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Biota Neotropica

versão On-line ISSN 1676-0611

Biota Neotrop. vol.18 no.1 Campinas  2018  Epub 15-Jan-2018

https://doi.org/10.1590/1676-0611-bn-2017-0394 

Inventory

Biodiversity of Holocene marine fish of the southeast coast of Brazil

Biodiversidade de peixes marinhos do Holoceno da costa Sudeste brasileira

Augusto Barros Mendes1 

Michelle Rezende Duarte1  * 

Edson Pereira Silva1 

1Universidade Federal Fluminense, Departamento de Biologia Marinha, Niterói, Brazil.


Abstract

Middens are archaeological sites dating between 8,000 and 1,000 years before present and are commonly found on the Brazilian coast. Data were collected from 68 middens allowing an inventory of 142 fish species, most of them recorded in no more than five sites. Conversely, Micropogonias furnieri and Pogonias cromis had the highest frequencies of occurrence. The biogeographic, ecological and economic data showed that most of the identified fish are widely distributed in the Western Atlantic (59.72%) and inhabit estuarine environments (53.99%), while most species have a demersal habit (35.92%) and exhibit oceanic migratory behaviour (28.87%). Lastly, the surveyed fish are predominantly carnivorous (72.54%) with some commercial value (96.48%). Chi-squared tests comparing midden inventory and current ichthyofauna checklists failed to show significant differences between them (p > 0.99). Thus, the results indicate that zoo-archaeological fish remains are key evidence of Holocene biodiversity and may help the establishment of more complete baselines.

Keywords:  Baselines; Fishermen-Gatherers-Hunters; Ichthyofauna; Middens; Species richness; Zooarchaeology

Resumo

Sambaquis são sítios arqueológicos, datando entre 8,000 e 1,000 anos antes do presente, encontrados na costa brasileira. Neste trabalho, dados ictiológicos referentes a 68 sambaquis da costa Sudeste do Brasil foram compilados e construído um inventário de referência no qual constam 142 espécies, a maioria das quais com registro em não mais que cinco sítios. Por outro lado, as espécies Micropogonias furnieri e Pogonias cromis apresentaram alta frequência de ocorrência nos sambaquis. Os dados biogeográficos, ecológicos e econômicos mostraram que a maioria das espécies registradas nos sambaquis são de ampla distribuição no Atlântico Ocidental (59.72%), habitam ambientes estuarinos (53.99%), tem um hábito demersal (35.92%) e comportamento oceânico migratório (28.87%). A maioria dos registros diz respeito a peixes carnívoros (72.54%) e com algum valor comercial (96.48%). A comparação da lista de ictiofauna registrada para os sambaquis com uma lista construída com base em inventários atuais de peixes para mesma região não mostrou diferenças significativas (teste de qui-quadrado, p> 0.99). Dessa forma, os resultados apresentados indicam que os vestígios de ictiofauna encontrados em sambaquis constituem uma amostra relevante da biodiversidade do Holoceno podendo ser muito úteis na construção de inventários de referências mais completos da fauna ictiológica da costa brasileira.

Palavras-chave:  Ictiofauna; Inventário de referências; Pescadores-Coletores-Caçadores; Riqueza de espécies; Sambaquis; Zooarqueologia

Introduction

Biodiversity-related research has developed significantly since the 1990s, when ecologists worldwide, concerned with anthropogenic effects on ecosystems, intensified their studies of environmental issues (Amaral & Jablonsky 2005, Lewinsohn & Prado 2005). Biodiversity is defined by the Convention on Biological Diversity as the variability among living beings of all origins, including terrestrial, marine and other aquatic ecosystems, and their associated ecological complexes, including intra- and inter-species as well as ecosystem diversity (Arruda et al. 2000).

Recently, the Census of Marine Life raised the estimated number of known marine species from approximately 230,000 to between 1 and 1.4 million; more than 1,200 new species were identified among specimens collected in known and previously unexplored waters (Costello et al. 2010). Furthermore, in a review of research related to Brazilian biodiversity, Siqueira et al. (2015) found that only 21% of 1,156 references from 2009 to 2014 addressed the richness of aquatic species, indicating that the marine environment remains little studied and is therefore largely unknown. Finally, baselines for long-term studies of marine biodiversity are scarce (Knowlton & Jackson 2008, Pinnegar & Engelhard 2008).

Baselines are reference biodiversity inventories that directly assess the species composition of a specific site for a given spatial extent and time. The data generated by such inventories are one of the most important tools for the conservation and management of natural areas, especially the associated endangered species (Silveira et al. 2010). The establishment of baselines is particularly important for the conservation of marine fish because this group is intensely exploited due to their commercial value and account for a significant share of global fishery production. In Brazil, fisheries have been key to the development of the country, concentrating 70% of the population near the coast, and the sea plays a key role in its history, culture and economy (Rosa & Lima 2008).

To be as accurate as possible, reference inventories of ichthyological fauna should include not only current data but also historic and prehistoric (fossil/sub-fossil) data as well (Furon 1969, Warwick & Light 2002, Willis & Birks 2006, Froyd & Willis 2008, Stahl 2008). However, collecting data on the species compositions of the past is complicated because fossil/sub-fossil records are largely characterised by being incomplete; that is, the biological data (species morphology, richness, diversity and evenness, among others) preserved in those records are influenced by non-linear modifications that occur from the time of death to the final burial of an organism (Ritter & Erthal 2016) and the species preservation potential (Prummel & Heinrich 2005). Therefore, prehistoric records are relatively scarce (Bittencourt et al. 2015).

However, there are some Holocene species composition records from sources including beaches, death assemblages and middens. Beaches and restingas originated in the Holocene, but their characteristics prevent the establishment of a chronology (Lacerda et al. 1984). Conversely, death assemblages allow for accurate chronological estimates and have the great advantage of being natural, thus showing actual tanatocenoses, but these formations are rare along the Brazilian coast (Ritter & Erthal 2016). However, middens, which are archaeological sites dating between 8,000 and 1,000 years before present (BP, according to the convention before 1950), are commonly found on the Brazilian coast and allow a chronology to be established because they show a stratigraphic sequence of different species compositions (Kneip et al. 1988, Gaspar 1998, Scheel-Ybert et al. 2009, Klokler et al. 2010).

Middens were built by groups of prehistoric fishermen-gatherers-hunters, which explains why they are found in estuarine areas at the intersections of rivers and the sea. These sites contain a wealth of resources including sediments, coal, lithic material and, above all, faunal remains. High numbers of molluscs and crustaceans, including sea and sand crabs, as well as echinoderms and fish have been found among the marine zoo-archaeological remains recovered from middens (DeBlasis et al. 2007, Figuti 1993, Lima 2000, Lima et al. 2003).

For fish species, their zoo-archaeological remains indicate their usefulness to midden populations, so most species recorded at these sites have a cultural meaning and show sociocultural and identity relationships and spatiotemporal economic characteristics (Figuti 1998, Barbosa-Guimarães 2013, Wagner & Silva 2014, Lopes et al. 2016). Accordingly, because the ichthyological remains in middens represent the diversity of prehistoric fishes obtained from a selective catch, this data source underestimates the diversity of Holocene fish. That is, the species diversity of the remains found in the middens is lower than that in natural communities (Gonzalez 2005, Costa et al. 2012).

Although midden fish records underestimate natural diversity, they are a key source of information on the ichthyological fauna of the past because prehistoric people could only have caught the fish available in the environments at the time. Furthermore, by-catch occurred; that is, species with no known anthropological relevance were incidentally fished with target species (Reitz & Wing 2008, Villagran & Gianini 2014, Beuclair et al. 2016). Therefore, midden records are a good indicator of Holocene biodiversity, providing data on fish species composition, abundance, distribution and richness as well as cultural information (diet, fishing gear, ritualistic symbols, ornaments and artefacts) (Souza et al. 2010a, Souza et al. 2010b, Faria et al. 2014, Mendes et al. 2014, Rodrigues et al. 2016a, Rodrigues et al. 2016b, Beuclair et al. 2016, Silva et al. 2016).

Thus, although middens are artificial accumulations (that is, built by prehistoric populations) of biological material, the presence or absence of species at these sites provides sufficient data to create a taxonomic list that may be useful for defining a historical record of biological diversity (Stahl 2008), so this study presents an inventory of marine ichthyological biodiversity from southeast Brazilian middens. This list is the first comprehensive inventory of Holocene fish fauna from this region and may help elucidate past natural ocean events, enabling the establishment of more complete baselines to inform conservation and management measures.

Methods

The inventory was constructed from an extensive bibliographical survey of the libraries of universities and institutions with archaeological collections from sites along the southeast coast of Brazil as well as online databases (Web of Knowledge, Scientific Electronic Library Online - SciELO, Google Scholar and the Thesis Database of the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES)). The data sources included scientific articles and books, thesis, dissertations, monographs and technical reports.

The list of species was analysed in terms of absolute and relative species richness and absolute and relative frequencies of occurrence. Absolute species richness is the number of species present at a sampled site, while the relative species richness is the ratio between that number and the total number of species. Similarly, the absolute frequency of occurrence is the number of sites at which a specific species occurs, and the relative frequency is the ratio between that number and the total number of sites.

Furthermore, taxonomic, biogeographic, ecological and economic data on the inventoried species were collected from the FishBase database (Froese & Pauly 2017) and categorised by distribution (range of occurrence), environment (habitat), habit (way of life at specific locations in the water column), behaviour (migratory movements), feeding guild (food requirements) and commercial value (demand for the species in the fish market).

The checklists constructed by Bizerril & Costa (2001) for Rio de Janeiro and Menezes (2011) for São Paulo were compared along with the inventory from the midden zoo-archaeological remains from this study to current ichthyological inventories for the same regions, and the species catalogued in speciesLink, a digital information system that integrates primary data from scientific collections in real time, for Espírito Santo were surveyed. Furthermore, a chi-squared test (χ2) was performed to assess whether the ratio of commercial and non-commercial species in the midden fish inventory differed significantly from the ratios in current fish checklists.

Results

Data were collected from 68 middens distributed in 19 locations along the coast of three states of the Southeast Region of Brazil: Espírito Santo (ES), Rio de Janeiro (RJ) and São Paulo (SP) (Figure 1). The location with the highest number of middens (12 sites, 17.65%) was Paraty in the state of Rio de Janeiro, which also had the highest number of documented sites (53, 77.95%). Conversely, Espírito Santo had the lowest number of middens (2, 2.94%; Table 1). From these total of 68 middens, 49 of them had records of 14C radiocarbonic dates (Figure 2). Occupation time ranged from 8,182 BP (Sambaqui de Camboinhas) to 675 BP (Sítio do Major). However, the majority of them were built and occupied during the period defined by Walker et al. (2012) as Late Holocene.

Figure 1 Map of the Southeast Region of Brazil with the locations of the inventoried middens.  

Table 1 Middens inventoried in the Southeast Region of Brazil with absolute (Rspp) and relative (relative Rspp) species richness and the associated references from the literature. 

Location Midden Code Rspp Relative Rspp References
Angra dos Reis Sambaqui da Caieira 1 27 0.190 Lima 1991, DSc Thesis, FFLCH-USP
Lopes et al. 2016, PLoS One 11(6): 1-36
Sambaqui da Caieira II 2 29 0.204 Lima 1991, DSc Thesis, FFLCH-USP
Figuti 1998, Revista Arqueologia 11: 57-70
Sambaqui do Algodão 3 71 0.500 Lima 1991, DSc Thesis, FFLCH-USP
Lopes et al. 2016, PLoS One 11(6): 1-36
Figuti 1998, Revista Arqueologia 11: 57-70
Sítio do Bigode I 4 38 0.268 Lima 1991, DSc Thesis, FFLCH-USP
Lopes et al. 2016, PLoS One 11(6): 1-36
Figuti 1998, Revista Arqueologia 11: 57-70
Sítio do Major 5 47 0.331 Lima 1991, DSc Thesis, FFLCH-USP
Lopes et al. 2016, PLoS One 11(6): 1-36
Figuti 1998, Revista Arqueologia 11: 57-70
Sítio do Peri 6 39 0.275 Lima 1991, DSc Thesis, FFLCH-USP
Lopes et al. 2016, PLoS One 11(6): 1-36
Figuti 1998, Revista Arqueologia 11: 57-70
Sítio Ilhota do Leste 7 14 0.099 Lima 1991, DSc Thesis, FFLCH-USP
Lessa & Carvalho 2015, Bol Mus Para Emílio Goeldi 10: 489-507
Tenório 2003, DSc Thesis, PUC-RS
Tenório 2003, Anais XII Congresso da SAB
Lessa & Coelho 2010, Rev Mus Arqueol Etnol 20: 77-89
Sambaqui do Acaiá 8 23 0.162 Lopes et al. 2016, PLoS One 11(6): 1-36
Macaé Sítio da Ilha de Santana 9 13 0.092 Lima 1991, DSc Thesis, FFLCH-USP
Magé Sítio Saracuruna 10 5 0.035 Lima 1991, DSc Thesis, FFLCH-USP
Mendonça de Souza 1981, Pré-história Fluminense, Instituto Estadual do Patrimônio Cultural, RJ
Mello & Mendonça de Souza 1977, Nheengatu 1: 43-58
Sambaqui Rio das Pedrinhas 11 9 0.063 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Sambaqui de Sernambetiba 12 2 0.014 Beltão et al. 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 145-155
Perez et al. 1995 In: Arqueologia do Estado do Rio de Janeiro, Arquivo Público do Estado do RJ pp. 29-34
Sambaqui de Amourins 13 1 0.007 Heredia et al. 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 175-188
Paraty Abrigo Ponta do Leste I 14 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Abrigo Ponta do Leste II 15 5 0.035 Mendonça de Souza 1981, Pré-história Fluminense, Instituto Estadual do Patrimônio Cultural, RJ
Sambaqui Olho D'Água 16 3 0.021 Mendonça de Souza 1981, Pré-história Fluminense, Instituto Estadual do Patrimônio Cultural, RJ
Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Toca do Cassununga 17 5 0.035 Mendonça de Souza 1981, Pré-história Fluminense, Instituto Estadual do Patrimônio Cultural, RJ
Toca dos Caboclos I 18 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Abrigo da Ilha Pelada 19 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Sítio Trindade III 20 6 0.042 Mendonça de Souza 1981, Pré-história Fluminense, Instituto Estadual do Patrimônio Cultural, RJ
Sambaqui do Forte 21 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Sambaqui do Perequê-Açu 22 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Sambaqui da Ilha Comprida 23 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Sambaqui do Pouso 24 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Sambaqui de Mamanguá 25 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Saquarema Sambaqui da Beirada 26 21 0.148 Kneip 1994, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 2
Magalhães et al. 2001, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 5
Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Kneip et al. 1988, Revista de Arqueologia 5: 41-54
Kneip et al. 1995 In: Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ 3: 3-12
Barbosa-Guimarães 2012, Sci Plena 8: 1-9
Sambaqui da Madressilva 27 8 0.056 Magalhães et al. 2001, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 5
Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Kneip 1997, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 4
Sambaqui da Pontinha 28 17 0.120 Kneip 1994, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 2
Magalhães et al. 2001, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 5
Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Kneip et al. 1995 In: Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ 3: 3-12
Sambaqui de Saquarema 29 24 0.169 Lopes et al. 2016, PLoS One 11(6): 1-36
Magalhães et al. 2001, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 5
Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Sambaqui do Moa 30 15 0.106 Kneip 1994, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 2
Magalhães et al. 2001, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 5
Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Machado 2014, MSc Thesis, PPGG-UFPA
Silveira 2001, DSc Thesis, FFLCH-USP
Costa et al. 2012, Rev Mus Arqueol Etnol 22: 51-65
Sambaqui do Saco 31 8 0.056 Magalhães et al. 2001, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 5
Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Kneip 1997, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 4
Sambaqui do Jaconé 32 9 0.063 Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Sambaqui de Mombaça I 33 3 0.021 Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Sambaqui de Itaúnas 34 5 0.035 Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Sambaqui Manitiba I 35 20 0.141 Lopes et al. 2016, PLoS One 11(6): 1-36
Magalhães et al. 2001, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ, 5
Barbosa-Guimarães 2013, An Acad Bras Ciênc 85: 415-429
Barbosa-Guimarães 2007, DSc Thesis, MAE-USP
Sambaqui da Ponte do Girau 36 3 0.021 Lopes et al. 2016, PLoS One 11(6): 1-36
Cabo Frio Sambaqui do Forte 37 2 0.014 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Costa et al. 2012, Rev Mus Arqueol Etnol 22: 51-65
Kneip 1980, Separata de Pesquisas, Série Antropologia, 31
Kneip et al. 1975, Separata da Revista do Museu Paulista-USP
Kneip et al. 1975, An Acad Bras Ciênc 47: 91-97
Gaspar 1991, DSc Thesis, FFLCH-USP
Gaspar 2003, Pesquisas, Série Antropologia-IAP 59: 1-163
Souza 2009, Monography, GeoQuater-UFRJ
Abrigo Arraial do Cabo 38 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Sambaqui Boca da Barra 39 10 0.070 Gaspar 1991, DSc Thesis, FFLCH-USP
Gaspar 2003, Pesquisas, Série Antropologia-IAP 59: 1-163
Barbosa 1999, MSc Thesis, PGCA-UFF
Sítio do Meio 40 1 0.007 Gaspar 1991, DSc Thesis, FFLCH-USP
Gaspar 2003, Pesquisas, Série Antropologia-IAP 59: 1-163
Gaspar & Scaramella 1992, Anais VI Reunião Científica da SAB
Sambaqui da Salina Peroano 41 2 0.014 Gaspar 1991, DSc Thesis, FFLCH-USP
Gaspar 2003, Pesquisas, Série Antropologia-IAP 59: 1-163
Franco & Gaspar 1992, Anais VI Reunião Científica da SAB
Sítio Ilha de Cabo Frio 42 15 0.106 Lopes et al. 2016, PLoS One 11(6): 1-36
Armação de Búzios Geribá II 43 1 0.007 Gaspar 1991, DSc Thesis, FFLCH-USP
Gaspar 2003, Pesquisas, Série Antropologia-IAP 59: 1-163
Arraial do Cabo Sítio Colônia de Pesca 44 2 0.014 Gaspar 1991, DSc Thesis, FFLCH-USP
Mendonça de Souza et al. 1983-1984, Arquivos do Museu de História Natural-UFMG 8/9: 107-119
Tenório et al. 2010, Rev Mus Arqueol Etnol 20: 127-145
Tenório et al. 2005, Anais XIII Congresso da SAB
Sítio Ponta da Cabeça 45 9 0.063 Gaspar 1991, DSc Thesis, FFLCH-USP
Tenório et al. 2010, Rev Mus Arqueol Etnol 20: 127-145
Tenório et al. 2005, Anais XIII Congresso da SAB
Sítío do Condomínio do Atalaia 46 1 0.007 Tenório et al. 2005, Anais XIII Congresso da SAB
Usiminas 47 24 0.169 Lopes et al. 2016, PLoS One 11(6): 1-36
Mangaratiba Sambaqui do Saí 48 5 0.035 Mendonça de Souza & Mendonça de Souza 1981-1982, Arquivos do Museu de História Natural-UFMG 6/7: 109-131
Rio das Ostras Sambaqui da Tarioba 49 15 0.106 Tuna 2015, MSc Thesis, PBMAC-UFF
Niterói Sambaqui de Camboinhas 50 12 0.085 Lopes et al. 2016, PLoS One 11(6): 1-36
Souza Cunha et al. 1981 In: Pesquisas arqueológicas no litoral de Itaipu, Niterói, RJ, Cia de Desenvolvimento Territorial
Souza Cunha et al. 1986, Anais XXX Congresso Brasileiro de Geologia
Vogel & Veríssimo 1981 In: Pesquisas arqueológicas no litoral de Itaipu, Niterói, RJ, Cia de Desenvolvimento Territoria
Kneip & Pallestrini 1984 In: Restigas: origem, estrutura, processo, CEUFF
Kneip 1979, Pesquisas de salvamento em Itaipu, Niterói, Rio de Janeiro, Cia de Desenvolvimento Territorial
Kneip 1995, Documento de Trabalho, Série Arqueologia, Museu Nacional-UFRJ 2: 83-102
Itaboraí Sambaqui Sampaio I 51 1 0.007 Pinto 2009, MSc Thesis, PPGArq-UFRJ
Rio de Janeiro Sambaqui da Embratel 52 2 0.014 Kneip et al. 1984 In: Restigas: origem, estrutura, processo, CEUFF
Kneip et al. 1984, Revista de Pré-História 6: 334-360
Sambaqui do Zé Espinho 53 12 0.085 Kneip et al. 1984 In: Restigas: origem, estrutura, processo, CEUFF
Kneip et al. 1984, Revista de Pré-História 6: 334-360
Vogel 1987 In: Coletores e pescadores pré-históricos de Guaratiba, Rio de Janeiro, EDUFF
Kneip et al. 1986, Separata da Rev Mus Pau
Cubatão Sambaqui Piaçaguera 54 63 0.444 Fischer 2012, MSc Thesis, MAE-USP
Gonzalez 2005, DSc Thesis, MAE-USP
Gonzalez & Amenomori 2003, Rev Mus Arqueol Etnol 13: 25-37
Filippini & Eggers 2005-2006, Rev Mus Arqueol Etnol 5-16: 165-180
Garcia 1972, DSc Thesis, IB-USP
Garcia & Uchôa 1980, Revista de Pré-História 2: 5-81
Duarte 1968, O sambaqui visto através de alguns sambaquis, Instituto de Pré-História da USP
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COSIPA 1 55 35 0.246 Figuti 1998, Revista Arqueologia 11: 57-70
Gonzalez 2005, DSc Thesis, MAE-USP
Figuti 1993, Rev Mus Arqueol Etnol 3: 67-80
Figuti 1994-1995, Revista de Arqueologia 8: 267-283
COSIPA 2 56 16 0.113 Gonzalez 2005, DSc Thesis, MAE-USP
Gonzalez & Amenomori 2003, Rev Mus Arqueol Etnol 13: 25-37
Figuti 1993, Rev Mus Arqueol Etnol 3: 67-80
Figuti 1994-1995, Revista de Arqueologia 8: 267-283
COSIPA 3 57 9 0.063 Figuti 1987, Institut de Paleontologie Humaine, Paris
Figuti 1989, Revista de Pré-História 7: 112-126
COSIPA 4 58 36 0.254 Figuti 1998, Revista Arqueologia 11: 57-70
Gonzalez 2005, DSc Thesis, MAE-USP
Figuti 1993, Rev Mus Arqueol Etnol 3: 67-80
Figuti 1994-1995, Revista de Arqueologia 8: 267-283
Ubatuba Sítio Tenório 59 38 0.268 Figuti 1998, Revista Arqueologia 11: 57-70
Gonzalez 2005, DSc Thesis, MAE-USP
Gonzalez & Amenomori 2003, Rev Mus Arqueol Etnol 13: 25-37
Filippini & Eggers 2005-2006, Rev Mus Arqueol Etnol 5-16: 165-180
Garcia 1972, DSc Thesis, IB-USP
Amenomori 1999, MSc Thesis, FFLCH-USP
Sítio do Mar Virado 60 28 0.197 Gonzalez & Amenomori 2003, Rev Mus Arqueol Etnol 13: 25-37
Amenomori 1999, MSc Thesis, FFLCH-USP
Amenomori 2005, DSc Thesis, MAE-USP
Uchôa 2009, CLIO-Série Arqueológica 24: 7-40
Nishida 2001, MSc Thesis, MAE-USP
Sítio Couves 1 61 6 0.042 Amenomori 1999, MSc Thesis, FFLCH-USP
Guarujá Sambaqui do Buracão 62 54 0.380 Gonzalez & Amenomori 2003, Rev Mus Arqueol Etnol 13: 25-37
Borges 2015, DSc Thesis, Muséum National D'Histoire Naturelle de Paris
Duarte 1968, O sambaqui visto através de alguns sambaquis, Instituto de Pré-História da USP
Amenomori 2005, DSc Thesis, MAE-USP
Sambaqui do Mar Casado 63 48 0.338 Gonzalez 2005, DSc Thesis, MAE-USP
Gonzalez & Amenomori 2003, Rev Mus Arqueol Etnol 13: 25-37
Borges 2015, DSc Thesis, Muséum National D'Histoire Naturelle de Paris
Duarte 1968, O sambaqui visto através de alguns sambaquis, Instituto de Pré-História da USP
Sambaqui Maratuá 64 24 0.169 Gonzalez 2005, DSc Thesis, MAE-USP
Ilhabela Sambaqui Abrigo Sul 65 2 0.014 Bendazzoli 2014, DSc Thesis, MAE-USP
Iguape Abrigo do Pindú 66 2 0.014 Bendazzoli 2014, DSc Thesis, MAE-USP
Bonetti 1997, MSc Thesis, FFLCH-USP
Serra Sambaqui do Péricles II 67 4 0.028 Rhea Estudos e Projetos Ltda 2009, Salvamento e monitoramento arqueológico na área do Alphaville Jacuhy
Vitória Sítio Campus 2 68 3 0.021 Perota 1972, Revista de Cultura da UFES 3: 39-45

Figure 2 Graphic with the 14C radiocarbonic dates of the 49 inventoried middens of the Southeast Region of Brazil. In the x axis are the middens (codes defined at Table 1) and in the y axis are the ranges of 14C radiocarbonic dating (given in year before present) found in the literature. The different periods of the Holocene were defined based in Walker et al. (2012): Early Holocene (11,700 ~ 8,200 BP), Middle Holocene (8,200 ~ 4,200 BP) and Late Holocene (4,200 BP ~ till today). 

A total of 142 fish species were inventoried, and most taxa belonged to class Osteichthyes (105, 73.94%). Sciaenidae was the most represented family with 21 species, and Cynoscion Gill, 1861 was the genus with the highest number of species, seven in total (Table 2). Of the Chondrichthyes (37, 26.06%), the family with the highest number of species was Carcharhinidae with 17 species, and the most representative genus was Carcharhinus Blainville, 1816 with 12 species (Table 3).

Table 2 Marine fish of class Osteichthyes from middens in the Southeast Region of Brazil with their absolute (F) and relative (relative F) frequencies of occurrence as well as the midden(s) in which they were recorded. The codes representing the middens are defined in Table 1

Family Species F Relative F Midden(s)
Albulidae Albula nemoptera (Fowler, 1911) 1 0.015 3
Ariidae Aspistor luniscutis (Valenciennes, 1840) 19 0.279 2, 3, 4, 5, 6, 11, 27, 28, 30, 31, 35, 54, 55, 58, 59, 60, 62, 63, 64
Bagre bagre (Linnaeus, 1766) 23 0.338 1, 2, 3, 4, 5, 6, 9, 10, 11, 20, 21, 22, 23, 24, 25, 48, 50, 54, 55, 58, 59, 62, 63
Bagre marinus (Mitchill, 1815) 18 0.265 1, 2, 3, 4, 5, 6, 8, 26, 28, 30, 35, 49, 53, 54, 62, 63, 64, 67
Cathorops spixii (Agassiz, 1829) 18 0.265 2, 3, 4, 5, 6, 26, 28, 29, 30, 35, 54, 55, 57, 58, 59, 62, 63, 64
Genidens barbus (Lacepède, 1803) 33 0.485 2, 3, 4, 5, 6, 10, 11, 12, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 48, 50, 54, 55, 58, 59, 60, 62, 63
Genidens genidens (Cuvier, 1829) 19 0.279 2, 3, 4, 5, 6, 8, 26, 28, 29, 35, 49, 50, 54, 55, 58, 59, 62, 63, 64
Genidens machadoi (Miranda Ribeiro, 1918) 1 0.015 54
Notarius grandicassis (Valenciennes, 1840) 12 0.176 2, 3, 4, 5, 6, 54, 55, 58, 59, 62, 63, 64
Potamarius grandoculis (Steindachner, 1877) 2 0.029 54, 63
Balistidae Balistes capriscus Gmelin, 1789 2 0.029 62, 63
Balistes vetula Linnaeus, 1758 12 0.176 1, 2, 3, 4, 5, 6, 9, 54, 55, 58, 59, 60
Carangidae Caranx crysos (Mitchill, 1815) 4 0.059 29, 54, 62, 63
Caranx hippos (Linnaeus, 1766) 23 0.338 1, 2, 3, 4, 5, 6, 8, 9, 26, 27, 28, 29, 30, 31, 35, 47, 50, 53, 54, 62, 63, 64, 67
Caranx ruber (Bloch, 1793) 1 0.015 62
Chloroscombrus chrysurus (Linnaeus, 1766) 1 0.015 62
Oligoplites saurus (Bloch & Schneider, 1801) 4 0.059 8, 26, 28, 30
Selar crumenophthalmus (Bloch, 1793) 1 0.015 8
Selene vomer (Linnaeus, 1758) 3 0.044 8, 47, 62
Seriola dumerili (Risso, 1810) 2 0.029 62, 63
Trachinotus falcatus (Linnaeus, 1758) 1 0.015 65
Trachurus lathami Nichols, 1920 1 0.015 54
Centropomidae Centropomus ensiferus Poey, 1860 3 0.044 3, 5, 42
Centropomus parallelus Poey, 1860 6 0.088 35, 47, 54, 62, 63, 64
Centropomus undecimalis (Bloch, 1792) 16 0.235 3, 11, 26, 27, 28, 29, 30, 32, 35, 54, 57, 62, 63, 64, 67, 69
Coryphaenidae Coryphaena hippurus Linnaeus, 1758 1 0.015 8
Dactylopteridae Dactylopterus volitans (Linnaeus, 1758) 5 0.074 9, 29, 60, 62, 63
Diodontidae Chilomycterus spinosus (Linnaeus, 1758) 12 0.176 1, 2, 3, 4, 5, 6, 47, 49, 54, 55, 58, 59
Diodon hystrix Linnaeus, 1758 11 0.162 2, 3, 4, 5, 6, 9, 54, 55, 58, 59, 63
Eleotridae Dormitator maculatus (Bloch, 1792) 1 0.015 54
Eleotris pisonis (Gmelin, 1789) 1 0.015 62
Elopidae Elops saurus Linnaeus, 1766 1 0.015 54
Ephippidae Chaetodipterus faber (Broussonet, 1782) 21 0.309 1, 2, 3, 4, 5, 6, 7, 9, 29, 35, 39, 47, 49, 53, 54, 55, 58, 59, 60, 61, 62
Gerreidae Diapterus auratus Ranzani, 1842 2 0.029 3, 5
Diapterus rhombeus (Cuvier, 1829) 5 0.074 3, 5, 6, 54, 62
Eugerres brasilianus (Cuvier, 1830) 2 0.029 54, 62
Gerres cinereus (Walbaum, 1792) 1 0.015 3
Haemulidae Anisotremus surinamensis (Bloch, 1791) 3 0.044 54, 62, 63
Anisotremus virginicus (Linnaeus, 1758) 6 0.088 1, 3, 4, 5, 6, 47
Conodon nobilis (Linnaeus, 1758) 13 0.191 2, 3, 4, 5, 6, 11, 54, 55, 58, 59, 60, 62, 63
Haemulon aurolineatum Cuvier, 1830 2 0.029 3, 47
Haemulon plumierii (Lacepède, 1801) 3 0.044 54, 62, 63
Haemulon sciurus (Shaw, 1803) 1 0.015 3
Haemulon steindachneri (Jordan & Gilbert, 1882) 3 0.044 1, 3, 47
Orthopristis ruber (Cuvier, 1830) 10 0.147 1, 2, 3, 4, 5, 6, 54, 55, 58, 59
Pomadasys crocro (Cuvier, 1830) 1 0.015 63
Hemiramphidae Hyporhamphus unifasciatus (Ranzani, 1841) 2 0.029 1, 3
Holocentridae Holocentrus adscensionis (Osbeck, 1765) 2 0.029 60, 62
Istiophoridae Istiophorus albicans (Latreille, 1804) 1 0.015 47
Kyphosidae Kyphosus sectatrix (Linnaeus, 1758) 3 0.044 9, 49, 60
Labridae Bodianus rufus (Linnaeus, 1758) 4 0.059 3, 8, 42, 47
Lobotidae Lobotes surinamensis (Bloch, 1790) 10 0.147 7, 39, 54, 55, 56, 58, 62, 63, 64, 66
Lutjanidae Lutjanus analis (Cuvier, 1828) 1 0.015 68
Lutjanus griseus (Linnaeus, 1758) 1 0.015 59
Lutjanus purpureus (Poey, 1866) 1 0.015 59
Lutjanus synagris (Linnaeus, 1758) 5 0.074 1, 3, 4, 5, 6
Ocyurus chrysurus (Bloch, 1791) 1 0.015 47
Malacanthidae Caulolatilus chrysops (Valenciennes, 1833) 1 0.015 53
Megalopidae Megalops atlanticus Valenciennes, 1847 3 0.044 54, 62, 63
Mugilidae Mugil liza Valenciennes, 1836 5 0.074 1, 3, 4, 5, 6
Paralichthyidae Paralichthys orbignyanus (Valenciennes, 1839) 1 0.015 54
Polynemidae Polydactylus oligodon (Günther, 1860) 6 0.088 14, 15, 17, 18, 19, 38
Pomacanthidae Pomacanthus paru (Bloch, 1787) 1 0.015 62
Pomatomidae Pomatomus saltatrix (Linnaeus, 1766) 21 0.309 2, 3, 4, 5, 6, 7, 9, 26, 28, 29, 30, 39, 41, 45, 53, 54, 55, 58, 59, 60, 63
Sciaenidae Bairdiella ronchus (Cuvier, 1830) 13 0.191 1, 2, 3, 4, 5, 6, 32, 49, 54, 55, 57, 58, 59
Cynoscion acoupa (Lacepède, 1801) 16 0.235 10, 11, 14, 15, 17, 18, 19, 20, 27, 35, 38, 54, 59, 62, 63, 64
Cynoscion guatucupa (Cuvier, 1830) 1 0.015 64
Cynoscion jamaicensis (Vaillant & Bocourt, 1883) 12 0.176 1, 2, 3, 4, 5, 6, 8, 32, 34, 49, 55, 58
Cynoscion leiarchus (Cuvier, 1830) 5 0.074 54, 55, 58, 62, 63
Cynoscion similis Randall & Cervigón, 1968 6 0.088 1, 3, 4, 5, 6, 36
Cynoscion striatus (Cuvier, 1829) 3 0.044 28, 29, 35
Cynoscion virescens (Cuvier, 1830) 19 0.279 11, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 38, 48, 58, 59, 62, 63
Isopisthus parvipinnis (Cuvier, 1830) 3 0.044 32, 54, 59
Larimus breviceps Cuvier, 1830 18 0.265 1, 2, 3, 4, 5, 6, 32, 33, 34, 49, 54, 55, 57, 58, 59, 60, 61, 63
Menticirrhus americanus (Linnaeus, 1758) 2 0.029 49, 59
Micropogonias furnieri (Desmarest, 1823) 53 0.779 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 38, 39, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62, 63, 64
Micropogonias undulatus (Linnaeus, 1766) 8 0.118 26, 27, 28, 29, 30, 31, 35, 50
Ophioscion punctatissimus Meek & Hildebrand, 1925 1 0.015 54
Pareques acuminatus (Bloch & Schneider, 1801) 1 0.015 35
Pogonias cromis (Linnaeus, 1766) 48 0.706 2, 3, 4, 5, 6, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37, 38, 42, 48, 49, 52, 53, 54, 55, 57, 58, 59, 60, 62, 63, 64, 68
Nebris microps Cuvier, 1830 1 0.015 59
Stellifer brasiliensis (Schultz, 1945) 1 0.015 54
Stellifer rastrifer (Jordan, 1889) 2 0.029 32, 54
Umbrina canosai Berg, 1895 1 0.015 29
Umbrina coroides Cuvier, 1830 1 0.015 42
Scombridae Katsuwonus pelamis (Linnaeus, 1758) 2 0.029 8, 47
Scomberomorus cf. brasiliensis Collette, Russo & Zavala-Camin, 1978 2 0.029 62, 63
Thunnus cf. atlanticus (Lesson, 1831) 1 0.015 64
Serranidae Cephalopholis fulva (Linnaeus, 1758) 4 0.059 54, 62, 63, 64
Epinephelus itajara (Lichtenstein, 1822) 4 0.059 54, 62, 63, 64
Epinephelus morio (Valenciennes, 1828) 6 0.088 3, 47, 54, 62, 63, 64
Hyporthodus niveatus (Valenciennes, 1828) 2 0.029 26, 29
Mycteroperca acutirostris (Valenciennes, 1828) 2 0.029 63, 64
Sparidae Archosargus probatocephalus (Walbaum, 1792) 20 0.294 2, 3, 4, 5, 6, 7, 9, 39, 53, 54, 55, 56, 57, 58, 59, 60, 62, 63, 64, 66
Archosargus rhomboidalis (Linnaeus, 1758) 8 0.118 3, 5, 26, 28, 29, 30, 31, 35
Calamus pennatula Guichenot, 1868 2 0.029 54, 62
Diplodus argenteus (Valenciennes, 1830) 2 0.029 9, 60
Pagrus pagrus (Linnaeus, 1758) 8 0.118 26, 28, 29, 30, 35, 47, 49, 53
Sphyraenidae Sphyraena barracuda (Edwards, 1771) 1 0.015 5
Sphyraena guachancho Cuvier, 1829 1 0.015 3
Tetraodontidae Lagocephalus laevigatus (Linnaeus, 1766) 24 0.353 2, 3, 4, 5, 6, 7, 8, 9, 26, 28, 35, 39, 42, 49, 54, 55, 56, 58, 59, 60, 61, 62, 63, 67
Sphoeroides spengleri (Bloch, 1785) 5 0.074 2, 3, 4, 5, 6
Sphoeroides testudineus (Linnaeus, 1758) 5 0.074 2, 3, 4, 5, 6
Trichiuridae Trichiurus lepturus Linnaeus, 1758 17 0.250 2, 3, 4, 5, 6, 8, 42, 47, 53, 54, 55, 58, 59, 60, 62, 63, 65
Triglidae Prionotus punctatus (Bloch, 1793) 1 0.015 1

Table 3 Marine fish of class Chondrichthyes from middens in the Southeast Region of Brazil with their absolute (F) and relative (relative F) frequencies of occurrence as well as the midden(s) in which they were recorded. The codes representing the middens are defined in Table 1

Family Species F Relative F Midden(s)
Alopiidae Alopias superciliosus Lowe, 1841 2 0.029 3, 50
Alopias vulpinus (Bonnaterre, 1788) 6 0.088 3, 53, 55, 56, 58, 60
Carcharhinidae Carcharhinus acronotus (Poey, 1860) 8 0.118 1, 3, 5, 42, 54, 62, 63, 64
Carcharhinus altimus (Springer, 1950) 2 0.029 3, 9
Carcharhinus brachyurus (Günther, 1870) 2 0.029 3, 5
Carcharhinus brevipinna (Müller & Henle, 1839) 8 0.118 3, 8, 26, 29, 42, 47, 49, 50
Carcharhinus falciformis (Müller & Henle, 1839) 1 0.015 3
Carcharhinus leucas (Müller & Henle, 1839) 10 0.147 3, 45, 54, 55, 56, 58, 59, 60, 62, 63
Carcharhinus limbatus (Müller & Henle, 1839) 11 0.162 1, 3, 4, 5, 6, 8, 45, 54, 62, 63, 64
Carcharhinus longimanus (Poey, 1861) 2 0.029 3, 45
Carcharhinus obscurus (Lesueur, 1818) 10 0.147 3, 8, 26, 29, 54, 55, 56, 58, 62
Carcharhinus perezii (Poey, 1876) 1 0.015 3
Carcharhinus plumbeus (Nardo, 1827) 10 0.147 1, 3, 5, 6, 26, 45, 47, 55, 56, 58
Carcharhinus porosus (Ranzani, 1839) 5 0.074 1, 3, 4, 5, 6
Negaprion brevirostris (Poey, 1868) 9 0.132 1, 2, 3, 4, 5, 6, 8, 29, 42
Prionace glauca (Linnaeus, 1758) 9 0.132 44, 54, 55, 56, 57, 58, 59, 60, 62
Rhizoprionodon lalandii (Müller & Henle, 1839) 4 0.059 3, 4, 5, 6
Rhizoprionodon porosus (Poey, 1861) 3 0.044 3, 4, 5
Galeocerdo cuvier (Péron & Lesueur, 1822) 23 0.338 1, 2, 3, 4, 5, 6, 7, 8, 30, 42, 44, 45, 46, 47, 54, 55, 56, 58, 59, 60, 62, 63, 64
Dasyatidae Bathytoshia centroura (Mitchill, 1815) 6 0.088 3, 7, 26, 29, 39, 50
Hypanus americanus (Hildebrand & Schroeder, 1928) 2 0.029 54, 63
Hypanus guttatus (Bloch & Schneider, 1801) 1 0.015 3
Ginglymostomatidae Ginglymostoma cirratum (Bonnaterre, 1788) 3 0.044 54, 62, 63
Gymnuridae Gymnura altavela (Linnaeus, 1758) 1 0.015 7
Lamnidae Lamna nasus (Bonnaterre, 1788) 7 0.103 1, 3, 4, 5, 6, 42, 47
Carcharodon carcharias (Linnaeus, 1758) 23 0.338 1, 2, 3, 4, 5, 6, 7, 8, 26, 29, 42, 45, 47, 50, 54, 55, 56, 58, 59, 60, 62, 63, 64
Isurus oxyrinchus Rafinesque, 1810 15 0.221 3, 7, 8, 37, 39, 42, 45, 47, 54, 55, 56, 58, 60, 62, 63
Isurus paucus Guitart, 1966 1 0.015 7
Myliobatidae Aetobatus narinari (Euphrasen, 1790) 24 0.353 3, 8, 9, 26, 28, 29, 30, 31, 35, 39, 42, 47, 49, 50, 54, 55, 56, 58, 59, 60, 61, 62, 63, 64
Myliobatis goodei Garman, 1885 5 0.074 54, 55, 56, 58, 59
Rhinoptera bonasus (Mitchill, 1815) 10 0.147 7, 39, 54, 55, 56, 58, 59, 60, 62, 63
Rhinoptera brasiliensis Müller, 1836 5 0.074 54, 59, 60, 61, 62
Odontaspididae Carcharias taurus Rafinesque, 1810 26 0.382 1, 2, 3, 4, 5, 6, 7, 8, 35, 40, 41, 42, 43, 45, 47, 50, 53, 54, 55, 56, 57, 58, 59, 60, 62, 63
Sphyrnidae Sphyrna lewini (Griffith & Smith, 1834) 2 0.029 3, 60
Sphyrna mokarran (Rüppell, 1837) 2 0.029 3, 29
Sphyrna tiburo (Linnaeus, 1758) 2 0.029 54, 59
Sphyrna zygaena (Linnaeus, 1758) 4 0.059 3, 5, 47, 59

The site with the highest species richness was the midden Sambaqui do Algodão in Angra dos Reis with 71 inventoried species and a relative species richness value of 0.5 (Table 1). Most of the inventoried species (63.38%) may be considered rare because they were recorded in no more than five of the 68 study sites. Conversely, Micropogonias furnieri (Desmarest, 1823) and Pogonias cromis (Linnaeus, 1766) had the highest frequencies of occurrence, being found in 53 (relative frequency = 0.78) and 48 (relative frequency = 0.71) of the sites, respectively.

The biogeographic, ecological and economic data showed that most of the identified fish are widely distributed in the Western Atlantic (59.72%) and inhabit estuarine environments (53.99%), while most species have a demersal habit (35.92%) and exhibit oceanic migratory behaviour (28.87%). Lastly, the surveyed fish are predominantly carnivorous (72.54%) with some commercial value (96.48%; Figure 3).

Figure 3 Biogeographical, ecological and economic data for the inventoried fish. A = Distribution; B = Environment; C = Habit; D = Behaviour; E = Feeding guild; F = Commercial value. 

In comparison to the current fish checklists, the middens contained 17.60% of the species recorded in Rio de Janeiro, 15.57% of the species recorded in São Paulo and 2.13% of the species recorded in Espírito Santo. Overall, 17.57% of the fish recorded in the entire Southeast Region were represented in the middens, but they accounted for 28.07% of the species in the region with some commercial value. Moreover, exclusively historic species were identified including 13 in Rio de Janeiro, 15 in São Paulo, and four in Espírito Santo (Table 4). The results from the χ2 tests indicated that were no significant differences in the number of commercial species in the historic and current inventories for the states (Rio de Janeiro: χ2 = 4.587 x 10-9, degrees of freedom = 3, probability > 0.995; São Paulo: χ2 = 3.549 x 10-12, degrees of freedom = 3, probability > 0.995; Espírito Santo: χ2 = 0.106, degrees of freedom = 3, probability > 0.99) or the entire Southeast Region (χ2 = 6.349 x 10-17, degrees of freedom = 3, probability > 0.995).

Table 4 Number of species from current fish inventories and middens from Rio de Janeiro (RJ), São Paulo (SP), Espírito Santo (ES) and the entire Southeast Region. 

n spp. RJ SP ES Southeast Region
Overall Past 104 90 6 142
Overall Present 591 578 282 808
Commercial Past 101 87 6 137
Commercial Present 412 340 196 488
Past Exclusive 13 15 4 5

Discussion

Middens are artificial accumulations of wildlife and cultural remains that were built by groups of pre-colonial humans during the Holocene (Lima et al. 2003, Mendes et al. 2014). Therefore, the species compositions of the organisms found in middens are presumably non-random and biased samples of natural biological communities at those sites because they were influenced or determined by various cultural factors, including food preference, the technological level of the fishing gear, harvesting and hunting artefacts, food taboos, funerary or ritualistic practices and how the materials were discarded and/or used. Therefore, some researchers believe that the faunal data from middens have selectivity biases that complicate any related inferences about ecosystems and their biodiversity (Baisre 2010, Rodrigues et al. 2016a). However, the comparison between the inventory of the marine fish identified in middens and those from general surveys of ichthyological fauna showed no significant differences in the number of species either with or without commercial value, indicating that middens contain data that are not solely applicable to prehistoric fisheries. Such wildlife remains apparently represent the fauna existing at the time that the archaeological sites were created but are also repositories of broader biodiversity data, despite any bias associated with the composition of zoo-archaeological remains (Lindbladh et al. 2007, Froyd & Willis 2008).

In a recent study using taxonomic tests, Faria et al. (2014) showed that the malacological taxonomic diversity in the Tarioba midden (Rio de Janeiro, Brazil) was not significantly different from that of a comprehensive list of the mollusc species from the entire coast of the state of Rio de Janeiro. Those findings and the results of the present study suggest that middens may contain key indicators of past biodiversity, despite their limitations, and furthermore, some studies of middens have shown detectable changes in species composition over time (Dalzell 1998, Lotze & Milewski 2004, Rosenberg et al. 2005, Maschner et al. 2008, Souza et al. 2016).

Studies focused on inventorying the fish species in middens have usually involved a limited number of sites (sampling areas). For example, Kloker et al. (2010) recorded 17 fish species from two sites on the south coast of Brazil (Santa Catarina state). In contrast, as part of a greater sampling effort, Lopes et al. (2016) recorded 97 fish species in 13 sites located on the coast of Rio de Janeiro, and in this study, the study area corresponded to 68 middens distributed over 1,000 km of the southeast coast of Brazil.

In using even greater effort than that undertaken by Lopes et al. (2016), this study used data which came from different kinds of publications (scientific articles, books, thesis, dissertations, monographs, technical reports etc) encompassing 48 years (1968-2016) of studies in the field. Therefore, the data compiled here came from a myriad of objectives and methodologies, for example, primary data which came from excavations were originated since superficial sampling till total material recovery. Following excavation the material recovered were dry sieved or under current water using different mesh sizes (2 to 10mm). Identification of the zoo-archaeological vestiges was done by handling different manuals and reference collections. Due to that the list recovered was carefully scrutinized. Criteria such as using only the more inclusive taxa and species with biogeographic range defined were used. Furthermore, the Linean definition of the species was fully checked for ambiguities and classification changes. In using these criteria any inconvenience related to the heterogeneity of sources were surpassed and the methodological choice gave an extensive baseline of fishes biodiversity during the Holocene in the Brazilian Coast.

The species richness from the midden fish inventory in this study was lower than that of current fish checklists (Bizerril & Costa 2001, Menezes 2011, speciesLink), which likely resulted from the selected sampling methods. All current checklists were developed from extensive bibliographical surveys that included studies that employed diverse methods (fishing records, scientific collections, the testimony of scientific experts, museum collection documents and environmental monitoring) as well as data accumulated from several years of academic research. In contrast, the midden records were fundamentally related to prehistoric fisheries or related cultural activities (fishing gear, ritualistic symbols, ornaments and artefacts) as well as by-catch. In all cases, the midden fish records were always informed by an understanding of prehistoric culture; that is, the midden fish inventory was constructed with data from archaeological studies of fishing cultures and thus focused on a limited number of target species.

Regarding the target species, the occurrence frequencies of M. furnieri and P. cromis in middens indicate that they were preferentially fished species. Barbosa-Guimarães (2013) observed that M. furnieri was the main fish species in Saquarema middens (Rio de Janeiro, Brazil) and thus inferred that it was the primary food of the midden peoples of that region. In turn, Souza Cunha et al. (1981) notes the presence of Pogonias sp. in the midden Sambaqui de Camboinhas (Niterói, state of Rio de Janeiro, Brazil), and the remains of that genus are commonly found in coastal middens (Kneip et al. 1975). Lopes et al. (2016) recorded M. furnieri and P. cromis as two of the three most common species in their study of Rio de Janeiro middens, and these two species are currently considered key fishery resources in the Southeast Region of Brazil (Mulato et al. 2015, Santos et al. 2016). Furthermore, estuarine, demersal and carnivorous species typically have significant commercial value, thus composing key fishing stocks (Tacon 1994, Santos & Câmara 2002, Haimovici et al. 2014), and it can be deduced that such species were critical fishing resources for midden peoples in the past.

On the one hand, the presence of species such as M. furnieri and P. cromis, which occur at high relative frequencies in middens, indicates that midden fish inventories contain prehistoric fishery data, but the numbers of fish with and without commercial value in middens are not significantly different from those in checklists of ichthyological fauna for the same sites. Moreover, the high number of exclusive species with low frequencies of occurrence in middens corroborates the hypothesis that midden fish records contain key data on Holocene ichthyological fauna and that such species are most likely by-catch. Additionally, the occurrence frequencies show that it is unlikely that midden peoples from neighbouring regions consumed different or unique species. Thus, the results from this study indicate that middens contain data on midden fishing and culture as well as past biodiversity.

Biodiversity inventories are essential for establishing baselines that inform species management and conservation measures (Gordillo et al. 2014), especially those related to endangered species, including fish. Currently, the effects of overfishing, pollution, invasive species and other ecological impacts have reduced marine ichthyological diversity (Povey & Keough 1991, Brosnan & Crumrine 1994, Polunin & Roberts 1996, Costello et al. 2010). Therefore, the study of ichthyological midden remains is a key tool for understanding prehistoric biodiversity, enabling the establishment of a historical perspective and thus more complete baselines to inform more effective management measures and reduce the threat of extinction currently faced by marine fishes.

In summary, the midden inventory of the Holocene marine fish of the southeast coast of Brazil contains data on prehistoric fisheries, which is supported by the high number of species with low frequencies of occurrence (or unique species) as well as by chi-squared tests that failed to show significant differences between the midden fish inventory and current ichthyofauna checklists. Thus, the results from this study clearly indicate that zoo-archaeological fish remains are key evidence of Holocene biodiversity.

Acknowledgments

The authors would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for financial support and Pos-doc Scholarship for MRD (Programa Nacional de Pós-Doutorado-PNPD) and Masters Scholarship for ABM.

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Received: June 15, 2017; Revised: December 16, 2017; Accepted: December 17, 2017

*Corresponding author: Michelle Rezende Duarte, e-mail: michellerezendeduarte@yahoo.com.br

Author Contributions Augusto Barros Mendes: Contribution to data collection, contribution to data analysis and interpretation, contribution to manuscript preparation and contribution to critical revision, adding intelectual content.

Michelle Rezende Duarte: Contribution to data analysis and interpretation, contribution to manuscript preparation and contribution to critical revision, adding intelectual content

Edson Pereira da Silva: Substantial contribution in the concept and design of the study, contribution to data collection, contribution to data analysis and interpretation, contribution to manuscript preparation and contribution to critical revision, adding intelectual content

Conflicts of interest The authors declare that there is no conflict of interest related to the publication of the data in this article.

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