, lapillus, and asteriscus, which in many cases, display a species-specific morphology (Campana, 1999; Mendoza, 2006). The saccular otolith, sagitta, is largest in most teleosts, and the lagenar otolith, asteriscus, is largest in most ostariophysians, while the utricular otolith, lapillus, is usually the most conspicuous otolith in Siluriformes (Platt, Popper, 1981; Assis, 2003). Although otolith appearance and shape indicate high levels of morphological differentiation between species (e.g., Popper et al., 2005; Deng et al., 2013; Volpedo, Vaz-dos-Santos, 2015), intraspecific variations may occur according to sex (e.g., Bose et al., 2017; Maciel et al., 2019), growth (e.g., Lombarte, Castellón, 1991; Bose et al., 2018), geography (e.g., Stransky et al., 2008; Treinen-Crespo et al., 2012) and environmental factors (e.g., Lombarte, Lleonart, 1993; Schulz-Mirbach et al., 2011).

Otolith morphological, morphometric and shape analyses have increasingly been applied as tools in stock assessments (Paul et al., 2013; Hüssy et al., 2016; Morawicki et al., 2022), ecological studies (Schulz-Mirbach et al., 2011; Tuset et al., 2016) and species discrimination (Popper et al., 2005; Deng et al., 2013; Mereles et al., 2021), evaluating intra- and inter-specific variability between different populations. Thus, the specific aim of our study was to provide an in-depth appraisal of the value of a lapillus otolith shape analysis to examine sexual-based dimorphism and for the identification of divergences among isolated Scleromystax barbatus populations from coastal Atlantic Rainforest streams.

Material and methods

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Study area. Scleromystax barbatus individuals were sampled in eight clear-water streams encompassing the southern (VR, GR, DM, CU, and PE locations) and southeastern (AR, PM, and AE locations) distribution of the species in the Atlantic Rainforest biome (Fig. 1), between 2019 and 2021, employing electrofishing and seine nets. Voucher specimens were deposited in the fish collection of the Museu de História Natural Capão da Imbuia (MHNCI) (Tab. 1).

FIGURE 1| Locations where Scleromystax barbatus populations were sampled in clear-water streams of the coastal Atlantic Rainforest biome. Red symbols represent the southern locations (VR, GR, DM, CU, and PE) and blue symbols indicate the southeastern locations (AR, PM, and AE).

TABLE 1 | Locations, number of females and males of Scleromystax barbatus, total length (mean ± SD) of individuals and vouchers of samplings conducted in the coastal Atlantic Rainforest biome.

Region	Location	Municipality/State	Stream	Coordinates	Females	Males	TL (mean ± SD)	Voucher
Southeastern (Se)	AR	Angra dos Reis/RJ	Ariró	22°54’07.33”S 44°20’46.56”W	3	9	55.0 ± 0.61	MHNCI 12735
	PM	Caraguatatuba/SP	Pereque-Mirim	23°43’33.51”S 45°26’14.10”W	4	8	50.5 ± 0.40	MHNCI 12827
	AE	Itariri/SP	Aerado	24°17’51.31”S 47°08’47.83”W	6	7	52.2 ± 0.59	MHNCI 12734
Southern (S)	VR	Jacupiranga/SP	Unamed	25°05’57.35”S 48°11’40.67”W	7	5	49.7 ± 0.30	MHNCI 12828
	GR	Guaraqueçaba/PR	Guaraqueçaba	25°15’49.11”S 48°18’35.24”W	4	8	52.0 ± 0.81	MHNCI 12829
	DM	Paranaguá/PR	Do Meio	25°24’11.27”S 48°52’23.54”W	7	3	49.9 ± 0.62	MHNCI 12830
	CU	Joinville/SC	Cubatão Norte	26°13’21.76”S 48°53’49.48”W	8	4	52.8 ± 0.33	MHNCI 12831
	PE	Barra do Sul/SC	Pernambuco	26°23’19.60”S 48°40’55.94”W	8	2	47.4 ± 0.51	MHNCI 12736

Data collection. Total lengths (TL; mm) were determined and otoliths were extracted from each specimen, washed, and stored dry before subsequent analyses. To reduce the effect of ontogenetic otolith changes, analyses were performed only for adult fish ranging from 4.0 to 8.0 cm TL. For the morphological analyses, the left lapillus otoliths of 93 individuals of S. barbatus, whereby 47 originated from females and 46 from males, were placed with the macular hump facing up (ventral surface), and with the anterior extreme pointing left. Two-dimensional digital images were recorded using a Leica® M205 C stereomicroscope using 16.0x objective coupled with a digital camera MC170 HD (Leica®) (magnification 160x), employing the LAS 4.8.0 software (Leica®) using reflected light with a dark background.

Data analysis. The lapillus otoliths were described according to Adams (1940) and Assis (2005). Otolith image analyses were performed in the shapeR package (Libungan, Pálsson, 2015) available in R environment (R Development Core Team, 2021). Otolith outlines and shape coefficients were assessed employing normalized elliptic Fourier transform and Wavelet functions. For all analyses, male and females of S. barbatus were grouped according to the location of capture: southern (VR, GR, DM, CU, and PE) and southeastern (AR, PM, and AE) distribution in the Atlantic Rainforest biome.

The Elliptic Fourier analysis provides information concerning overall differences in otolith shape, describing and characterizing outlines in a quantifiable manner (Lestrel, 1997). The method fitted a number of harmonic functions to capture crenulations and lobes on the otolith edges (Tracey et al., 2006). The Wavelet method is useful for detecting shape differences at specific regions, which may be located at a given angle on the otolith outline (Libungan, Pálsson, 2015). The Wavelet method fits a series of approximating functions within restricted domains to quantify the outline shapes (Graps, 1995), and has been proven an adequate method to detect inter- and intraspecific differences (Tuset et al., 2021). Prior to the shape analyses, the outlines of each image were smoothed to remove the high frequency of pixel noise around the otolith contour using the smoothout function with 100 iterations.

The Fourier/Wavelet coefficients were standardized by fish length (Libungan, Pálsson, 2015), and the otolith shape of S. barbatus was reconstructed using the mean Fourier/Wavelet coefficients and plotted using the ‘plotFourierShape’ and ‘plotWaveletShape’ functions, respectively (Libungan, Pálsson, 2015). Prior to the analysis concerning inter-population differences (males/females and southern/southeastern groups), five Fourier and Wavelet coefficients that did not meet normality (Shapiro-Wilk’s tests) and homoscedasticity (Levene’s tests) assumptions were removed, totaling 40 Fourier and 50 Wavelet coefficients.

The shape variations among the groups were compared by a Canonical Analysis of Principal coordinates (CAP) applied to the Fourier/Wavelet coefficients using the capscale function available in the vegan package (Oksanen et al., 2013)The ordination of the population’s averages along the first two canonical axes was evaluated graphically with shape descriptors. An ANOVA-like permutation test for the CAP was applied to assess the significance of constraints employing 1000 permutations. A minimum of 0.01% was adopted as the significance level. All statistical analyses were performed in the R environment (R Development Core Team, 2021).

Results​

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The lapillus otoliths of S. barbatus display an elongation in the superior-inferior axis, with uneven wavy bottom edges, while the gibbus maculae is large, prominent, occupying much of the surface of the otolith and the sulcus is short, wide and contours the inner gibbus maculae region (Fig. 2). The ANOVA-like permutation test for the Fourier/Wavelet coefficients indicated significant differences between otoliths of males of Scleromystax barbatus from southern and southeastern areas in the Atlantic Rainforest biome, and also between otoliths of males from southeastern areas and females of southern areas of the Atlantic Rainforest biome (Tab. 2).

FIGURE 2| Ventral view of the left lapillus otoliths of Scleromystax barbatus from streams in the southern (VR, GR, DM, CU, and PE) and southeastern (AR, PM, and AE) regions of the Atlantic Rainforest biome. A (Anterior), M (Medial).

TABLE 2 | Analysis of variance (ANOVA-like) permutation tests for Fourier and Wavelet coefficients of otolith shape among males and femalesof Scleromystax barbatus from southern and southeastern areas in the Atlantic Rainforest biome. Bold numbers denote significant differences (considering F and p-values). DF = Degree of freedom, SS = Sum of squares. SeFe (Females from the southeastern region), SeMa (Males from the southeastern region), SFe (Females from the southern region), SMa (Males from the southern region).

Variables	DF	Fourier			Wavelet
		SS	F	P	SS	F	P
All groups	3	0.027	1.9393	0.024	5.178	1.8634	0.027
Southeastern (Se) vs. Southern (S)	1	0.008	2.3115	0.039	3.908	4.5173	0.003
Female (Fe) vs. Male (Ma)	1	0.002	0.4975	0.765	0.332	0.3593	0.944
SeFe vs. SMa	1	0.002	0.3212	0.902	0.451	0.4431	0.862
SeFe vs. SFe	1	0.009	2.2639	0.061	1.890	2.0973	0.059
SeFe vs. SMa	1	0.013	2.0781	0.073	2.293	2.0503	0.063
SeMa vs. SFe	1	0.011	3.1020	0.014	2.281	2.8054	0.014
SeMa vs. SMa	1	0.015	2.9842	0.015	2.954	3.1036	0.010
SFe vs. SMa	1	0.003	0.7711	0.544	0.492	0.5679	0.780
Residual	89	0.406			82.432

The Fourier and Wavelet reconstructions showed differences among the mean otolith outlines between the southern and southeastern areas (Fig. 3). The highest variation was observed for the extremum anterior, the posterior region and medial regions of the sulcus. Otoliths from the southeastern areas are more elongated in these portions, mainly in the Wavelet reconstruction. Conversely, high overlaps in the lateral sulcus and in the lateral and medial gibbus maculae regions were observed.

FIGURE 3| Mean otolith shape based on the Fourier (above) and Wavelet (below) reconstructions for males and females of Scleromystax barbatus from southern and southeastern regions in the Atlantic Rainforest biome. Lines represent the groups: SeFe (Females from the southeastern region), SeMa (Males from the southeastern region), SFe (Females from the southern region), SMa (Males from the southeastern region).

The CAP assessments indicated that otolith shape was not homogeneous among the southern and southeastern regions, for both coefficients (ANOVA-like, P < 0.01). The first two principal coordinates axes explained 94.4% of the total Fourier coefficient variation and 94.3% of the Wavelet coefficient variation (Fig. 4).

FIGURE 4| Otolith shapes of males and females of Scleromystax barbatus from southern and southeastern regions in the Atlantic Rainforest biome employing a Canonical Analysis of Principal Coordinates (CAP) applied to Fourier (above) and Wavelet (below) coefficients. Bold letters represent the mean canonical coordinates surrounding the standard error for each population. Lines represent the groups: SeFe (Females from the southeastern region), SeMa (Males from the southeastern region), SFe (Females from the southern region), SMa (Males from the southeastern region).

Discussion​

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The morphologies of Scleromystax barbatus lapillus otolith are very characteristic and can be effectively assign to lapillus otolith of most Callichthyidae family (Volpedo, Fuchs, 2010). Although it is not possible to establish a morphological pattern for the otoliths of Siluriformes (Cutrim, Batista, 2005; Volpedo, Fuchs, 2010; Sánchez, Martínez, 2017), due to the great diversity of this monophyletic group (Malabarba, Malabarba, 2019) and phenotypic plasticity (Alexandrou et al., 2011; Lujan, Armbruster, 2012), the lapillus otoliths analyzed in the present study correspond to the non-clupeiform type proposed by Assis (2005). Furthermore, the prominent and large gibbus maculae and the elongation noted in its posterior-anterior axis correspond to the ovoid model proposed by Sánchez, Martínez (2017) for the Loricariidae lapillus.

Among the three pairs of otoliths, the lapillus is the one that presents the most regular edge shape and the most homogeneous structure constitution, indicating that geometric morphometry and shape indices are less efficient, due to the difficulty in finding comparable (homologous) structures (Assis, 2005; Adams et al., 2009; Tuset et al., 2021). For this reason, the use of contour analyses is more indicated for this type of otolith, as these methodologies are more efficient to capture all small otolith silhouette variations (Mereles et al., 2021; Tuset et al., 2021). In fact, Fourier and Wavelet analyzes were proven efficient in identifying different S. barbatus groups, with Wavelet descriptors proving slightly more sensitive to capture these variations through canonical and ANOVA analyses. Similar results have been reported by other studies for lapillus using shape analyses (Pavlov, 2022; Qiao et al., 2022; D’Iglio et al., 2023).

Reconstruction of otolith shapes employing Fourier and Wavelet analyses indicates that changes in S. barbatus otolith shapes occur mainly in the anterior-posterior direction and at the edges of the sulcus and gibbus maculae regions. The otoliths of males and females of S. barbatus from the southeastern areas in the Atlantic Rainforest biomeare more elongated in the anterior-posterior direction and present larger sulcus and gibbus maculae regions, and their borders are more heterogeneous when compared to males and females from the southern areas.

Otolith shapes have been proven an efficient tool to identify marine and estuarine fish populations (Cardinale et al., 2004; Boudinar et al., 2016; Bose et al., 2017; Adelir-Alves et al., 2018; Zarei et al., 2023), assisting in the management of species used as fishing resources (Avigliano et al., 2014; Moreira et al., 2019; Kikuchi et al., 2021; Neves et al., 2021; Ibañez et al., 2022; Morawicki et al., 2022; Soeth et al., 2022; Barnuevo et al., 2023; Franco et al., 2023), and also used to explain the current distribution of many species, although few studies on neotropical fish employing otolith shape to distinguish populations are available (da Costa et al., 2018; Mereles et al., 2021). As for marine and estuarine fish, our results indicate that assessments of otolith shape also constitute an interesting tool to differentiate isolated populations of freshwater fish.

Although the factors that determine otolith shapes are not fully understood, as they can be generated and influenced by ontogeny, adaptations, sexual dimorphism, phylogenetic and biogeographical processes (Tuset et al., 2016), the combination of genetic and environmental causes may be responsible for the differentiation of the otolith shapes in geographically isolated populations (Cardinale et al., 2004; Vignon, Morat, 2010; Berg et al., 2018; Santos, Vaz-dos-Santos, 2023). Differences observed in the otolith shapes of S. barbatus can therefore be attributed to regional variations in fish life history mediated by differences in environmental factors between the southern and southeastern areas in the Atlantic Rainforest biome, for instance. The combination of these factors may explain otolith shape differences among the investigated S. barbatus populations, which despite being restricted to coastal Atlantic Rainforest streams, is widely distributed (Reis, 2003; Oyakawa et al., 2006), inhabiting regions presenting different climatic conditions. Our results also indicate that sex may not be the determining factor for differentiation between otoliths of S. barbatus, although this species presents marked sexual dimorphism (Oyakawa et al., 2006).

The otolith shape analysis applied herein was efficient in geographically discriminating the sampled groups and may contribute to a better understanding of the current S. barbatus distribution in the Atlantic Forest. However, additional studies are required to investigate the influence of genetic effects and their environmental interactions to better understand how these factors can affect otolith shape among different S. barbatus populations.

Acknowledgments​

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We are grateful to Adriano Hauer, Axel M. Katz, Thiago T. Batista for the aid in field collections. We also thank the Laboratory of Evolutionary Genetics (LabGEv), especially Roberto F. Artoni, for allowing us to use his photographic equipment. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); through a doctoral scholarship to RHD under VA supervision respectively.

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Authors

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Roger Henrique Dalcin¹ and Vinicius Abilhoa^1,2

^[1]    Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná. Av. Cel. Francisco H. dos Santos, s/n, Jardim das Américas, 81531-980 Curitiba, PR, Brazil. (RHD) roger_dalcin@hotmail.com (corresponding author).

^[2]    Museu de História Natural Capão da Imbuia, MAPCF/PMC, Rua Prof. Nivaldo Braga, 1369, 82810-080 Curitiba, PR, Brazil. (VA) vinicius.abilhoa@gmail.com.

Authors’ Contribution

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Roger Henrique Dalcin: Conceptualization, Formal analysis, Methodology, Writing-original draft.

Vinícius Abilhoa: Conceptualization, Formal analysis, Methodology, Supervision, Writing-review and editing.

Ethical Statement​

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The specimens were collected under a collection permit authorized by Instituto Chico Mendes de Conservação da Biodiversidade (SISBIO 73016).

Competing Interests

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The author declares no competing interests.

How to cite this article

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Dalcin RH, Abilhoa V. Discriminating Scleromystax barbatus (Siluriformes: Callichthyidae) populations from Atlantic Rainforest streams employing otolith shape. Neotrop Ichthyol. 2024; 22(1):e230129. https://doi.org/10.1590/1982-0224-2023-0129

Copyright​

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This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Distributed under

Creative Commons CC-BY 4.0

© 2024 The Authors.

Diversity and Distributions Published by SBI

Accepted February 2, 2024 by Paulo Pompeu

Submitted May 15, 2023

Epub April 19, 2024