Folk taxonomy of the gray mullets (Mugilidae: Mugiliformes) in a marine extractivist reserve of northern Brazil

Mayra Nascimento¹, Ítalo Lutz² , Suélly Fernandes³, Camila Cardoso³, Tatiane Medeiros Rodrigues⁴, Pedro Oliva⁵ and Bianca Bentes⁴

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Abstract​

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Introduction​

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The gray mullets, family Mugilidae, are pelagic fish that are often found in large shoals, and are exploited commercially in all the regions in which they occur (Menezes, 1983; Szpilman, 2000). Seven species (all members of the genus Mugil) are found on the coast of Brazil (Herbst, Hanazaki, 2014; Menezes et al., 2015): M. curema Valenciennes, 1836, M. incilis Hancock, 1830, M. brevirostris Miranda Ribeiro, 1915, M. trichodon Poey, 1875, M. curvidens Valenciennes, 1836, M. rubrioculus Harrison, Nirchio, Oliveira, Ron & Gaviria, 2007, and M. liza Valenciennes, 1836.

In the northeastern extreme of the Brazilian state of Pará, Mugil is harvested primarily by artisanal fisheries, which use a range of different capture techniques and use these fish traditionally as a source of subsistence (Nascimento et al., 2016). The captures are made by working partnerships or by members of the fishers’ own families with incomes typically shared (Bentes et al., 2012), and the characteristics and dynamics of the system are influenced by environmental characteristics (Maccord et al., 2007; Silva et al., 2012). Nascimento et al. (2016) verified the catches of Mugilidae between the years 2008 to 2010 where 4,755 landings from 270 vessels were recorded, accounting for a production of 358.9 tons in the Ajuruteua Peninsula, Pará.

The recognition of fish species by artisanal fishers is often based on generic empirical characteristics that are passed traditionally between generations, as well as certain behavioral traits, such as reproductive events and foraging patterns (Berlin et al, 1973; Mourão, Nordi, 2002a). The recognition of species based on traditional fishers’ classification can provide an essential tool for the identification of the ecological patterns (Previero et al., 2013; Messias et al., 2019) and the correction of fishery data that may have large catches landed (Herbst, Hanazaki, 2014; Tesfamichael et al., 2014; Damasio et al., 2015). Folk taxonomy, as used in the present study, is a field of ethnobiology that elucidates the principles of the classification and naming of species of organisms based on emic knowledge (Berlin, 1992).

In general, the traditional knowledge of fishing communities is rich in detail and is often consistent with scientific classifications, and is considered to be indispensable for scientific research (Atran, 1998; Clauzet et al., 2005; Clauzet et al., 2007; Ramires et al., 2012a,b). Mourão, Nordi (2002a) found that a folk classification based on the local bioecological knowledge of fishers in northeastern Brazil was 71% consistent with the scientific taxonomy of the fish species. In 2014, Herbst, Hanazaki, registered life cycle patterns of mullets in Santa Catarina coast (Brazil) based in fishers’ knowledge, thus, they found that mullets spawning occurs throughout the coast of the Santa Catarina State and they feed in lagoons and riverine systems but also out at sea during migration, adding to scientific knowledge the fishing and biological aspects, observing by fisher.

Although several recent studies have focused on the systematics and taxonomy of the mullet family Mugilidae, the identification of species or even genera is often difficult, and a number of controversies persist, which suggest the existence of cryptic species that may have been identified erroneously in some studies (Durand et al., 2012; Konan et al., 2014; Durand, Borsa, 2015; Xia et al., 2016). The present study investigated the principal characteristics used by the artisanal fishers of the Caeté-Taperaçu Extractive Reserve in Bragança (Pará) in northern Brazil, to identify the mugilid species that occur in region, with the aim of compiling diagnostic tools for the rapid identification of these fish.

Material and methods

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Study location. The Ajuruteua coastal plain extends from Maiaú Point to the mouth of the Caeté River, covering an area of 1,570 km², which includes estuarine plains, coastal plateaus, and river, and part (652.7 km²) of the world’s most extensive continuous mangrove domain (Souza-Filho, El Robrine, 1996). The region has semidiurnal macrotides (amplitude > 4 m), a warm and humid climate, and mean annual precipitation of 2,000–3,000 mm. This region has one of the most productive fisheries in the Brazilian state of Pará (Seap/Prozee/Ibama, 2006; Isaac et al., 2011).

The Caeté-Taperaçu Marine Extractive Reserve (RESEX) is a partially protected area located in the municipality of Bragança, northeastern Pará, Brazil. This protected area covers approximately 42,100 hectares, and is inhabited by traditional populations that obtain their livelihood primarily from artisanal fishing, and are encouraged constantly to participate in local management plans and to contribute to the development of practices and strategies that permit the systematic integration of traditional and scientific knowledge (Abdala et al., 2012).

The study focused on two villages, Pescadores and Bonifácio, which are located within the Caeté-Taperaçu RESEX, on the left margin of Caeté Bay, 40 km from the town of Bragança (Pereira et al., 2009) (Fig. 1). The two villages have approximately 392 permanent inhabitants, of which, 80% have no fixed income and rely on fishing for their subsistence (Pereira et al., 2007; Gomes et al., 2009; Monteiro et al., 2009). The relevance of fishing for these communities, together with the local abundance of Mugil, determined the selection of this area for ethnotaxonomic research.

FIGURE 1| Map of Ajuruteua Plateau, on the northern coast of Brazil, showing the two villages at which the ethnotaxonomic data on the fish of the family Mugilidae were collected in the present study.

Data collection. The data were obtained in interviews based on the application of semi-structured questionnaires (S1) (Albuquerque et al., 2010) that cover taxonomy (how they recognize the species; predominant characteristics and some behavioral aspects of the species), fishing (gear and ways of catch), and the bioecology of the local ethnospecies. Fishers of varying ages resident throughout both study villages (Pescadores and Bonifácio) were interviewed using the snowball method, which is used in non-probabilistic sampling, where each interviewee indicates the next person to be interviewed in the village, based on the assumptions of the study (Bailey, 1982; Bernard, 1995; Silvano et al., 2006; Albuquerque et al., 2010). The number of interviews is assumed to be adequate when no new information is added in subsequent interviews, that is, that the answers begin to be repeated.

During the interviews, each subject was shown a catalog of photographs of mugilid species (S2), always in the same order, and asked to name the body structures and indicate the principal differences among the species, identifying the ethnospecies mentioned previously. This approach facilitates the differentiation of the species by the interviewee (Begossi et al., 2008; Albuquerque et al.,2010). Although M. margaritae Menezes, Nirchio, Oliveira & Sicchramirez, 2015, a new mullet species from Venezuela described by Menezes et al. (2015), is not known to occur on the Brazilian coast, it was included in the interviews to certify its possible occurrence by the fishers.

All the interviews were applied with the prior consent of the subject, who was required to sign a free and informed consent term with the Sistema de Autorização e Informação da Biodibversidade (SISBIO). All the interviews were recorded using a portable Sony® recorder, so that specific questions could be reviewed during data processing (Mourão, Nordi, 2003). The terms used by the fishers to differentiate the ethnospecies are summarized for comparative purposes (Tab. 1). The local seasons were classified following Moraes et al. (2005), that is, the rainy season (known locally as the winter) lasts from December to July, while the dry season (the local summer) lasts from August to November.

TABLE 1 | Characteristics and equivalences used by fishers to describe the fish of the family Mugilidae in the Caeté-Taperaçu Marine Extractive Reserve in Bragança, northern Brazil. a: Technical characteristics, b: Equivalent characteristics according to the fishers interviewed.

Analyses. The data were analyzed qualitatively following the model proposed by Mourão, Nordi (2003), which is based on the compilation of a Venn Diagram (Hunn, 1976), which is used to compare the ethnotaxonomic arrangement with the scientific classification, and determine the proximity between the folk and scientific species of mullet (Mourão, Montenegro, 2006). A presence (1)/absence (0) matrix of the atributes used to identify the species was compiled to verify the principal characteristics used by the fishers to identify their ethnospecies.

A Redundancy Analysis (RDA) was run with a Monte Carlo permutation test (9999 permutations) to evaluate the statistical significance of the results. In the manual method, with a 5% error margin, the variables were included successively in the analysis, with the dependent variables being tested against each independent variable. The data were processed in Microsoft Excel 2010 spreadsheets and the RDA was run in CANOCO 4.54 (Software for Canonical Community Ordination) (ter Braak, Šmilauer, 2002).

Results​

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Only two of the 28 fishers interviewed in the present study were woman. A majority of the interviewees (65%) have lived in their village of residence since being born, and have been involved in fishing for at least 12 years. The terminologies used to designate the body structures of Mugil were consensual in most cases, with no variation in the terms used to refer to the head, mouth, and scales. However, the fins were referred to as ‘guias’ by two interviewees, while the dorsal fin was denominated ‘esporão’ by three individuals (Fig. 2; Tab. 2).

TABLE 2 | Scientific species of Mugil genus with their respective vernacular names and number of reports by the fishers of the Caeté-Taperaçu Marine Extractive Reserve in Bragança, northern Brazil. Catalog of photographs of mugilid species to view of photographs of mugilid species used (see S2).

FIGURE 2| Morphological features of a gray mullet (Mugilidae), showing the terminology used by the fishers of the Caeté-Taperaçu Marine Extractive Reserve in Bragança, Pará, Brazil.

A total of eight generic folk taxa (corresponding to the family Mugilidae) were identified and considered ‘parentes’ or relatives. In most cases, these taxa were monotypic, that is, they corresponded to a single folk species. Six Mugil species were recognized by the fishers: M. brevirostris, M. curema, M. incilis, M. liza, M. rubrioculus,and M. trichodon. However, M. liza and M. trichodon were designated as ‘unrecognized’ or ‘absent from the region’ in a large number of cases.

Each scientific species corresponded to at least three generic folk taxa and one folk species, however, the endings of the terms often overlapped. Six interviewees referred to M. incilis as the ‘caica’,for example, but ten others classified it as the ‘tainha grande’, while M. curema, M. rubrioculus, and M. trichodon were all identified by most fishers as ‘tainha chata’ (Fig. 3).

FIGURE 3| Folk taxonomy designated by the artisanal fishers of the Caeté-Taperaçu Marine Extractive Reserve for the gray mullet (Mugilidae) and the corresponding scientific classification. The numbers within parentheses indicate the number of fishers reporting the ethnospecies. * = the number of fishers who stated that they did not know the ethnospecies or that it did not occur in the region.

The Redundancy Analysis (Figs. 4A–B) indicates that most of the ethnospecies have similar definitions. The ‘caica’, for example, can be included in a group of ethnospecies that are small and have smaller scales and eyes, together with ‘pratiqueira’, ‘sajuba/ribação’, and ‘ribação’. It was not possible to define which characteristics best fit definition of the ethnospecies ‘sajuba’, ‘barrasco’, ‘pratiqueira/barrasco’, ‘sajuba/barrasco/ribação’, and ‘irichona’, given that they are all associated with the characteristics ‘baby mullet’ and ‘sexual dimorphism’ (Fig. 4C). The ‘ribação’ is what we call the baby mullet, that’s what we call them when they come in large shoals, by the thousand (interviewee P22; 32 years old).

FIGURE 4| Results of the Redundancy Analysis (RDA) of the definition of the ethnospecies by the artisanal fishers from the Caeté-Taperaçu Marine Extractive Reserve in Bragança, northern Brazil, with the characteristics that best identify each taxon. A. CA: ‘caica’, PA: ‘pratiqueira’, PR: ‘pratiqueira/ribação’, SR: ‘sajuba/ribação’, RI: ‘ribação’, UR: ‘urubarana’, PQ: ‘pratiqueirão’, FI: ‘filhotes’; B: narrow body, B1: juvenile of large mullet, D: does not grow a lot, G: narrow headed, I: small headed, M: small eyed, P: small scales, U: does not jump, Z: smells. B. TA: ‘tainha’, TM: ‘tainha macho’, TBR: ‘tainha branca’, TB: ‘tainha boi’, TC: ‘tainha chata’, TGP: ‘tainha grande/puá’, TG: ‘tainha grande’, TCU: ‘tainha curimã’, CT: ‘caica tamatarana’, SA: ‘sajuba’, A: rounded body, C: grows a lot, E: back dark/bluish, F: flattened head, H: rounded head, J: large headed, L: large eyed, N: red eyed, O: large scales, Q: rounded scales, R: shiny scales, S: scales close together, V: smart, X: stupid. C. PB: ‘pratiqueira/barrasco’, BA: ‘barrasco’, BR: ‘barrasco/ribação’, SBR: ‘sajuba/barrasco/ribação’, IR: ‘irichona’, A1: sexual dimorphism, C1: ‘baby mullet’.

Few of the characteristics used by the fishers interviewed in the present study are consistent with those used in scientific descriptions of Mugil species. The red eyes of the ‘tainha chata’ may nevertheless correspond to the ‘reddish orange’ eyes observed in recently-preserved specimens of M. rubrioculus by Menezes et al. (2015); (Tab. 3).

TABLE 3 | Comparison of the folk and scientific taxonomies of the species of the genus Mugil (Menezes et al., 2015) identified by the artisanal fishers of the Caeté-Taperaçu Marine Extractive Reserve in Bragança, northern Brazil.

A practical guide for the identification of Mugilidae species was generated using the information obtained from the questionnaire responses (S3 and S4).

Discussion​

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A number of features have direct influence on the identification of mugilid species by the local fishers in the study area on the Ajuruteua Peninsula. Considering the often-subtle differences among the taxa of this family, the folk classification applied by the fishers may minimize the difficulties of species recognition. In this context, and considering the relative abundance and the wide knowledge of fishers about Mugil species in the catches landed by the local artisanal fisheries, the local nomenclature may facilitate the cataloging of catches on the Ajuruteua Peninsula.

The fishers almost invariably use morphological characteristics to identify Mugil, including the size and shape of the body, the configuration of its scales, head, eyes, and tail, as well as coloration, the presence or absence of teeth and odors. Even so, the fishers themselves admit to the difficulty of differentiating these mullets, given their morphological similarities: ‘the mullets are almost all pretty much the same, there is little difference between them’.

The identification of Mugil is not only linked to the morphology of the fish, but also to their behavior and biological characteristics (Mourão, Nordi, 2002b; Herbst, Hanazaki, 2014). The presence of a characteristic scent in some species, for example, has not been reported previously, and is unlikely to be a valid trait in zoological taxonomy due to its subjectivity. In the present case, however, interviewees referred specifically to characteristic scent in the ‘caica’ and ‘pratiqueira’folk species, although possibly only in the juveniles of these taxa.

In the present study, the fishers cited at least once the ethnospecies (‘caica’) to designate most small scientific species, reinforcing the idea of an association between identification and the size or age of the specimen (Clauzet et al., 2005, 2007). As the term ‘caica’ has not been associated with Mugil brevirostris, which is the smallest species of mullet found on the northern coast of Brazil (Menezes et al., 2015), and considering the scarcity of data on the biology of the Mugil species from this region, it seems likely that the generic term ‘caica’ can be associated with the recruited juveniles of various Mugil species, which may be common in local estuaries and coastal lagoons (Aguirre, Gallardo-Cabello, 2004). This reinforces the conclusion that the ontogenetic development of the organism may be among the main criteria for designation as a folk taxa.

Similarly, to the fishers interviewed in the present study, the large mullet corresponds to M. incilis, whose principal diagnostic trait in its scientific classification is the large numbers of scales (41–44) in the longitudinal line from the base of the pectoral fin to the base of the tail (Araújo et al., 2004;Menezes et al., 2015). To the fishers, however, these large mullets have smaller scales that are ‘closer together’, which may be related to large number of scales or their overlap in this species.

The scientific classification of M. curema and M. rubrioculus relies heavily on the coloration of the tip of the second dorsal fin and the base of the pectoral fin (Harrison et al., 2007; Menezes et al., 2015). However, these traits were not recognized by the artisanal fishers interviewed in the present study, who classified the two species in the same folk species, ‘tainha chata’. The folk classification prioritizes the flattened shape of the body in both species, even though this may not discriminate between the adult specimens of the two species, and there is no scientific evidence of any difference in this trait.

In general, the traits recognized by the fishers refer to the most evident characteristics of the fish, which often contradicts the criteria accepted by systematic zoologists. In some cases, however, the criteria used by the fishers may be even richer than those adopted by conventional science, including aspects of trophic ecology and spatial distribution (Silvano, Begossi, 2012; Damasio et al., 2015; Ramires et al., 2015).

The folk species ‘tainha chata’ has been fractionated into subspecies according to Berlin’s (1992) classification system, given that it corresponds to three scientific species, even though some of the traits listed for the folk species correspond to only one scientific species, in particular the presence of reddish orange eyes in the fresh specimens, found only in M. rubrioculus. Many folk classification systems identify species that correspond to more than one scientific taxon (Pinto et al., 2016; Carvalho et al., 2018; Mourão, Barbosa Filho, 2018).

Mugil margaritae, the new mullet species described by Menezes et al. (2015) was not recognized by 12 (42.9%) of the fishers, with one referring to the fish as a ‘captive species, which occurs only in southern Brazil’. Up to now, M. margaritae has been recorded only on the coast of Venezuela, although it is not entirely unlikely that it may occur in Brazilian waters, given the proximity of these habitats (Menezes et al., 2015).

The designations ‘sajuba/barrasco/ribação’, ‘barrasco’, ‘pratiqueira/barrasco’, and ‘irichona’ include ‘male specimens’ and ‘juveniles.’The ‘barrasco’ is a type of ‘ribação’ that starts off as a male and grows as big as the ‘tainha chata’, but it is fatter, and rather than eggs, it produces this white stuff that comes out like milk if you squeeze its belly (interviewee P7; 58 years old). The ‘irichona’ is small, but it has a belly because it is always spawning (interviewee P12; 61 years old).

At the present time, the fishery statistics of the region register the species M. curema, M. liza, and Mugil sp. under the vernacular names ‘tainha’ and ‘caica’, without distinguishing the ethnospecies (Lutz et al., 2016), or only as ‘tainha’ (Nascimento et al., 2016). As observed in the present study, the term ‘tainha’ is the vernacular for all the Mugil species that occur in the region, that is, ‘mullet’. It is important to note, however, that this lack of precision in the logging of catches may not only reflect cultural misunderstandings, but also impact management practices, given that some species (M. liza) are already overfished in some regions (MPA, 2015), while others (e.g., M. curema, M. incilis, and M. rubrioculus) are still abundant the northern coast of Brazil (Giarrizzo et al., 2013).

Many of the popular names and the folk classification of the Mugil species of the northern coast of Brazil are local denominations. In southern Brazil, M. curema is widely denominated ‘parati’, for example, while M. liza is referred to as the ‘curimã’ or ‘tainha’ (Menezes, 1983; Seckendorff, Azevedo, 2007; Mendonça, Bonfante, 2011). Given this, new studies are necessary in other coastal regions of Brazil to determine the specificity of the vernacular names recorded up to now (Fischer, 2013).

This regional vernacular reinforces the need for an in-depth investigation of fish ethnotaxonomy not only of Mugil, but of all groups, but in particular those of significant commercial interest (Freire, Pauly, 2005). In addition, fishery management that does not integrate cultural practices and traditional knowledge will distance public policies from local realities, weakening top-down management strategies, an all-too common phenomenon in Brazilian politics. Local knowledge of the diversity of organisms reflects their economic, cultural, and psychological importance (Mourão, Nordi, 2002a), and should be prioritized in any initiative for fishery or conservation management, such as producing a guide that assists in species identification: Ethnoguide of the mullet species of the Amazon coast (S3) and the Portuguese version “Etnoguia das espécies de tainhas da costa Amazônica” (S4).

Acknowledgments​

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We would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the scientific initiation scholarship awarded to the first author, and everyone who contributed directly or indirectly to this study.

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Authors

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Mayra Nascimento¹, Ítalo Lutz² , Suélly Fernandes³, Camila Cardoso³, Tatiane Medeiros Rodrigues⁴, Pedro Oliva⁵ and Bianca Bentes⁴

^[1]    RARE Brasil Organização, Avenida Governador José Malcher, 1094, Bairro Nazaré, 66055-260 Belém, PA, Brazil. (MN) mayra.nascimento@ymail.com.

^[2]    Laboratório de Genética Aplicada, Instituto de Estudos Costeiros, Universidade Federal do Pará, Alameda Leandro Ribeiro S/N, Bairro Aldeia, 68600-000 Bragança, PA, Brazil. (IL) italofreitas91@hotmail.com (corresponding author).

^[3]    Instituto de Estudos Costeiros, Universidade Federal do Pará, Alameda Leandro Ribeiro S/N, Bairro Aldeia, 68600-000 Bragança, PA, Brazil. (SF) suellycrispereira@hotmail.com, (CC) camilanacbio@gmail.com.

^[4]    Núcleo de Ecologia Aquática e Pesca da Amazônia, Universidade Federal do Pará, Avenida Perimetral s/n, Bairro Guamá, Belém, PA, Brazil. (TMR) tnr.medeiros@gmail.com, (BB) bianca@ufpa.br.

^[5]    Laboratório de Cartografia, Geoprocessamento e Modelagem, Instituto de Estudos Costeiros, Universidade Federal do Pará, Alameda Leandro Ribeiro s/n, Bairro Aldeia, 68600-000 Bragança, PA, Brazil. (PO) chira.oliva@gmail.com.

Authors’ Contribution

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Mayra Nascimento: Conceptualization, Formal analysis, Investigation, Methodology, Software, Validation, Writing-original draft, Writing-review and editing.

Ítalo Lutz: Formal analysis, Software, Supervision, Visualization, Writing-review and editing.

Suélly Fernandes: Data curation, Project administration, Visualization.

Camila Cardoso: Investigation, Project administration, Supervision.

Tatiane Medeiros Rodrigues: Visualization, Writing-review and editing.

Pedro Oliva: Methodology, Validation.

Bianca Bentes: Conceptualization, Investigation, Resources, Supervision, Writing-review and editing.

Ethical Statement​

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Sistema de Autorização e Informação da Biodibversidade (SISBIO – license number 47679/1).

Competing Interests

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The author declares no competing interests.

How to cite this article

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Nascimento M, Lutz I, Fernandes S, Cardoso C, Rodrigues TM, Oliva P, Bentes B. Folk taxonomy of the gray mullets (Mugilidae: Mugiliformes) in a marine extractivist reserve of northern Brazil. Neotrop Ichthyol. 2022; 20(4):e220061. https://doi.org/10.1590/1982-0224-2022-0061

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

© 2022 The Authors.

Diversity and Distributions Published by SBI

Accepted October 25, 2022 by Osmar Luiz

Submitted June 30, 2022

Epub December 19, 2022