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Article

Insights of Otoliths Morphology to Reveal Patterns of Teleostean Fishes in the Southern Atlantic

by
Lucinha Santos
1,* and
André Martins Vaz-dos-Santos
1,2,*
1
Aquaculture and Sustainable Development Post-Graduation Program, Palotina Sector, Federal University of Paraná (PGADS-UFPR), Rua Pioneiro, Palotina 85950-000, PR, Brazil
2
Sclerochronology Laboratory, Palotina Sector, Federal University of Paraná (LABESC-UFPR), Rua Pioneiro, Palotina 85950-000, PR, Brazil
*
Authors to whom correspondence should be addressed.
Fishes 2023, 8(1), 21; https://doi.org/10.3390/fishes8010021
Submission received: 18 November 2022 / Revised: 22 December 2022 / Accepted: 26 December 2022 / Published: 28 December 2022
(This article belongs to the Special Issue Otoliths and Their Applications in Fishery Science II)
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Abstract

:
The sagitta otoliths of teleostean fishes are usually used in diverse studies. Their shapes are species-specific, and the qualitative description of their morphological features seems to be a simple task, despite its subjectivity. On the other hand, morphometric techniques have been developed with a focus on objectivity, reproducibility, and accuracy. Considering this, the otoliths morphology was reviewed and evaluated in terms of robustness as a taxonomic tool and to highlight ecomorphological patterns. The otoliths morphology of 179 teleostean fishes from the Southern Atlantic were analyzed. For each species, the fish total length range, eighteen otolith morphological features (OMFs), and relative proportions were annotated. Species habitat and habit were also recorded. Data analyses were based on exploratory analysis, correlation, nonmetric multidimensional scaling, and a two-way permutational analysis of variance. The most descriptive OMFs were: colliculum, sulcus acusticus (morphology, position, orientation, and opening), and otolith profile. The otolith morphology was significantly related to species habitat and habit, with a new pattern described for deep-ocean pelagic species. In conclusion, otoliths morphology is robust whenever it is based on the comparative method application (otoliths among otoliths), considering the constant updates of fishes’ taxonomy and the use of proper sample sizes linked to morphometric techniques.

1. Introduction

Fish sensory systems involve different adaptations concerning vision, chemoreception (smell, taste), electroreception, magnetic reception, and mechanoreception (sound detection, postural equilibrium). Mechanoreception regards the lateral line system and the inner ear, this last constituted by three semicircular canals filled with endolymph and three pairs of otolithic organs (sagitta, lapillus, and asteriscus). The otoliths detect sounds and changes in body acceleration/orientation, information that is transduced by sensory hair cells [1,2]. Otoliths are constituted by calcium carbonate, organic matter, and other elements, grow continuously along the fish’s life, and do not suffering resorption. These properties make them useful for diverse studies such as growth, migration, and stocks assessment, among others [2,3]. Usually, the most used otolith is the sagitta, the largest one.
Tuset and collaborators [3] and Volpedo and Vaz-dos-Santos [2] reviewed historical studies that consolidated the use of otoliths features as a taxonomic tool due to their species-specific shapes. There are a dozen of otoliths guides available for different areas and periods, mainly from the 1970’s [4,5]. The level of otoliths descriptions varies among references, from images [6,7,8] to complete qualitative quantitative descriptions [5,9]. Some of these references also include identification keys at different taxonomic levels [10,11,12,13].
Otoliths features (i.e., shape, chemistry, growth patterns) are driven both by genetic and environmental determinants related to habitats and habits [14,15]. These determinants comprise fish metabolism related to food intake, growth, breathing, excretion [16,17], sound production [1,18], general behavior, and locomotion type [19,20], and environmental features such as depth, temperature, salinity, hydrodynamics, biological production, etc. [21,22,23]. Then, otoliths morphology is the result of a complex interaction between intrinsic and extrinsic factors [24], making them a valuable tool in understanding ecological patterns [22,25,26,27]. Lombarte and Tuset [4] defined ecomorphology of sensory organs as “the science that compares the morpho functional and ecological data of species”. This environmental association was focused by diverse authors on different habitats, such as continental shelves [21,28], the Antarctic Sea [23,29,30], an estuarine system [31], rocky environments [20,32], and freshwater environments [17,33,34].
Both taxonomic and ecological approaches are based on various otoliths qualitative and quantitative (morphometry) characters to describe their morphology [4,35], the former tending to be subjective whereas the latter is objective. Qualitative characters were standardized by Tuset and collaborators [3], and, even so, they are subject to greater or lesser bias in the analysis. For example, the otolith shape (outline) definition depends on an interpretation, whereas the presence/absence of the colliculum is objective. On the other hand, otoliths morphometry is based on a set of measurements (e.g., length, height, width, weight, perimeter, area, landmarks, outline, wavelets), some of them used to calculate shape indices [36]. Data analyses of the measurements involves bivariate, multivariate, and geometric techniques [37,38,39,40], a scientific field that has been progressing and changing a lot lately [40].
This scenario calls attention to the morphology field: otoliths descriptions should be robust enough for taxonomic identification and to infer ecological patterns. Whereas otoliths morphometry continues to be vanguardist, otoliths morphology seems to be quiescent, and we aimed to evaluate its robustness as an identification tool and to highlight ecomorphological patterns. The study was based in the following premises: (i) otoliths are species-specific; (ii) otoliths morphology is suitable for taxonomic identification; (iii) available information in otoliths guides are enough for the first two premises; and (iv) otoliths reflect fish habitats and habits. Available information in otoliths guides for the Southern Atlantic was analyzed with proper statistical techniques to attain the study goals. Analytical aspects related to sample size and subjectivity were also discussed.

2. Materials and Methods

In the Southern Atlantic, the area between 22° S and 34° S (from Cape Frio to Chuí, Brazil) (Figure 1) is highly productive in terms of fisheries resources [41]. The oceanographic conditions are well studied from the coast to the upper slope, presenting a wide variety of marine environments and a diverse ichthyofauna, including important fishery resources [41,42]. Considering a reference for the area, the marine ichthyofauna comprises close to 594 species in comparison to 1297 in Brazil [43].
The database was obtained from the “Atlas of marine bony fish otoliths of Southeastern-Southern Brazil” (AMBFO), a sequence of published articles presenting otolith descriptions of 186 fish species from the area between 22° S and 34° S [13,44,45,46,47,48,49]. Earlier studies about otolith morphology in the area were not included to standardize the analyses criteria [50,51,52,53]. The otoliths descriptions were based on standard references for the field [3,54], considering eighteen morphological features: otolith shape, anterior and posterior region shapes, dorsal and ventral edges, otolith profile, rostrum and antirostrum development and orientation, pseudorostrum and pseudo-antirostrum development, and sulcus acusticus features, i.e., position, orientation, opening, morphology, and colliculum, ostium and cauda development [13]. The minimum and maximum fish total lengths (TL, mm), the number of otoliths analyzed, and the relative proportions values based on otolith length (OL, mm), height (OH, mm), and thickness (OT, mm) were also annotated (OL/TL × 100, OL/OH × 100, OL/OT × 100 and OH/OT × 100). Data were analyzed only for symmetric sagitta, not including the Pleuronectiformes and the lapillus of Siluriformes [47].
Fish species and otoliths information were compiled and entered in a spreadsheet. Only qualitative otolith morphological features (OMFs) with at least 70% of frequency in the same type of description were recorded, avoiding the use of less informative ones. This value was empirically settled to encompass, for example, two observed otoliths in a total of three. Fish classification and nomenclature was updated for orders and families [55] and for species and authors [56]. Species habitats were attributed as follows: inner-neritic (≤ 50 m depth), rocky-neritic, neritic (over the continental slope), oceanic (highly migratory), and deep ocean (upper slope, 100 ≤ 600 m depth) [57,58,59,60,61]. The occupation and use of the marine environment, i.e., species habit, comprised the benthic, demersal, and pelagic categories [62].
The analysis was done based on order level, and an exploratory data analysis was performed, quantifying the number of OMFs available. To verify the sample size effect on the sample, the Spearman correlation was calculated between the number of OMFs with the number of individuals analyzed and the fish total length range [63]. The availability of a given OMF was also graphically analyzed in terms of frequency, and the number of its various categories counted. For an identification tool, only the OMFs available for 90% or more of the total species were used to analyze exclusive ones at order level.
Ecological assessment of orders (i.e., habitat and habit) based on otoliths features was done based on qualitative and quantitative elements. Numerical data (relative proportions) were previously transformed using log(x + 1) [63]. Species habitat, habits, and the relative proportions were submitted to a nonmetric multidimensional scaling analysis (nMDS) using the Bray-Curtis distance and the TO algorithm with 9999 permutations [64,65]. In sequence, a two-way permutational multivariate analysis of variance (two-way PERMANOVA) was performed to ascertain significances [66]. Results descriptions used average values and t confidence intervals. Additional discriminant analyses (by habitat and habit) were performed and presented in an appendix. It was used the free software Paleontological Statistics (PAST) version 4.12 (University of Oslo, Norway). In all statistical procedures, it was considered α = 0.05 [63].

3. Results

The total of 179 species analyzed comprised 40 orders and 69 families, all belonging to Class Actinopterygii, Subclass Neopterygii, Infraclass Teleostei (Table 1). The largest number of species was recorded in Carangiformes and Eupercaria, both with 18 species, followed by Perciformes (n = 15), Scombriformes (n = 13), Clupeiformes (n = 12) and Gadiformes (n = 11). These six orders together included 50% of the total species analyzed. A total of fourteen orders were represented by only one species. The highest number of species belonged to the Carangidae (n = 18), Sciaenidae (n = 16), Myctophidae (n = 8) and Serranidae and Engraulidae families, these last two with seven species each. These species comprised a total of 6196 otoliths analyzed.
Among the OMFs and following the selection criteria, the minimum number observed was eight and the maximum was eighteen with a median value of thirteen (Figure 2A). The availability of OMFs description varied from 100% (colliculum of sulcus acusticus) to 46.93% (ventral edge) (Figure 2B). By order, these numbers varied a lot, considering the number of species analyzed (Figure 3 and Table 1). The sample size effect was significative, and the number of OMFs was negatively correlated with the number of otoliths (individuals) analyzed (rs = −0.406, p < 0.001, Figure 2C) and the fish total length range (rs = −0.428, p < 0.001, Figure 2D).
The OMFs variation, in a descending order of availability (the same of Figure 2B), were:
  • Colliculum absent or present (heteromorphic, holomorphic, homomorphic, monomorphic, unimorphic).
  • Sulcus acusticus morphology (archaesulcoid, heterosulcoid, homosulcoid, pseudo-archaesulcoid).
  • Sulcus acusticus position (inframedian, median, supramedian).
  • Otolith profile (biconvex, concave-convex, flattened, plane-convex).
  • Sulcus acusticus orientation (ascending, slightly ascending, descending, horizontal).
  • Sulcus acusticus opening (caudal, mesial, ostial, ostio-caudal, para-ostial, pseudo-ostial).
  • Rostrum absent or present (developed, underdeveloped/undeveloped).
  • Ostium absent or present (bent, bent-concave, discoidal, elliptic, funnel like, lateral, oval, rectangular, round-oval, tubular).
  • Otolith shape (34 categories).
  • Sulcus acusticus cauda absent or present (elliptic, funnel like, oval-circular, round-oval, slightly curved, and tubular and eight more variations).
  • Antirostrum absent or present (developed, underdeveloped, undeveloped).
  • Anterior and posterior regions (irregular, angled, blunt, double-peaked, flattened, lanceolate, notched, oblique, peaked, round, and their combinations).
  • Rostrum antirostrum orientation: when applicable, in agreement and in disagreement (not in agreement).
  • Dorsal edge (entire, lobed, sinuate, irregular, and their combination).
  • Pseudorostrum and pseudo-antirostrum absent or present (developed and underdeveloped/undeveloped).
  • Ventral edge (crenate, dentate, entire, irregular, lobed, round, serrate, sinuate, and their combinations).
The first six OMFs comprised more than 90% of occurrence (colliculum, sulcus acusticus morphology, position, orientation and opening, and otolith profile), and the attempt to delineate any identification system failed due to the absence of exclusive features by order and family.
Otoliths of neritic species predominated in the sample (inner-neritic = 45, rocky-neritic = 11, neritic = 75), followed by deep ocean (n = 47), and one oceanic (n = 1) species, the only not included in the quantitative analysis (Appendix A). The demersal habit was the most numerous (n = 88), followed by pelagic (n = 77), and benthic (n = 14). The nonmetric multidimensional scaling ordinated the orders’ habitats and habits well (Figure 4), with a stress level of 0.1779. The first coordinate explained 0.8024 of the variances. Neritic in general and deep-ocean species were separated along the first coordinate. Neritic species were differentiated between pelagic and demersal habits and deep ocean between benthic and demersal habits. The specific neritic habitats were not clearly differentiated due to the values overlap. Habitat and habit play a significant role in the relative proportion values, mainly in the interaction (Table 2). The percentages of matches (given and predicted groups) also predominated in the discriminant analyses (Appendix B).
By fish habitats (F = 4.0586, p = 0.0006), the OL/TL relative proportion differentiated inner-neritic species from the others, with the lower mean value (±t confidence interval) 2.5420 ± 0.375. The other habitats presented higher and overlapped values, from the neritic lower confidence limit (2.9604) to the rocky-neritic upper confidence limit (4.4016). The OL/OH had some confusing patterns; the inner-neritic (67.0 ± 6.290) and deep-ocean (66.0147 ± 6.290) were overlapping, and the rocky-neritic (58.8218 ± 7.114) and neritic species (55.1472 ± 3.977) were overlapping with lower values. The values of OL/OT relative proportion did not show any pattern related to habitats, ranging from the rocky-neritic lower confidence limit (14.3128) to the inner-neritic upper confidence limit (23.6768). The neritic habitat was the only habitat differentiated by the OH/OT relative proportion (37.5587 ± 2.844), whereas the others overlapped inside the deep-ocean confidence limits (32.2572 ± 5.991).
Considering the fish habits (F = 3.9072, p = 0.0033), demersal species tend to differentiate from pelagic and benthic ones, presenting higher values of relative proportions. The most remarkable difference was found in the OL/TL values that allow to discriminate the habits. Benthic species presented the mean value of 2.1014 ± 0.736, demersal species 3.7372 ± 0.251, and pelagic species 2.8165 ± 0.382. The OL/OH and OL/OT relative proportions were not differentiated, and the benthic averages encompassed the values of demersal and pelagic species (66.3400 ± 14.020 for OL/OH and 20.4464 ± 4.633 for OL/OT). The OH/OT relative proportion also allowed to differentiate fish habits, with the mean values of 33.4057 ± 4.537 for benthic species, 37.8457 ± 3.661 for demersal species, and 30.4030 ± 1.843 for pelagic species.
The interaction between fish habitat and habits was the most relevant explanatory factor (F = 4.0047, p = 0.0001) (Table 2, Figure 5). The OL/TL relative proportion separated the demersal neritic species from the lower confidence limit (2.5453) of inner-neritic to the upper (4.9535) of rocky-neritic. Benthic and pelagic species could not be differentiated with this variable. Deep-ocean species did not present overlapped values in the OL/TL relative proportion: 1.5680 ± 1.554 for benthic species, 3.3989 ± 0.437 for demersal, and 5.1631 ± 1.470 for pelagic. The OL/OH relative proportion was also robust for deep-ocean species (49.0700 ± 25.848 for benthic species, 61.2214 ± 7.694 for demersal, and 81.6529 ± 9.121 for pelagic species), although it was not effective for neritic species. The OL/OT relative proportion presented the highest values for inner-neritic benthic species (27.2820 ± 4.289), the others all falling inside the deep-ocean benthic species confidence interval (15.3340 ± 11.614). The values of OH/OT relative proportion were differentiated for neritic demersal species (41.2302 ± 4.077) and for deep-ocean pelagic species (21.4179 ± 1.845).

4. Discussion

The species here analyzed were sampled in different areas and periods [13,44,45,46,48,49]. The systematic surveys conducted in different spatial temporal scales were focused on demersal neritic species (1985–1988), on pelagic neritic species (2005), on deep-ocean pelagic and demersal species (1996–2006), and on inner-neritic and rocky-neritic species (2010–2014) [13,45]. In this way, the database was subject to an unavoidable selectivity in terms of species occurrence, although the results of otolith analysis followed the same criteria. Nevertheless, the option to not include earlier studies [50,51,52,53] did not affect the taxonomic composition at the order level and the habitat and habit representativeness, ensuring robustness for the current analyses.
In a regional scale, comprising the Paranaguá Estuarine Complex and adjacent areas (25°15′–25°35′ S, 48°20′–48°45′ W), there are detailed descriptions of otoliths from some inner-neritic common species not recorded in sources used, like the clupeiform Chirocentrodum bleekerianus, Pellona harroweri, Lycengraulis grossidens, some Anchoa spp. [51,52], and the sciaenid species Bairdiella ronchus, Cynoscion acoupa, C. microlepidotus, and Nebris microps [53]. These absences were not a problem, because clupeiform and sciaenid fish were well represented herein (twelve and sixteen species, respectively). But these examples evidence that otoliths guides are neither a whole biodiversity record nor do they denote fish communities; they represent some of the most common marine species, including important fisheries resources [11,67]. In the current case, although the database was from different areas and periods, it attained almost fifty percent of the total species of this portion of the Southern Atlantic [43].
Sample size is an important question in biological studies, related to sufficiency, accuracy, precision, and power in statistic tests [63]. For otoliths analysis, the adoption of the ecological rule (at least ten otoliths) from different body size length classes is recommended [35]. Current results confirmed that large sample sizes reduce the otolith morphological features precision, i.e., more variability is added to a given description. Although expected, this is a key point in otoliths descriptions. Most of available otoliths guides presented descriptions based on few otoliths—less than ten [3,5,9,68]. Although valid and good descriptions, some factors that affect intraspecific variability in otoliths features cannot be rigorously evaluated with a small sample size. These factors include ontogeny, sexual dimorphism, growth rates, and distinct population units [6,17]. Especially in relation to ontogeny, information about first maturity allows to determine the adult morphological pattern of an otolith [69,70]. This is important: the species-specific shape of otoliths is an adult attribute, because in fish larvae they are still circular/oval.
A practical example of the sample size effect can be evaluated considering Beryx splendens. The same samples were analyzed first by Rondon and collaborators [71] and then by Conversani and collaborators [49], both following the same main reference [3]. There are many divergent results from the former and the later study, respectively, including: sample size (259 vs. 29), otolith shape (pentagonal vs trapezoidal), anterior region (peaked vs oblique), posterior region (angled vs peaked-round), ventral edge (crenate vs lobed-sinuate), sulcus acusticus position (median vs supramedian), and sulcus acusticus opening (pseudo-ostiocaudal vs ostiocaudal). It is astonishing that these descriptions do not match, although they are based on the same sample and method. In this case, increasing the number of otoliths (repetition) was welcome to create a pattern favoring the first description [71]. Analyzing a large sample (n ≥ 10) for each combined category (size class, gender, sample site, season, etc.) is a way to control differences related to ontogeny and sexual dimorphism in otoliths shape [17].
The aforementioned situation evidences the variability of otolith morphological features, which was the reason for the failure in delineating an identification system. Campana [6] has already tried to create an identification key at the order/family level, but he discontinued it. Herein, during the data analysis, there were attempts to apply a cluster analysis combining morphology and morphometric data [72], which were also not successful. The constant use of new OMFs and measurements in otoliths descriptions is an attempt to reduce bias and improve the otoliths accuracy for taxonomic identification [11]. Nevertheless, it is important to consider that species affiliation is not stable, and taxa are rearranged and/or discovered yearly [6,9,55,56]. The database here used exemplifies this [13,44,45,46,48,49], once they followed a systematic organization (order level) before Betancurt-R and collaborators [55]. Thus, the use of identification keys demands a constant update [11].
Related to otoliths descriptions available in different guides, methodological differences are a priori source of incomparability among studies. Even so, most of the available sources were adapted from primary ones. Hecht [68] redefined and redescribed earlier otolith terminology, looking for standardized descriptions and making it useful as “a guide and key”, followed by several authors [11,29,73,74]. Morrow [10] and Härkonen [75] nomenclature also had wide application [9,12,67,76]. Otoliths descriptions of particular taxa incurred in the same way, for some Carapidae and Sciaenidae [77,78], for Bembrops heterurus [79], for five Pampus spp. [39], for three Pagellus species [24], inter alia.
Since 1993, the International Otolith Symposium put forward the otolith science and the needed standardization concerning otoliths descriptions [2]. Kalish and collaborators [80] standardized the general terms used for otolith morphology. Then, practically all previous otolith guides were reviewed by Tuset and collaborators [3]. The most relevant OMFs for species identification are the rostrum, antirostrum, and the sulcus acusticus [3,6,40]. Our results were obtained at order level and matched this, but this was not enough to elaborate a straight system for identification based on otolith features due to their variability [4], even using a higher taxonomic level. This variability was observed in most OMFs, not only restricted to the general shape [3]. The incipient use of the otolith external face can be another source of bias, since they are valuable and were presented with images, but not described [11]. Thus, the suitability of otoliths morphology for taxonomic identification is relative, still lying in the subjectivity. Otoliths descriptions are a useful empiric tool based on the comparative method, i.e., otoliths among otoliths [8].
The use of otoliths measurements constitutes a way for an objective analysis, and there is a myriad of studies about these methods. Linear measurements are the simplest and still practical for a quick assessment by means of regression analysis [38,53,69,81]. Shape indices and geometric morphometrics appeared in the 2000’s [37,38], and then they were widely applied [40]. Shape indices are those indicators based on perimeter and area: circularity, edge complexity, form factor, rectangularity, and roundness [36], not including the relative proportions. Tuset and collaborators [40] showed that shape indices should not be used for species identification, recommending the use of AFORO algorithm (k-nearest neighbors). Nevertheless, our results concerning fish orders revealed general trends related to habitat and habit, endorsing the interactions between organisms and environment [21,82].
The Southern Atlantic (22° S–34° S) environment is widely studied [41,42]. The continental shelf is wide, reaching 250 Km off the coast of the São Paulo state. The three predominant water masses are related to habitats herein used: inner and rocky-neritic are related to the Coastal Water (CW, varied temperature, salinity < 34); neritic to the Tropical Water (TW, > 20 C, salinity > 36.40) over the continental shelf, and deep ocean to the Central Water of the South Atlantic (CWSA, < 20 C, salinity < 36.40) at the continental slope. Thus, our categories comprised different environmental conditions (depth, temperature, salinity), and otoliths relative proportions expressed this as follows.
Otolith development is intrinsic to fish metabolism, whose rates are related to environmental factors [15,24,81,83]. Proportionally longer and wider otoliths were recorded for rocky-neritic and demersal species, highlighting the sound production ones (Sciaenidae), a pattern related to audition in coastal areas and the relatively slower swimming [1,6,67,84]. On the other hand, pelagic fish usually have proportionally smaller and oval otoliths, related to a reduction in mass to occupy the water column [23]. The deep-ocean pelagic species were outside of this pattern. This can be explained by the association of depth (100 ≤ 600 m at the upper slope) with the small size of these species, mainly Myctophiformes of up to 100 mm of total length, and the general trend that pelagic shoaling has bigger otoliths than no shoaling [67].
In this sense, relative proportions allowed to infer the relationships between otoliths morphology and different environmental and ecological patterns [26,54,81]. Even considering the heterogeneous samples analyzed, otoliths morphometry continues to be highly informative, still considering some mismatches (see discriminant analyses in Appendix B). Nonetheless, homogeneous samples can represent a given fish community and enhance their ecological relationships. In a higher precision level than here, due to a standardized sample effort for the primary data acquisition, otoliths analysis revealed trophic guilds for rockfishes [32] and in a continental shelf [21]. Recently, it was proved that sagitta otolith morphology displays similarities dependent on the sampled environment, accurately assessed with objective sampling, large sample sizes, and governing biological factors monitoring [17].

5. Conclusions

Otoliths morphology described by different otolith morphological features are still useful for an empirical taxonomic identification using the comparative method (otoliths among otoliths), depending on good illustrations [5,6,8]. This method cannot be neglected, and it is recommended to increase and complete collections that support otoliths descriptions by updating them. This is essential to support other analysis, such as age attribution [85]. Intraspecific variations and the constant changes in the fish taxonomy (order/family/genus/species) make otoliths morphology a dynamic field [11].
The use of otoliths morphology to identify ecological patterns is improved when based on focused sampling efforts for fish community assessments [20,83]. The use of large sample sizes is necessary to control sources of variability [17]. Sample size for otoliths analyses must be observed in novel studies (n ≥ 10 at each combined category of analysis), not only related to otoliths morphology but also in other fields (chemistry, geographic variation, and others). The analysis of a reduced number of otoliths does not sustain robust results and inferences.
Relative proportions in lieu of shape indices revealed general ecological patterns related to habit and habitats, and the current study showed a particular situation related to the pelagic deep ocean species at order level. Additionally, these indicators are still efficient for intraspecific diagnosis related to ontogeny, and they can be used with caution, i.e., observing sampling design and sufficiency, and sources of bias.

Author Contributions

Conceptualization, A.M.V.-d.-S.; methodology, L.S. and A.M.V.-d.-S.; software, L.S. and A.M.V.-d.-S.; validation, A.M.V.-d.-S.; formal analysis, L.S. and A.M.V.-d.-S.; investigation, L.S. and A.M.V.-d.-S.; resources, A.M.V.-d.-S.; data curation, L.S. and A.M.V.-d.-S.; writing—original draft preparation, L.S. and A.M.V.-d.-S.; writing—review and editing, L.S. and A.M.V.-d.-S.; visualization, L.S. and A.M.V.-d.-S.; supervision, A.M.V.-d.-S.; project administration, A.M.V.-d.-S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

L.S. and A.M.V.S. thanks the National Council for Scientific and Technological Development (CNPq) for the scholarship and research grant, respectively. Both authors thanks the reviewers for their valuable, neutral, and constructive evaluations. We are also in debt with Fishes Editorial team that makes this publication possible.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table
Table A1. Number of species with otolith descriptions by order, fish habitat and habit in the Southern Atlantic (B = benthic, D = demersal, P = pelagic).
Table A1. Number of species with otolith descriptions by order, fish habitat and habit in the Southern Atlantic (B = benthic, D = demersal, P = pelagic).
Orders.Inner-NeriticRocky-NeriticNeriticOceanicDeep Ocean
BDPDPBDPPBDP
Albuliformes 1
Anguilliformes2 2
Clupeiformes 10 2
Argentiniformes 1
Stomiatiformes 1
Aulopiformes 1 4
Myctophiformes 9
Zeiformes 2
Gadiformes 11
Polimixiiformes 1
Beryciformes 1
Trachichthyiformes 1
Ophidiiformes 2 1
Batrachoidiformes 1
Scombriformes 17131
Syngnathiformes 3 2
Gobiiformes3
Ordem Incertae Sedis Carangaria 33
Carangiformes 5 13
Atheriniformes 1
Beloniformes 5
Mugiliformes 2
Bleniiformes 1
Ordem Incertae Sedis Eupercaria 17 1
Gerreiformes 23
Uranoscopiformes 1
Labriformes 1
Ephippiformes 1
Chaetodontiformes 1
Lutjaniformes 3 5 1
Spariformes 1 2
Priacanthiformes 1 1
Caproiformes 1
Lophiiformes 1 2
Tetraodontiformes 14 1
Pempheriformes 1 3
Centrachiformes 2
Perciformes 14 1
Total511295644427152814

Appendix B

Both discriminant analyses using transformed values of relative proportions were performed using Mahalanobis distance and cross-validation (jackknifing). The overall correct classifications were 46.07% (habitat) and 55.62% (habit) (Table A2).
In terms of habitat, otoliths relative proportions presented the following patterns:
  • Inner-neritic species presented the highest correspondence between given and predicted categories, sustained mainly by Tetraodontiformes, Beloniformes, Anguiliformes, and Priacanthiformes, all of them matching 100%. For other orders, the mismatches were not a problem, once they occurred in the closed category neritic (e.g., Clupeiformes, Carangiformes, Mugiliformes). An interesting disagreement comprised Lutjaniformes and Gerreiformes, reclassified as rocky-neritic, a usual pattern for some species of these orders. This evidence shows the role of genetic determinants, mainly for Lutjaniformes.
  • Rocky-neritic species were the less numerous. The Ephippiformes and most Lutjaniformes (Lutjanus spp., Anisotremus surinamensis) were properly assigned by discriminant analysis. Probably due to the reduced number of species, Bleniiformes, Chaetodontiformes, and Centrachiformes were erroneously reclassified as neritic.
  • Neritic species correctly reclassified comprised mainly Perciformes (Serranidae), Carangiformes (Carangidae), and the order incertae sedis Eupercaria (Sciaenidae), the most typical group distributed along the continental shelf. Reclassifications as inner-neritic species were not a problem. The wrong reclassifications as rocky-neritic species comprised a miscellanea with no clear pattern, demanding further investigations. Some Perciformes (Triglidae) and Spariformes (Sparidae) were attributed to deep-ocean category by jackknifing, a pertinent classification considering some species of these groups not recorded here.
  • Deep-ocean species presented high variability in terms of reclassification. The small size orders (Stomiatiformes, Myctophiformes) matched, sustaining the emergent pattern of relative proportions herein described. Other groups also reinforced the deep-ocean pattern (Argentiniformes, Zeiformes, Polymixiiformes, Beryciformes). Misclassifications were detected in relation to Gadiformes, Lophiiformes, and Pempheriformes (varied patterns). The remarkable mistake comprised the order Aulopiformes, all of them reclassified as rocky-neritic species.
Considering the habits, the percentage of concordant classifications were higher in relation to habitats:
  • Benthic species comprised mainly Gobiiformes, Anguilliformes, and Lophiiformes, properly assigned after jackknifing. There was no trend in relation to the benthic mismatches.
  • Demersal species presented the highest absolute number of matches, including representative orders such as Gadiformes (most part), Perciformes, Mugiliformes, and Eupercaria. Some species recategorized as pelagic ones comprised a number of Gadiformes (Macrouridae) and other groups (e.g., Aulopiformes, Gerreiformes) whose species are “more swimmer” in the water column, reflecting in the otoliths relative proportions.
  • Pelagic species (Carangiformes, Clupeiformes, Scombriformes and others) were correctly classified in the given group. Uncorrected reclassifications as benthic species did not evidence a pattern, except for some Tetraodontiformes and Beloniformes, because they are “maneuver” fishes. The pelagic species attributed as demersal ones by discriminant analysis also did not evidence any trend.
It was not possible to analyze both categories combined (i.e., habitat + habit) using a discriminant analysis due to the small number of categories.
Table
Table A2. Confusion matrices from discriminant analyses based on otolith relative proportions by habitat and habit in the Southern Atlantic.
Table A2. Confusion matrices from discriminant analyses based on otolith relative proportions by habitat and habit in the Southern Atlantic.
HabitatPredicted Groups (Jackknifed)Total
inner-neriticrocky-neriticneriticdeep-ocean
inner-neritic25 (55.6%)8 (17.8%)8 (17.8%)4 (8.9%)45
rocky-neritic1 (9.1%)4 (36.4%)4 (36.4%)2 (18.2%)11
neritic13 (17.3%)20 (26.7%)36 (48.0%)6 (8.0%)75
deep-ocean8 (17.0%)13 (27.7%)9 (19.1%)17 (36.2%)47
Total47455729178
HabitPredicted Groups (Jackknifed)Total
benthicdemersalpelagic
benthic9 (64.3%)3 (21.4%)2 (14.3%)---14
demersal11 (12.5%)55 (62.5%)22 (25.0%)---88
pelagic23 (30.3%)17 (22.4%)36 (47.3%)---76
Total447559---178

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Figure 1. The studied area in the Southern Atlantic. The 100 m isobath delineates the continental shelf.
Figure 1. The studied area in the Southern Atlantic. The 100 m isobath delineates the continental shelf.
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Figure 2. (A) Frequency of total otolith morphological features available. (B) Frequency of each otolith morphological feature available (n = 179) for fish species from the Southern Atlantic. (C) Dispersion diagram between the number of otolith morphological features and the number of otoliths analyzed. (D) Dispersion diagram between the number of otolith morphological features and the fish total length range. The numbers above the columns are the absolute frequencies.
Figure 2. (A) Frequency of total otolith morphological features available. (B) Frequency of each otolith morphological feature available (n = 179) for fish species from the Southern Atlantic. (C) Dispersion diagram between the number of otolith morphological features and the number of otoliths analyzed. (D) Dispersion diagram between the number of otolith morphological features and the fish total length range. The numbers above the columns are the absolute frequencies.
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Figure 3. Boxplot of the number of otolith morphological features available by order for fish species from the Southern Atlantic.
Figure 3. Boxplot of the number of otolith morphological features available by order for fish species from the Southern Atlantic.
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Figure 4. Two-dimensional ordination from the nonmetric multidimensional scaling (nMDS) based on the Bray–Curtis distance based on 178 fish otolith data (habitats, habits, and otolith relative proportions) from the Southern Atlantic (diamond = inner-neritic, square = rocky-neritic, star = neritic, dot = deep ocean, black = benthic, red = demersal, blue = pelagic).
Figure 4. Two-dimensional ordination from the nonmetric multidimensional scaling (nMDS) based on the Bray–Curtis distance based on 178 fish otolith data (habitats, habits, and otolith relative proportions) from the Southern Atlantic (diamond = inner-neritic, square = rocky-neritic, star = neritic, dot = deep ocean, black = benthic, red = demersal, blue = pelagic).
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Figure 5. Mean values and t confidence intervals for the otolith relative proportions interaction between fish habitat and habit (B = benthic, D = demersal, P = pelagic, TL = total length and otolith length-OL, height-OH, and thickness-OT).
Figure 5. Mean values and t confidence intervals for the otolith relative proportions interaction between fish habitat and habit (B = benthic, D = demersal, P = pelagic, TL = total length and otolith length-OL, height-OH, and thickness-OT).
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Table
Table 1. Summary of orders and families of fish species with sagitta otoliths from the Southern Atlantic analyzed in the current study (numbers in bold indicates the number of species by order).
Table 1. Summary of orders and families of fish species with sagitta otoliths from the Southern Atlantic analyzed in the current study (numbers in bold indicates the number of species by order).
TaxaN spTaxaN sp
Albuliformes1Carangiformes18
Albulidae1Carangidae18
Anguilliformes4Atheriniformes1
Congridae2Atherinopsidae1
Muraenidae2Beloniformes5
Clupeiformes12Belonidae2
Chirocentridae1Hemiramphidae3
Clupeidae3Mugiliformes2
Engraulidae7Mugilidae2
Pristigasteridae1Bleniiformes1
Argentiniformes1Blenniidae1
Argentinidae1Order Incertae Sedis Eupercaria18
Stomiatiformes1Malacanthidae2
Sternoptychidae1Sciaenidae16
Aulopiformes5Gerreiformes5
Cholorophthalmidae5Gerreidae5
Myctophiformes9Uranoscopiformes1
Myctophidae8Pinguipedidae1
Neoscopelidae1Labriformes1
Zeiformes2Labridae1
Grammicolepididae1Ephippiformes1
Zeniontidae1Ephippidae1
Gadiformes11Chaetodontiformes1
Bregmacerotidae2Chaetodontidae1
Macrouridae4Lutjaniformes9
Merlucciidae1Haemulidae6
Moridae2Lutjanidae3
Phycidae2Spariformes3
Polimixiiformes1Sparidae3
Polimixiidae1Priacanthiformes2
Beryciformes1Priacanthidae2
Berycidae1Caproiformes1
Trachichthyiformes1Caproidae1
Trachichthyidae1Lophiiformes3
Ophidiiformes3Lophiidae1
Ophidiidae3Ogcocephalidae2
Batrachoidiformes1Tetraodontiformes6
Batrachoididae1Diodontidae2
Scombriformes13Monacanthidae1
Ariommatidae1Tetraodontidae3
Gempylidae1Pempheriformes4
Pomatomidae1Acropomatidae2
Scombridae5Percophidae2
Stromateidae1Centrachiformes2
Trichiuridae4Kyphosidae2
Syngnathiformes5Perciformes15
Centriscidae2Peristediidae1
Dactylopteridae1Scorpaenidae2
Mullidae2Sebastidae1
Gobiiformes3Serranidae7
Gobiidae3Setarchidae1
Order Incertae Sedis Carangaria6Triglidae3
Centropomidae2Number of Orders = 40
Polynemidae1Number of Families = 69
Sphyraenidae3Number of species = 179
Table
Table 2. PERMANOVA two-way based on transformed values of relative proportions OL/TL × 100, OL/OH × 100, OL/OT × 100 and OH/OTx100 (SS = sum of squares, df = degree of freedom, MS = mean square, F = statistics, p = probability value).
Table 2. PERMANOVA two-way based on transformed values of relative proportions OL/TL × 100, OL/OH × 100, OL/OT × 100 and OH/OTx100 (SS = sum of squares, df = degree of freedom, MS = mean square, F = statistics, p = probability value).
SourceSSdfMSFp
Habitat0.157330.05244.05860.0006
Habit0.100920.05053.90720.0033
Interaction0.310460.05174.00470.0001
Residual2.14411660.0129
Total2.7126177
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Santos, L.; Vaz-dos-Santos, A.M. Insights of Otoliths Morphology to Reveal Patterns of Teleostean Fishes in the Southern Atlantic. Fishes 2023, 8, 21. https://doi.org/10.3390/fishes8010021

AMA Style

Santos L, Vaz-dos-Santos AM. Insights of Otoliths Morphology to Reveal Patterns of Teleostean Fishes in the Southern Atlantic. Fishes. 2023; 8(1):21. https://doi.org/10.3390/fishes8010021

Chicago/Turabian Style

Santos, Lucinha, and André Martins Vaz-dos-Santos. 2023. "Insights of Otoliths Morphology to Reveal Patterns of Teleostean Fishes in the Southern Atlantic" Fishes 8, no. 1: 21. https://doi.org/10.3390/fishes8010021

APA Style

Santos, L., & Vaz-dos-Santos, A. M. (2023). Insights of Otoliths Morphology to Reveal Patterns of Teleostean Fishes in the Southern Atlantic. Fishes, 8(1), 21. https://doi.org/10.3390/fishes8010021

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