Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

The Path towards Endangered Species: Prehistoric Fisheries in Southeastern Brazil

  • Mariana Samôr Lopes,

    Affiliation Universidade Federal Fluminense, Instituto de Biologia, Campus do Valonguinho, Outeiro São João Batista, s/n°.CEP: 24020–141, Niterói, Rio de Janeiro, Brasil

  • Thayse Cristina Pereira Bertucci ,

    thathab@gmail.com

    Affiliation Universidade Federal Fluminense, Instituto de Biologia, Campus do Valonguinho, Outeiro São João Batista, s/n°.CEP: 24020–141, Niterói, Rio de Janeiro, Brasil

  • Luciano Rapagnã,

    Affiliation Universidade Federal Fluminense, Instituto de Biologia, Campus do Valonguinho, Outeiro São João Batista, s/n°.CEP: 24020–141, Niterói, Rio de Janeiro, Brasil

  • Rafael de Almeida Tubino,

    Affiliation Universidade Federal Fluminense, Instituto de Biologia, Campus do Valonguinho, Outeiro São João Batista, s/n°.CEP: 24020–141, Niterói, Rio de Janeiro, Brasil

  • Cassiano Monteiro-Neto,

    Affiliation Universidade Federal Fluminense, Instituto de Biologia, Campus do Valonguinho, Outeiro São João Batista, s/n°.CEP: 24020–141, Niterói, Rio de Janeiro, Brasil

  • Acácio Ribeiro Gomes Tomas,

    Affiliation Instituto de Pesca, Centro APTA Pescado Marinho, Av. Bartolomeu de Gusmão 192, Santos, São Paulo, CEP: 11030–906, Brasil

  • Maria Cristina Tenório,

    Affiliation Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Antropologia. Quinta da Boa Vista, Rio de Janeiro, CEP: 20940–040, Brasil

  • Tânia Lima,

    Affiliation Universidade Federal do Rio de Janeiro, Museu Nacional, Departamento de Antropologia. Quinta da Boa Vista, Rio de Janeiro, CEP: 20940–040, Brasil

  • Rosa Souza,

    Affiliation Universidade Federal Fluminense, Instituto de Biologia, Campus do Valonguinho, Outeiro São João Batista, s/n°.CEP: 24020–141, Niterói, Rio de Janeiro, Brasil

  • Jorge Domingo Carrillo-Briceño,

    Affiliation Palaeontological Institute and Museum, University of Zürich, Karl-Schmid-Strasse 4, Zürich 8006, Switzerland

  • Manuel Haimovici,

    Affiliation Universidade Federal do Rio Grande, Instituto de Oceanografia, Campus Carreiros, Av. Itália, Rio Grande, Rio Grande do Sul, CEP: 96201–900, Brasil

  • Kita Macario,

    Affiliation Universidade Federal Fluminense, Instituto de Física, Campus da Praia Vermelha, Boa Viagem, CEP: 24210–310, Niterói, Rio de Janeiro, Brasil

  • Carla Carvalho,

    Affiliation Universidade Federal Fluminense, Instituto de Física, Campus da Praia Vermelha, Boa Viagem, CEP: 24210–310, Niterói, Rio de Janeiro, Brasil

  • Orangel Aguilera Socorro

    Affiliation Universidade Federal Fluminense, Instituto de Biologia, Campus do Valonguinho, Outeiro São João Batista, s/n°.CEP: 24020–141, Niterói, Rio de Janeiro, Brasil

The Path towards Endangered Species: Prehistoric Fisheries in Southeastern Brazil

  • Mariana Samôr Lopes, 
  • Thayse Cristina Pereira Bertucci, 
  • Luciano Rapagnã, 
  • Rafael de Almeida Tubino, 
  • Cassiano Monteiro-Neto, 
  • Acácio Ribeiro Gomes Tomas, 
  • Maria Cristina Tenório, 
  • Tânia Lima, 
  • Rosa Souza, 
  • Jorge Domingo Carrillo-Briceño
PLOS
x

Abstract

Brazilian shellmounds are archaeological sites with a high concentration of marine faunal remains. There are more than 2000 sites along the coast of Brazil that range in age from 8,720 to 985 cal BP. Here, we studied the ichthyoarchaeological remains (i.e., cranial/postcranial bones, otoliths, and teeth, among others) at 13 shellmounds on the southern coast of the state of Rio de Janeiro, which are located in coastal landscapes, including a sandy plain with coastal lagoons, rocky islands, islets and rocky bays. We identified patterns of similarity between shellmounds based on fish diversity, the ages of the assemblages, littoral geomorphology and prehistoric fisheries. Our new radiocarbon dating, based on otolith samples, was used for fishery characterization over time. A taxonomical study of the ichthyoarchaeological remains includes a diversity of 97 marine species, representing 37% of all modern species (i.e., 265 spp.) that have been documented along the coast of Rio de Janeiro state. This high fish diversity recovered from the shellmounds is clear evidence of well-developed prehistoric fishery activity that targeted sharks, rays and finfishes in a productive area influenced by coastal marine upwelling. The presence of adult and neonate shark, especially oceanic species, is here interpreted as evidence of prehistoric fisheries capacity for exploitation and possibly overexploitation in nursery areas. Various tools and strategies were used to capture finfish in seasonal fisheries, over rocky reef bottoms and in sandy littoral environments. Massive catches of whitemouth croaker, main target dermersal species of South Atlantic coast, show evidence of a reduction in body size of approximately 28% compared with modern fisheries. Fishery activity involving vulnerable species, especially in nursery areas, could mark the beginning of fish depletion along the southeastern Brazilian coast and the collapse of natural fish populations.

Introduction

When investigating early archaeological settlements in Brazil, South America [1], the existence of an undisturbed marine fauna predating European colonization is expected. The archaeological evidence of prehistoric fisheries shows high abundance and diversity of marine faunal remains recovered from Brazilian shellmounds [2,3,4,5,6,7,8,9,10,11,12]. However, the main goal of these studies is to elucidate the archaeological context of fisher-gatherer settlements. The ichthyoarchaeological remains testify to well-developed fisheries for sharks, rays and finfishes, as well as to shellfish gathering and hunting of marine reptiles and mammals. Prehistoric subsistence fisheries could have been the cause of early differential disturbances in local fish fauna resources due to the assumed use of beach seines, gillnets, hook and line, traps and spearfishing.

A key study on prehistoric fisheries in the Caribbean [13] strongly supports the claim that overexploitation did not occur. However, the debate about fish depletion, overexploitation, extinction and environmental degradation in prehistoric and colonial times continues [14,15]. Prehistoric overfishing could be associated with local environmental degradation as a consequence of human uses of the landscape affecting the marine environment, community dynamics and spatially subsidized food webs [16,17,18,19], and overexploitation based exclusively on prehistoric fisheries might not have been the exclusive cause [15,20,21]. This hypothesis was widely discussed using evidence from comparative analyses of Pacific islands and channel ecosystems under archaeological investigation [22,23]. However, tropical Western Atlantic prehistoric fisheries differ in terms of Holocene paleoenvironments, fish assemblages and large-scale vulnerability at the time of prehistoric fisheries along the South American coast ([1]; S1 Appendix).

Prehistoric fishery exploitation patterns along the Atlantic coast of South America, from Brazil to Argentina are not well described. Brazilian shellmounds ranges from 8,720 to 985 years calibrated before present (cal BP) [1,24,25,26,27,28,29,30,31]. Previous ichthyological records from these archaeological sites were documented only by faunal lists without illustrative diagnostic species characters or museum catalog numbers to corroborate the species identifications. The present contribution is an attempt to improve our understanding of Rio de Janeiro’s shellmounds by providing new, detailed and accurate taxonomic lists and analyses of the relevant fish assemblages.

Contiguous with south Brazil and Uruguay, Argentinean ichthyoarchaeological sites, situated on the coast of San Matías Gulf in Patagonia (6,800 to 890 yr BP), show evidence of local prehistoric fisheries. The abundance of otoliths indicates that the predominant bony fish target was the whitemouth croaker, Micropogonias furnieri [32,33,34,35], a coastal finfish species also present in Brazilian coastal shellmounds.

Fishery tools, such as projectile points, manufactured mainly with bones are frequently recovered from the Brazilian shellmounds [30]. Moreover, evidence that allows us to infer the use of wood and vegetable fiber for the construction of fish traps, beach seines and or gillnets used for massive captures of large fish schools is not preserved. Indirect evidence of boat constructions based on lithic tools and records in detailed rock paintings reveal fluvial skillful navigators in Northeastern of Brazil [36]. In addition, the frequency of skeletal anomalies found in human remains recovered from the shellmounds, including auditory meatus exostoses, osteoarthritis, osteoarthrosis and other degenerative effects [37,38], is usually considered to be a marker of sailing and aquatic labor in cold waters [39,40,41], suggesting the engagement of those human populations in traditional fishery activity for subsistence. Stable isotope analyses of δ14C and δ15N in human skeletons from the shellmounds of Southern Brazil indicate a diet strongly dependent on marine resources [42]. Therefore, in agreement with previous research [43], the abundance and diversity of fish remains from the shellmounds provides unequivocal proof of fisheries that were able to operate in open waters over sandy and rocky bottoms.

Shellmounds are not necessarily horizontally stratified due to sequential periods of occupation, and the areas selected for specific activities may vary from the center to the periphery of the shellmound [44,45]. These sandy shellmounds are usually dome-shaped, and the archaeological variation in vertical section is based on changes in sediment texture and color, settlement size, abundance and diversity of mollusks, intercalation of sterile sandy layers (i.e., without ichthyoarchaeological remains) and evidence of cultural activities (e.g., burials and stoves). However, in contrast with archaeological evidence from settlements, in some shellmounds, the layers could not be distinguished [46].

The Rio de Janeiro shellmounds [1] are located in a coastal landscape characterized by sandy plains with coastal lagoons, rocky islands, islets and rocky bays [47]. These coastal areas are strongly influenced by seasonal upwellings, occurring during the austral summer [48,49,50,51], which increase marine productivity and the potential resources for fisheries.

Therefore, the main goal of this study is to highlight the fish diversity and faunal assemblage of ancient fisheries based on the skeletal remains deposited in the shellmounds along the southeastern Brazilian coast. Additionally, we correlate shark diversity and abundance in the shellmounds with the abilities of specific fisheries to exploit resources, which could lead to overexploitation. The groundfish catches were the result of multi-gear strategies in seasonal fisheries. Radiometric age, geochemical analyses and climate reconstruction of these ichthyoarchaeological remains [52,53,54,55] were used to supporting our findings.

Historical accounts of ancient fisheries

Ichthyoarchaeological evidence and historical accounts from the Caribbean and tropical South America suggest that early prehistoric target species corresponded to the most accessible and vulnerable animals, such as sharks, large groupers [56,57,58], turtles [59,60] and sea mammals [61,62,63,64].

Colonial accounts from 1587 [56] on the semi-sedentary indigenous community that lived in Brazil during the early days of Portuguese colonization refer to the paleo-Indian fisheries’ expertise and their use of rich marine food supplies; the accounts additionally demonstrate a traditional knowledge of fish diversity, reproductive aggregation of fish, fishery areas and environmental relationships. Regarding fish diversity, a list of the 43 most important species of fish was reported accurately (Table 1) [56]. These fish records are in agreement with the prehistoric data presented here. Most of the historic narrative regarding fish captures concerns reproductive periods in coastal and estuarine areas, where bony fishes form compact aggregations along the littoral zone during the intertidal phase. The account ‘curiosi rerum naturae’ [56] refers to high marine fish abundance, especially during the summer on the coast of Salvador in the state of Bahia (northeast Brazil), when female bony fishes have large gonads. Additionally, the narrative talks about the ‘docile and very easily caught giant grouper on the beaches’, the large tarpon size, ‘longer than an Indian is tall’, and the ‘thousands of mullet caught during a single day fishing’, revealing a picture of the abundance of fishery resources [56,65]. All these historical narratives are in agreement with the fact that Brazilian neo-Indians were skilled fishermen, using arrows, marksmanship, and fishery lines with hooks; they built fish traps with wood and rocks in an intertidal beach and small nets for cooperative fisheries. These undeniable skills were possibly inherited from ancestral paleo-Indians who perfected the art of fishing [66].

Shellmounds are the best testimonial resource for understanding the paleo-Indian fishery activities. However, most of the original context of Brazilian shellmounds was destroyed due to the use of mollusk shells to produce lime and fertilizers for paving of roads and streets, construction of forts, colonial houses, churches, among others applications. This occurred starting in 1549 in the area of Salvador, Bahia and other colonial settlements along the Brazilian coast and continued until the 1960s, when archaeological shellmounds became protected under Brazilian federal law.

Geographic setting

From south to north, the landscape of the Rio de Janeiro coast is characterized by the presence of a crystalline shield (Serra do Mar relief), with plenty of high (approximately 1,200 m) mountain scarps parallel to the Atlantic Ocean in the vicinity of Angra dos Reis [67]. The area is characterized by short rivers flowing to the coast and fluviomarine plains in an embayment (i.e., Ribeira Bay), a jagged coastline, with small peninsulas and several rocky islets [68]. The beaches and the sandy stretches are not developed, and the shellmounds are predominantly located over the rocky islets in an area dominated by mangrove flood plains. Small submarine channels approximately 6 to 10 m deep characterize the coastal bathymetry, and near Ilha Grande bay, the depth reaches approximately 30 m. Ilha Grande is a massive structural island with fairly rugged relief; it is isolated from the mainland by a channel approximately two kilometers wide.

The Itaipú-Camboinhas region is located on the oceanfront of Niterói and has sandy beaches dominated by dunes and sandy bars, which separate the sea from Piratininga and Itaipu coastal lagoons. The semicircular sandy beach has depths of approximately 3 to 16 m that extend almost 1,000 m offshore. The landscape has a mountainous relief aligned in the SW-NE direction [47]. The Camboinhas shellmound is located over a sand dune, near the coastal line and the tidal channel of Itaipu Lagoon.

The Saquarema region is located in a landscape characterized by a crystalline rock relief, which separates the two major drainage basins that feed the Saquarema lagoon complex [47,68]. The sandy shore is shallow but exposed to high-energy coastal wind and waves. The area has the highest concentration of shellmounds in Rio de Janeiro; they are distributed along the sandy coastal plain of the inland sandbanks, facing the lagoon (e.g., Beirada, Manitiba, Ponte do Girau and Saquarema shellmounds).

In Arraial do Cabo, the structural NE-SW trend is characterized by a metamorphic basement (i.e., Pontal de Atalaia), rising up to 172 m high, and the adjacent Cabo Frio Island, an igneous alkaline rock (syenite, trachyte and breccia) with altitudes of approximately 380 m [69]. The Usiminas shellmound is located in the Cabo Frio Island, 50 m above sea level, facing the coastal plain, where the water depth is approximately 5 m. In contrast, the oceanfront cliffs on the opposite coast reach 50 m in depth near the coastline. Additionally, the Ilha do Cabo Frio shellmound is located on a small sandy beach characterized by an active dune that faces towards the landscape, associated with the outcrop layers that overlap the Cabo Frio beach rock [65,70]. Part of the lower layer of this shellmound is located below sea level [29].

Materials and Methods

Selected shellmounds from the southeastern coast of Rio de Janeiro State, Brazil have three main features: (1), the potential marine influence of the Cabo Frio upwelling system (i.e., seasonal oceanographic mixing of South Atlantic Central Water, Subtropical Shell Water and the Brazilian Current, increasing biological productivity); (2), the marine environment (i.e., shallow waters, coastal lagoons and a rocky bottom); and (3), coastal geomorphology (i.e., sandy coastal plains, rocky islands and rocky bays).

The shellmounds included in this study are the following: the Usiminas shellmound [71], on a rocky settlement, and the Ilha do Cabo Frio shellmound [72], on a sandy beach on Cabo Frio Island (23°00' 18" S, 42°00' 20" W); Saquarema [72], Beirada [46], Manitiba [73] and Ponte do Girau [74] shellmounds, on a sandy coastal plain with coastal lagoons in the Saquarema lagoon complex (22°55' 66" S, 42°29' 00" W); Camboinhas shellmound [75], on a sandy coastal plain with coastal lagoons in the oceanic region of Niterói (22°57' 54" S, 44°02' 53" W); Algodão, Major, Bigode, Caieira and Peri shellmounds [76], on rocky islets and coastal rocky bays in the Ribeira Bay, Angra dos Reis (22°55' 48" S, 44°20' 48" W); and Acaiá shellmound (personal communication of an unpublished manuscript: Tenório, M.C. ‘Os sambaquieiros e a gruta do Acaiá: Reconstituição do processo de formação de um sítio’), on a rocky island in the oceanfront of Ilha Grande (Fig 1).

thumbnail
Fig 1. Study area along the southeastern Brazilian coast showing shellmound locations.

https://doi.org/10.1371/journal.pone.0154476.g001

We studied all the specimens deposited in the ichthyoarchaeological collection of Museu Nacional, Universidade Federal do Rio de Janeiro (MN-UFRJ), Rio de Janeiro, Brazil, and their use for this research was authorized by the collection managers, who are coauthors of this study (MCT and TL).

We have organized a referential species collection based on 679 diagnostic osteological and dental characters (details in S2 Appendix). Quantitative analyses of fish specimens and species recovered from each shellmound are necessary for accurate data interpretation. However, different archaeological methods were used in these shellmounds during excavation conducted by UFRJ archaeologists between 1981 and 2005. The methods included sieving techniques, removing material and curatorial processing. These and others questions regarding the repository, catalog and samples labels will require more detailed assessment, which is beyond of the scope of this study. Consequently, the fish diversity analyzed here is based on a qualitative study and the frequencies of species by shellmound.

All relevant specific characteristics of examined species were identified based on comparative anatomy, using 39 shark and ray specimens (among teeth, vertebrae and spines) housed at the Universidade Estadual do Rio de Janeiro (UERJ) and using at least 115 otoliths and 21 dry finfish individual skeletons housed at the Universidade Federal Fluminense (UFF) (details in S3 Appendix). All structures are in a good state of conservation and relevant specific osteological characteristics were also identified based on extensive bibliographic review.

Photographs of the otoliths were taken with a Leica M205A multifocal stereomicroscope. Photographs of bones, sharks and rays teeth were taken using a digital microscope and digital camera. A complete atlas of the most common diagnostic teeth, otoliths and bones recovered and observed from shellmound collections is included in the plates of the present paper.

Cluster analysis was performed under the Paleontological Statistics Software (PAST, version 2.17c) on Q-mode (i.e., grouping variables) to analyze shellmound similarity patterns. This exploratory technique identifies the relationships and patterns among multiple variables across samples and has been applied in a wide range of scientific fields, such as marine and fisheries ecology [77,78,79,80]. The analysis was based on the presence and absence of fish assemblages in the shellmounds, archaeological site ages, littoral geomorphology and prehistoric fisheries. The unweighted pair-group average (UPGMA) algorithm was used with the Bray-Curtis similarity-association matrix of [81].

Estimates of shark-body total length (TL) were based on 660 isolated vertebrae, using a unique linear regression equation for each species: Carcharias taurus TL = 36.786 +10.753 CR [82], Sphyrna lewini TL = 4.51 + 23.64 CR [83], Carcharhinus brevipinna CD = 0.0159 PCL– 0.1285, PCL = 0.799 TL– 9.07 [84] and Carcharodon carcharias FL = 21+ 11.8 CR, FL = 0.94 TL– 5.74 [85], where TL is the total length, FL is the fork length, PCL the precaudal length, CD the vertebral centrum diameter and CR the vertebral centrum radius.

The main teleostean fish target, based on the frequency observed in the shellmounds, was the whitemouth croaker, Micropogonias furnieri [86], which was present in all shellmounds with the exception of the Usiminas and Ilha do Cabo Frio shellmounds, both on Cabo Frio Island. The life history of M. furnieri in the Western Atlantic Ocean is well known [87,88], and they can be found in commercial [89,90] and local artisanal fisheries [77,91]. We used this species to interpret and compare changes between past and present coastal fisheries on the southeastern Brazilian coast. We tested for differences between the medians of length frequency distributions (Student’s t-test, PAST software v. 3.7) after checking for normality and homogeneity of variances.

A total of 5,532 archaeological whitemouth croaker, Micropogonias furnieri, otoliths were measured using digital callipers. These specimens were distributed among the shellmounds as follows: Ponte do Girau (376 specimens), Beirada (2,541 specimens), Manitiba (1,372 specimens), Algodão (1,148 specimens) and Camboinhas (95 specimens). Fish total lengths (TL) were calculated based on the archaeological otolith total length (OL) using the following equation, which we derived from a regression analysis: TL = 24.34 + 22.57 OL (r = 0.988, n = 93). To compare the estimates of body size length data between shellmound samples, we performed a nonparametric variance analysis of medians (Kruskal-Wallis test) and an a posteriori test of the shellmound context, analyzing the localities and related environmental factors using the free software R [92].

We chose not to use the South American Western Atlantic fish records [88]; instead, specific references of modern fish diversity and abundance in the littoral areas close to the shellmounds of Rio de Janeiro were obtained from Arraial do Cabo [58,93,94], Itaipu [77,95] and Ribeira Bay in Angra dos Reis [96], and these were used in comparisons with fishery records.

Data from the Brazilian fishery survey of whitemouth croaker in the Itaipu modern fisheries (i.e., artisanal and semi-industrial) are based on records compiled between 2000 and 2004 [77] from the Angra dos Reis Bay from semi-industrial fisheries captures reported between 2013 and 2014. At Guanabara Bay, a fishery study was conducted using a bottom trawl between 2005 and 2007 [91].

The samples for radiochronology were prepared and analyzed at the Radiocarbon Laboratory of the Universidade Federal Fluminense (LAC-UFF). The otolith samples were chemically treated with HCl and converted to CO2 by hydrolysis with H3PO4. Graphitized samples were placed in the 40-sample wheel of the SNICS ion source and measured in an NEC 250 kV Single Stage Accelerator System (SSAMS) [97]. Typical currents were 50 μA12C-1 (measured at the low energy Faraday cup). Graphite standard and calcite blanks yielded average 14C/13C ratios of 6 x10-13 and 7x10-13, respectively. The average machine background was approximately 50 kHz for the unprocessed graphite, while the average precision ranged from 0.3 to 0.5%. Data analyses were carried out on LACAMS software developed at the Physics Institute of Universidade Federal Fluminense [98]. Calibration of otolith radiocarbon dates was performed with OxCal software v 4.2.3 from the Oxford University [99], using the Marine13 curve [100] in the 2-sigma range with an offset for local marine reservoir corrections (ΔR 14C years) according to the following shellmound localities: Saquarema [53], Manitiba [55] and Southeastern Brazil [101]. Cross-comparisons were conducted in the Beta Analytic Inc. laboratory, following standard protocols.

We exclusively used the fish otolith radiocarbon dates to determine ages for chronological interpretation of the fish assemblages of most shellmounds, except for those from the Cabo Frio Island, where otoliths of whitemouth croaker could not be recovered; additionally, a few otoliths from Ilha Grande could not be dated. Consequently, we refer only to ages that were not derived from otolith samples for the Usiminas, Ilha do Cabo Frio and Acaiá shellmounds. The age ranges of those sites are based on charcoal and shell data ([29,102]; personal communication).

Results

Shellmound radiocarbon dating based on otoliths and the identified fish assemblages are shown in Table 2. Manitiba serves as an example of a multilayer shellmound (i.e., seven archaeostratigraphic layers in 2.2 m of depth) and demonstrates the difficulty in distinguishing radiocarbon age differences between successive layers; here, the calibration curve associated with the error bar and the reservoir effect cause the age range to overlap (Fig 2). This inhibits inferring a chronological sequence for fisheries in shallow shellmounds. We, therefore, use individual shellmound dating as a marker of settlement period.

thumbnail
Table 2. Ichthyoarchaeological records from the Rio de Janeiro shellmounds (Saquarema, Cabo Frio, Niterói, Ilha Grande and Angra dos Reis).

https://doi.org/10.1371/journal.pone.0154476.t002

thumbnail
Fig 2. Modeled age based on whitemouth croaker otolith samples from multiple archaeological layers of Manitiba in Saquarema using OxCal v 4.2.3 [99].

This figure shows ages obtained by radiochronology (vertical lines). The error bar, represented by the horizontal line, shows a range of ages that spans approximately 370 years across the seven archaeostratigraphic sections, hindering a precise dating of the layers.

https://doi.org/10.1371/journal.pone.0154476.g002

A total of 97 fish species have been identified from the Rio de Janeiro shellmounds, representing 37% of the total (265 spp.) modern species recorded from the Rio de Janeiro coast [e.g., Arraial do Cabo (135 spp.), Itaipu (165 spp.) and Angra dos Reis (139 spp.)]. Table 2 shows the occurrence in archaeological sites of the great white shark, Carcharodon carcharias, the sand tiger shark, Carcharias taurus, the porbeagle shark, Lamna nasus, the lemon shark, Negaprion brevirostris, the tiger shark, Galeocerdo cuvier, and a large diversity of other sharks (such as Carcharhinidae, Sphyrnidae, and other coastal species) in the rocky islet shellmounds of Angra dos Reis (Ribeira Bay: Algodão, Bigode, Caieira, Major and Peri sites), Ilha Grande (Acaiá) and Cabo Frio Island (Usiminas and Ilha do Cabo Frio). The data also include the occurrence of other rarer shark species found in the shellmounds located over sandy coasts and coastal lagoons. These remains (i.e., shark teeth and vertebrae) have been recovered in 100% of the analyzed shellmound samples, especially from those associated with rocky islands and islets. The remains of the spotted eagle ray, Aetobatus narinari, were the most frequent from the ray group (batoids). The frequency of bony fish remains suggest that some species of groundfish, inhabitants of sandy and muddy bottom or rocky spots, such as croakers (Sciaenidae), snappers (Lutjanidae), grunts (Haemulidae), groupers (Serranidae) and snooks (Centropomidae), were common target species. Sea catfish (Ariidae) and mullet (Mugilidae) species were frequent in localities with sandy and muddy bottoms associated with coastal lagoons. Rocky reef fishes, which are mostly durophagous (i.e., feeding on mollusks, echinoids and crabs), are represented by species of parrotfish (Scaridae), pufferfish (Tetraodontidae) and porcupinefish (Diodontidae), and their remains were particularly frequent in localities associated with rocky islands. Pelagic fish, including bluefish (Pomatomidae), sailfish (Istiophoridae), dolphinfish (Coryphaenidae), jacks (Carangidae), mackerel and tuna (Scombridae), were frequent in the shellmounds located in coastal and rocky islands oceanfront areas.

Based on the analyzed fish assemblages from shellmounds in Rio de Janeiro State, the nearshore fishery remains analyzed here were deposited 5,595 cal BP in the lagoon region of Saquarema and in the oceanfront region of Niterói (Fig 3, black circles). They were characterized by catches of coastal species associated with sandy bottoms and coastal lagoons. The fish could be accessible using beach seines during reproductive aggregation and spawning. These schools of fish include croaker, drum, catfish, mullet and snook. Later, approximately 4,414 cal BP, fishery activity records suggest a targeting of pelagic resources in protected rocky bays and around coastal rocky islets (Fig 3, black triangle). Rocky reef fishes were also a common target, and advances in artisanal fishery and multi-gear techniques remained successful until colonial times. At least since 3,290 cal BP, the fish assemblage recovery from the shellmounds located on the oceanic islands of Cabo Frio and Ilha Grande (Fig 3, black square) suggests a clear predominance of pelagic fisheries and a secondary use of rocky reef species.

thumbnail
Fig 3. Cluster analysis of shellmound similarities.

Age ranges (green letters) based on otolith data. Calibration was performed using Marine13 [100] in the 2-sigma range. The overall ΔR was found to be -56.5 to 120.5 [101]. The results at specific sites are as follows: ΔR Saquarema: -272 to -8 [53] and ΔR Manitiba: -224 to 60 [55]. Question marks indicate that radiocarbon dating of otoliths was not available; consequently, we plot shellmound age ranges (red numbers) based on charcoal and shell analyses ([29,102]; personal communication).

https://doi.org/10.1371/journal.pone.0154476.g003

The estimation of shark body size (TL) (Table 3) indicates that the spinner shark, Carcharhinus brevipinna, ranged from 44.3 to 263.1 cm; the sand tiger shark, Carcharias taurus, ranged from 79.3 to 192.2 cm; unidentified shark species of the genus Carcharhinus ranged from 38.8 to 115.1 cm; the hammerhead shark, Sphyrna sp., ranged from 10.1 to 40.0 cm; and the great white shark, Carcharodon carcharias, ranged from 88.2 to 249.6 cm.

thumbnail
Table 3. Summary of shark species and body size data recorded from the Rio de Janeiro shellmounds.

https://doi.org/10.1371/journal.pone.0154476.t003

Estimation of the body size distribution of whitemouth croaker, Micropogonias furnieri [range: 17.8 to 84.8 cm TL in all shellmounds (mean length ± SD: 43.3 ± 9.9 cm)]. These ichthyoarchaeological data overlap the modern size distributions from modern fisheries in Itaipu and Angra dos Reis in Rio de Janeiro State (Fig 4). However, the body size distribution of whitemouth croaker catches from prehistoric fisheries shows a probabilistic tendency toward higher frequencies of large specimens, resulting in an estimated 28% reduction in body size based on modern catches.

thumbnail
Fig 4. Frequency of body size classes of whitemouth croaker, M. furnieri.

Ichthyoarchaeological (dashed line, N = 5,532) and modern fisheries (solid line, N = 3,914).

https://doi.org/10.1371/journal.pone.0154476.g004

The results of ANOVA analyses (Kruskal-Wallis) on the median body sizes of whitemouth croaker show that, among the localities (Chi-squared = 1,042.3; df = 4, p values < 0.05), Beirada and Ponte do Girau shellmounds have significant similarities, and both are significantly different from other localities based on an a posteriori test (p values < 0.05). The comparative values of median body sizes from various environments and coastal geomorphologies (Chi-squared = 965.4, df = 2, p values < 0.05) reveal significant differences based on a posteriori tests (p values < 0.05) (Fig 5).

thumbnail
Fig 5. ANOVA analyses (Kruskal-Wallis) of medians based on estimates of body size classes of ichthyoarchaeological otoliths of Micropogonias furnieri, using R software (R Core Team 2012).

(1) A posteriori test of body size medians versus shellmound localities. (2) A posteriori test of body size medians versus paleoenvironments where the shellmounds are located.

https://doi.org/10.1371/journal.pone.0154476.g005

The overlap of age ranges between the sequence of archaeological layers (Fig 2) dismisses the multilayer interpretation of the body size distribution in a given shellmound, and we use the Manitiba shellmound as the best example of this. However, the median body sizes of whitemouth croakers in different layers of the Manitiba shellmound show different values and an apparent tendency toward cyclicity of medians from the archaeological surface layer toward deeper layers. This could be interpreted as the result of seasonal oscillations in the intensity of the seasonal marine coastal upwelling (Fig 6).

thumbnail
Fig 6. Comparative analyses of body size medians of whitemouth croaker from the multiple archaeological layers in the Manitiba shellmound in the Saquarema region.

Note the differences among the layers, from the surface to deeper layers, and the trend of apparent cyclicity. The red line indicates the median of the total data set.

https://doi.org/10.1371/journal.pone.0154476.g006

Individual drilled shark teeth included Carcharodon carcharias, Carcharhinus altimus, C. leucas, C. plumbeus, Galeocerdo cuvier and Sphyrna mokarran (Fig 7). The biodiversity of fish fauna records was illustrated based on individual diagnostic structures (i.e., otoliths, teeth or bones remains) from the recovered specimens (Figs 815).

thumbnail
Fig 7. Drilled shark teeth.

(1a-b) Carcharodon carcharias, lower tooth, Major, MNUFRJ-ZA-146. (2a-b) Carcharhinus altimus, upper tooth, Acaiá, MNUFRJ-ZA-868. (3a-b) Carcharhinus leucas, upper tooth, Ilha do Cabo Frio, MNUFRJ-ZA-869. (4a-b) Carcharhinus plumbeus, upper tooth, Caieira, MNUFRJ-ZA-97. (5a-b) Galeocerdo cuvier, indet. position tooth, Acaiá, MNUFRJ-ZA-870. (6a-b) Sphyrna mokarran, upper tooth, Algodão, MNUFRJ-ZA-54. Scale bar 1 cm.

https://doi.org/10.1371/journal.pone.0154476.g007

thumbnail
Fig 8. Shark teeth from Rio de Janeiro shellmounds.

(1a-b) Carcharias taurus, upper tooth, Usiminas, MNUFRJ-ZA-565. (2a-b) Alopias superciliosus, upper tooth, Saquarema, MNUFRJ-ZA-Col.L.Kneip 28151. (3a-b) Carcharodon carcharias, upper tooth, Algodão, MNUFRJ-ZA-02. (4a-b) Isurus oxyrinchus, upper tooth, Algodão, MNUFRJ-ZA-21. (5a-b) Lamna nasus, lower tooth, Algodão, MNUFRJ-ZA-16. (6a-b) Carcharhinus acronotus, upper tooth, Algodão, MNUFRJ-ZA-01. (7a-b) Sphyrna mokarran, lower tooth, Major, MNUFRJ-ZA-149. (8a-b) Carcharhinus limbatus, upper tooth, Algodão, MNUFRJ-ZA-05. (9a-b) Carcharhinus plumbeus, upper tooth, Algodão, MNUFRJ-ZA-44. (10a-b) Galeocerdo cuvier, tooth, Algodão, MNUFRJ-ZA-17. (11a-b) Negaprion brevirostris, upper tooth, Algodão, MNUFRJ-ZA-25. (12a-b) Rhizoprionodon lalandii, lower tooth, Bigode, MNUFRJ-ZA-87, and (13a-b) upper tooth, Algodão, MNUFRJ-ZA-70. (14a-b) Rhizoprionodon porosus, upper tooth, Bigode, MNUFRJ-ZA-88. (15a-b) Sphyrna mokarran, upper tooth, Caieira II, MNUFRJ-ZA-99. (16a-b) Sphyrna zygaena, lower tooth, Major, MNUFRJ-ZA-161. Scale bar: 1 cm. Views: labial (1b, 2a-5a, 6b, 7a, 8-10b, 11-13a, 14-15b, and 16a), lingual (1a, 2-5b, 6a, 7b, 8-10a, 11-13b, 14-15a, and 16b).

https://doi.org/10.1371/journal.pone.0154476.g008

thumbnail
Fig 9. Ray teeth, vertebrae and dermal denticle from Rio de Janeiro shellmounds.

(1a-b) Pristis sp., vertebrae, Usiminas, MNUFRJ-ZA-597 and, (2a-b) Algodão, MNUFRJ-ZA-624. (3a-c) Rhinoptera sp., tooth, Algodão, MNUFRJ-ZA-498, and (4a-c) Acaiá, MNUFRJ-ZA-708. (5a-b) Ray indet., vertebrae, Saquarema, MNUFRJ-ZA-Col.L.Kneip-08125. (6a-b) Dasyatis centroura, caudal spine, Saquarema, MNUFRJ-ZA-Col.L.Kneip-087-1. (7a-b) Aetobatus narinari, lower plate fragment, Usiminas, MNUFRJ-ZA-424. (8–10) Dasyatidae indet., dermal denticle, Usiminas, MNUFRJ-ZA-407. Scale bar: 1 cm.

https://doi.org/10.1371/journal.pone.0154476.g009

thumbnail
Fig 10. Shark and ray vertebrae from Rio de Janeiro shellmounds.

(1a-c) Carcharias taurus, vertebrae, Usiminas, MNUFRJ-ZA-570. (2a-c) Carcharodon carcharias, vertebrae, Algodão, MNUFRJ-ZA-625, and (3a-b) Beirada, MNUFRJ-ZA-576. (4a-c) Carcharias taurus, vertebrae, Algodão, MNUFRJ-ZA-621. (5a-c) Carcharhinus brevipinna, anterior vertebrae, Usiminas, MNUFRJ-ZA-567, (6a-c) anterior vertebrae, Beirada, MNUFRJ-ZA-575, and (7a-c) posterior vertebrae, Usiminas, MNUFRJ-ZA-568. (8a-c) Carcharhinus sp., vertebrae, Usiminas, MNUFRJ-ZA-569. (9a-c) Rhizoprionodon sp., vertebrae, Usiminas, MNUFRJ-ZA-571. (10a-c) Carcharhinus sp., vertebrae, Algodão, MNUFRJ-ZA-620, (11a-c) Acaiá, MNUFRJ-ZA-715, and (12a-c) Algodão, MNUFRJ-ZA-623. (13a-c) Sphyrna sp., vertebrae, Usiminas, MNUFRJ-ZA-572, and (14a-c) Camboinhas, MNUFRJ-ZA-853. Scale bar: 1 cm.

https://doi.org/10.1371/journal.pone.0154476.g010

thumbnail
Fig 11. Teleostean otoliths from the Rio de Janeiro shellmounds.

(1) Albula nemoptera, Algodão, MNUFRJ-ZA-190. (2a-c) Bagre marinus, Algodão, MNUFRJ-ZA-196. (3a-c) Genidens genidens, Camboinhas, MNUFRJ-ZA-845. (4) Hemiramphus sp., Caieira II, MNUFRJ-ZA-316, and (5) Caieira II, MNUFRJ-ZA-317. (6) Centropomus ensiferus, Algodão, MNUFRJ-ZA-206. (7) Centropomus undecimalis, Algodão, MNUFRJ-ZA-205. (8) Epinephelus sp., Major, MNUFRJ-ZA-269. (9) Epinephelus marginatus, Usiminas, MNUFRJ-ZA-521. (10) Lutjanus synagris, Algodão, MNUFRJ-ZA-228. (11) Lutjanus sp., Major, MNUFRJ-ZA-279. (12) Ocyurus chrysurus, Usiminas, MNUFRJ-ZA-519. (13) Diapterus rhombeus, Caieira II, MNUFRJ-ZA-306. (14) Diplodus sp., Algodão, MNUFRJ-ZA-215, and (15) Algodão, MNUFRJ-ZA-217. (16) Gerres cinereus, Algodão, MNUFRJ-ZA-223. (17) Anisostremus virginicus, Algodão, MNUFRJ-ZA-192. (18) Haemulon aurolineatum, Usiminas, MNUFRJ-ZA-517. (19) Haemulon sciurus, Algodão, MNUFRJ-ZA-184). (20) Haemulon steindachneri, Algodão, MNUFRJ-ZA-220. (21) Archosargus rhomboidalis, Algodão, MNUFRJ-ZA-194. (22) Archosargus sp., Algodão, MNUFRJ-ZA-193. (23) Bairdiella ronchus, Algodão, MNUFRJ-ZA-203. (24) Cynoscion jamaicensis, Acaiá, MNUFRJ-ZA-876. (25) Cynoscion microlepidotus, Algodão, MNUFRJ-ZA-213. (26) Cynoscion acoupa, Manitiba, MNUFRJ-ZA-559. (27) Larimus breviceps, Algodão, MNUFRJ-ZA-226. (28) Micropogonias furnieri, Algodão, MNUFRJ-ZA-232. (29) Pareques acuminatus, Manitiba, MNUFRJ-ZA-875.

https://doi.org/10.1371/journal.pone.0154476.g011

thumbnail
Fig 12. Teleostean otoliths from the Rio de Janeiro shellmounds.

(1) Pogonias cromis, Ponte do Girau, MNUFRJ-ZA-562. (2) Umbrina coroides, Ilha do Cabo Frio, MNUFRJ-ZA-874. (3) Mugil liza, Algodão, MNUFRJ-ZA-233. (4) Sphyraena guachancho, Algodão, MNUFRJ-ZA-236. (5) Hyporhamphus unifasciatus, Algodão, MNUFRJ-ZA-2230.

https://doi.org/10.1371/journal.pone.0154476.g012

thumbnail
Fig 13. Teleostean skeletal remains from the Rio de Janeiro shellmounds.

(1a-b) Aspistor sp., hyoid bar, Manitiba, MNUFRJ-ZA-537. (2a-b) Bagre marinus, frontal, Algodão, MNUFRJ-ZA-500. (3a-c) Cathorops sp., dentary, Manitiba, MNUFRJ-ZA-542. (4) Genidens barbus, supraoccipital, Manitiba, MNUFRJ-ZA-538. (5–7) Genidens sp., nucal plate, Manitiba, MNUFRJ-ZA-554, and (8a-b) hyoid bar, Manitiba, MNUFRJ-ZA-534. (9a-b) Sargocentrum sp., dentary, Acaiá, MNUFRJ-ZA-675. (10) Centropomus parallelus, supraoccipital, Usiminas, MNUFRJ-ZA-387. (11a-b) Centropomus undecimalis, premaxillary, Usiminas, MNUFRJ-ZA-439. (12a-c) Epinephelus sp., premaxillary, Usiminas, MNUFRJ-ZA-444, and (13a-c) dentary, Ilha do Cabo Frio, MNUFRJ-ZA-871. (14a-c) Mycteroperca sp., dentary, Usiminas, MNUFRJ-ZA-392. (15a-c) Caranx sp., premaxillary, Camboinhas, MNUFRJ-ZA-851, and (16a-b) dentary, Acaiá, MNUFRJ-ZA-744. (17a-b) Selene vomer, premaxillary, Acaiá, MNUFRJ-ZA-663, and (18a-b) dentary, Acaiá, MNUFRJ-ZA-667. Scale bar 1 cm.

https://doi.org/10.1371/journal.pone.0154476.g013

thumbnail
Fig 14. Teleostean skeletal remains from the Rio de Janeiro shellmounds.

(1a-b) Oligoplites saurus, premaxillary, Usiminas, MNUFRJ-ZA-438. (2a-c) Lutjanus sp., dentary, Algodão, MNUFRJ-ZA-858. (3a-b) Gerreidae indet., premaxillary, Algodão, MNUFRJ-ZA-485. (4a-c) Anisostremus sp., premaxillary, Algodão, MNUFRJ-ZA-859, and (5a-b) dentary, Algodão, MNUFRJ-ZA-692. (6a-b) Diplodus sp., premaxillary, Acaiá, MNUFRJ-ZA-682. (7a-b) Archosargus sp., premaxillary, Ilha do Cabo Frio, MNUFRJ-ZA-873. (8a-b) Sparisoma sp., upper pharyngeal tooth plate, Acaiá, MNUFRJ-ZA-730. (9) Pogonias cromis, pharyngeal tooth, Manitiba, MNUFRJ-ZA-552. (10a-b) Mugil sp., opercle, Manitiba, MNUFRJ-ZA-550. (11a-b) Bodianus rufus, premaxillary, Acaiá, MNUFRJ-ZA-828, and (12a-b) dentary, Ilha do Cabo Frio, MNUFRJ-ZA-872. (13) Sparisoma sp., premaxillary, Usiminas, MNUFRJ-ZA-436. (14a-b) Scarus sp., maxillary, Algodão, MNUFRJ-ZA-993. Scale bar 1 cm.

https://doi.org/10.1371/journal.pone.0154476.g014

thumbnail
Fig 15. Teleostean skeletal remains from the Rio de Janeiro shellmounds.

(1a-b) Scarus sp., angulo-articular, Algodão, MNUFRJ-ZA-496, and (2a-c) pharyngeal tooth, Acaiá, MNUFRJ-ZA-724. (3a-c) Sparisoma sp., dentary, Acaiá, MNUFRJ-ZA-720, and (4a-b) angulo-articular, Acaiá, MNUFRJ-ZA-666. (5a-b) Scarus sp., lower pharyngeal tooth plate, Acaiá, MNUFRJ-ZA-674. (6a-c) Trichiurus lepturus, dentary, Acaiá, MNUFRJ-ZA-746. (7a-b) Katsuwonus pelamis, maxillary, Acaiá, MNUFRJ-ZA-705, and (8a-c) vertebrae, Acaiá, MNUFRJ-ZA-710. (9) Scomberomus sp., hypural complex, Acaiá, MNUFRJ-ZA-701. (10a-b) Istiophorus albicans, hypural, Usiminas, MNUFRJ-ZA-471. (11) Sphyraena barracuda, dentary, Usiminas, MNUFRJ-ZA-395. (12a-b) Lagocephalus laevigatus, premaxillary, Acaiá, MNUFRJ-ZA-679. (13a-c) Sparisoma sp., lower pharyngeal tooth plate, Usiminas, MNUFRJ-ZA-428. (14) Diodon sp., tooth plate, Usiminas, MNUFRJ-ZA-429. (15a-b) Chilomycterus spinosus, dentary, Algodão, MNUFRJ-ZA-487. Scale bar 1 cm.

https://doi.org/10.1371/journal.pone.0154476.g015

Discussion

We recognized 97 fish species from the Rio de Janeiro shellmounds based on detailed anatomic analysis of diagnostic structures. However, some taxonomic records (i.e., at least 44 taxa) that were previously cited in technical reports and unpublished theses about the Rio de Janeiro shellmounds could not be located in the MN-UFRJ repository for identification. These unexamined species are not under institutional catalogue records, and their descriptions or illustrations are not available. We, therefore, choose to exclude those ‘specimens’ from our analysis.

Population structures from shellmounds suggest that the estimated body length of coastal species (e.g., carcharhinids) follows a common pattern of juvenile and adult body length. Moreover, very small teeth and vertebrae of lamnids and sphyrnids collected from the shellmounds of Angra dos Reis and Cabo Frio Island indicate the possible presence of pregnant females, neonates and juveniles in a protected coastal area. Similar evidence is provided by large and very small vertebrae of sawfishes, Pristis spp. (Fig 9).

The Carcharhinus brevipinna size estimation is in agreement with the common length of contemporary specimens (i.e., 250 cm TL [71]), and the species is classified as a threatened species [103]. The estimated sizes of Carcharias taurus are two times smaller than those of their living counterpart (i.e., 250 cm TL [71]), which is classified as a vulnerable species [104]. Juvenile sizes of Carcharhinus species coincide with the most common length of the living counterpart. Sphyrna spp. size is nine times smaller than the common length estimation of the living counterpart and could be represented here by neonate specimens [in comparison with the adults body size (i.e., 370 cm TL [88])]. Sphyrna species are currently classified as an endangered species [105]. The size of Carcharodon carcharias is three times smaller than the common body length of their living counterpart (i.e., 541 cm TL for males and 594 cm for females [88]), which is classified as a vulnerable species [106]. The presence of small vertebrae (and some teeth) is suggestive of neonates of Lamnidae, Carcharhinidae, Sphyrnidae and Pristidae species and provides irrefutable support for the presence of pregnant females and juveniles in these nursery areas.

There are three criteria to identify an area as a nursery [107]: (1), an area with a high frequency of sharks; (2), an area to which shark species have a tendency to remain or return for extended periods; (3), an area or habitat that is repeatedly used across years. Sharks’ philopatry [108] and the evidence of residence and the site fidelity suggest that oceanic species preferentially return to their exact birthplaces (i.e., natal philopatry) or birth regions (i.e., regional philopatry) for either parturition or mating even though they make long distance movements that would allow them to breed elsewhere [109]. Modern philopatric are represented by Holocene species in the Brazilian shellmounds, and include Carcharias taurus, Carcharodon carcharias, Carcharhinus leucas, C. limbatus, Galeocerdo cuvier and Negaprion brevirostris [109].

Special remarks are made regarding the presence of cosmopolitan sharks with long-distance oceanic migration, such as G. cuvier and C. carcharias. The tiger shark, G. cuvier, spends the majority of its time in the upper 50 m of water and is recorded to migrate approximately 1,100 to 1,800 km [110,111,112]. The white shark, C. carcharias, during its ‘patrolling’ behavior, mostly swam in depths between 5 and 50 m and during migration, swam almost exclusively at the surface [113]. The long distance oceanic migration of this shark is record to be approximately 4,000 km between the Pacific coast of California and Mexico to the Hawaiian islands [113,114]. Both tiger and white sharks were represented in the shellmounds by perforated teeth, some of them recovered as pendant necklaces associated with human burials and bones [115]. Moreover, modern shark nursery areas were recognized in Brazil [116,117].

Estimated teleostean size class ranges in selected shellmounds, based on 5,532 otoliths of Micropogonias furnieri, showed a long history of fishery exploitation (ca 5,595 cal BP until today). The frequency distribution of whitemouth croaker, M. furnieri, body sizes based on otoliths from the Ponte do Girau, Algodão, Beirada, Manitiba and Camboinhas shellmounds, and the body size (TL) estimates from modern fisheries (i.e., artisanal and semi-industrial) in the Itaipu and Angra dos Reis regions, Rio de Janeiro State (Fig 4), suggest two modal distributions of body size frequencies, with overlap between prehistoric and modern fisheries. In comparison to the size estimated based on otoliths of M. furnieri from the shellmounds, a probabilistic tendency of a reduction in body size of 28% in modern catches may be attributed to overexploitation.

Despite M. furnieri being a species with medium resilience to fishing pressure (i.e., criteria based on values of selected life-history parameters: high fertility and high body growth parameter, K [118]), the regional assessments of current stocks indicate overexploitation [89,90]. Results indicate that body size medians between shellmounds and related environment/coastal geomorphology were significantly different (Fig 5). These differences could be interpreted as a consequence of seasonal variations of fishery areas and the intrinsic life history of the species.

The prehistoric fisheries and time series records along archaeostratigraphic sections vary from a single to seven layers based on the chronological sequences of settlements studied here, while the calibrated radiocarbon models, based on fish otoliths and shell samples by layer, show close or overlapping age probability distributions of individual shellmounds [52,53,55]. Consequently, the shallow profile of individual shellmounds studied here from Rio de Janeiro State could be treated arbitrarily as a single unit for the purpose of a fisheries analysis.

The results, in terms of richness, point toward an early stage of overexploitation of medium- to large-sized, vulnerable fish species, characterized by late maturity, slow growth, low reproductive rates, longevity, spawning aggregations and often ovoviviparous and/or viviparous life histories [119,120,121]. Groupers also exhibit slow growth, low reproductive rates and increased longevity, and reproductive adults leave shallow water habitats and move to deep waters after spawning [122,123]. Our results suggest that prehistoric fishing pressure on coastal areas was sufficient to cause the initial phase of population declines [58,124,125].

Prehistoric fishery methods were able to catch medium to large sharks, skipjack tunas, sailfish and groupers and could have included seined or floating gillnets, spears and long-lines. However, more resilient demersal species did not decline as drastically. Therefore, it is plausible that seasonal fisheries that used beach seines during high upwelling productivity contributed to massive catches of groundfish schools. Other small species could be caught by hooks or traps.

Sawfishes were present during prehistoric times in southeastern Brazil [126]; however, nowadays, these species are a nearly extinct taxon [127], and the last record of the great white shark was in the mid 80’s [128]. Carcharias taurus is a common shark caught in summer in small numbers in artisanal gillnet fisheries on the Rio de Janeiro coast [128]. Nothing is known about the porbeagle shark, Lamna nasus, in the Brazilian region, a rare shark caught in longlines from the 60’s to the 90’s [129]. This species is distributed from southern Brazil and Uruguay to Argentina [130].

Diverse evidence of archaeological artifacts of gorges, bones and shell fishhooks (including an early fishhook, dated to 42,000 yr BP [131]) and fishing lines (from native fiber plants or human hair) used for inshore or pelagic fisheries was recorded worldwide [15,132,133]. The presence of projectile points in archaeological sites in California, USA (~ 12,200 to 11,200 yr BP) associated with marine and aquatic faunal remains is common [134]. Moreover, the only known evidence of fishery tools from Brazilian archaeological sites are manufactured bony spear-tips [30], without clear evidence of possible techniques for massive catches or refined manufacture of hooks used for pelagic or large demersal fishes (S4 Appendix).

Shark teeth are culturally significant in the worldview of indigenous mythology, and numerous archaeological burials of human skeletons in Brazilian shellmounds were decorated with necklaces made with drilled shark teeth [115]. Drilled shark teeth are also present in Argentinian and Uruguayan middens [135]. Individually, drilled shark teeth are here represented by Carcharodon carcharias, Galeocerdo cuvier, Carcharhinus altimus, C. leucas, C. plumbeus and Sphyrna mokarran (Fig 7). However, another possibility is the use of shark teeth for tool manufacturing, e.g., affixed to pieces of wood with vegetal fibers, similar to Polynesian artifacts [127], or as points of arrows.

The analysis of the ichthyofauna shows significant differences between expected fish assemblages (i.e., based on modern occurrences in the coastal area) and the record of observed species in shellmounds (Table 2, Figs 715). A high diversity of fish species in the shellmounds reveals the fishery and coastal navigation skills of ancient fishermen and the high importance of coastal fisheries for those prehistoric communities. Such prehistoric fishery activities on vulnerable species and special nursery areas could correspond to the beginning of fish stock depletion along the southeastern Brazilian coast. Overexploitation of such coastal fisheries became unequivocally intense during colonial times resulting in the near collapse of natural fish populations, especially affecting large-sized species such as sharks and giant groupers.

However, in terms of natural resources, we assume that eight biases might have affected the ichthyoarchaeological samples under study: (1), selective targeting of certain species (i.e., unpalatable taste, poisonous fishes, small sizes, etc.); (2), the inaccessibility of certain available species (e.g., limitations of employed fishing techniques or presence of adverse marine environmental conditions); (3), minimal potential preservation of some species (i.e., some fishes such as sardines could be consumed entirely); (4), non-uniform employment of archaeological sieving techniques (i.e., the use of large mesh sizes and loss of small stingray teeth such as those of Dasyatis, Gymnura, or Mobula species and otoliths, like those of syngnathids, cynoglossids, achirids, atherinids, bleniids and gobiids); (5), archaeological priority (i.e., ichthyoarchaeological remains such as bones, teeth and otoliths could be considered of secondary importance during field activities, except when they exhibit holes, cutting or intentional abrasion); (6), early overexploitation and fish stock depletion (i.e., large and diverse shark species and rocky reef fish are well represented only in the Angra dos Reis shellmounds); (7), the presence of non-diagnostic or broken bones or eroded otoliths (i.e., unclassified species); and (8), missing specimens.

Conclusions

Prehistoric fishery activity along the Rio de Janeiro coast under the influence of coastal marine upwellings was characterized by massive catches of demersal finfish that inhabit sandy and coastal marine lagoons (e.g., Micropogonias furnieri), rocky reef fishes caught near islands and islets (e.g., Epinephelus morio), and pelagic fishes caught near rocky cliffs and islands (e.g., Istiophorus albicans). Shark fisheries could have been located in nursery areas of protected rocky cliff bays in Arraial do Cabo, Cabo Frio Island, Angra dos Reis and Ilha Grande.

Prehistoric records of high elasmobranch diversity in the Ribeira Bay provide clear evidence for the exploitation of natural populations of sharks and rays since pre-colonial times, especially of bigger species such as the porbeagle shark, Lamna nasus, the sand tiger shark, Carcharias taurus, the great white shark, Carcharodon carcharias, and sawfishes, Pristis sp. All these are vulnerable species that could have been rare, especially when taking into consideration that today they are rare or present in reduced numbers in the Ribeira Bay or in the adjacent Angra dos Reis region.

Hence, the results produced here should be addressed as a baseline reference of the ichthyodiversity during the prehistoric times, promoting further debate on the relationships established with past fishing activities, as well as changes in local and regional oceanographic systems.

Supporting Information

S1 Appendix. Distribution of shellmounds along the South American coast.

https://doi.org/10.1371/journal.pone.0154476.s001

(DOCX)

S2 Appendix. Ichthyoarchaeological material.

Ichthyological collection, Zooarchaeology, Museu Nacional, Universidade Federal do Rio de Janeiro (UFRJ)–curators: Maria Cristina Tenório, Tânia Lima.

https://doi.org/10.1371/journal.pone.0154476.s002

(DOCX)

S3 Appendix. Modern material.

A. Ichthyological collection, Departamento de Biologia Animal e Vegetal—Instituto de Biologia, Universidade do Estado do Rio de Janeiro (UERJ)—curators: Ulisses Leite Gomes, Maisa da Cruz Lima, Cristina Paragó, Alexandra Pinto Quintans. B. Ichthyological collection, Otoliths, Departamento de Biologia Marinha—Instituto de Biologia, Universidade Federal Fluminense (UFF)–curator: Orangel Aguilera. C. Ichthyological collection, Dry skeletons, Departamento de Biologia Marinha—Instituto de Biologia, Universidade Federal Fluminense (UFF)–curators: Orangel Aguilera.

https://doi.org/10.1371/journal.pone.0154476.s003

(DOC)

S4 Appendix. The unknown prehistoric fishing.

Artwork by Eduardo Agelvis.

https://doi.org/10.1371/journal.pone.0154476.s004

(DOCX)

Acknowledgments

The authors would like to thank Angela Camardella and Winner Soares for assistance in the shellmounds repository of MN-UFRJ. Filomena Crancio helped us during our fieldtrip to the Saquarema region and the visit to the shellmounds. Fernando Tuna helped us during the acquisition of otolith measurements and the preparation of the osteological collection. We thank David Canabarro for assistance during the field trip to the Cabo Frio Island and for geomorphological explanations. Thanks to Ana Luiza Albuquerque and Andre Belem for constructive discussions about the coastal upwelling in southeastern Brazil. We thank Edson Silva and Aguinaldo Nepomuceno for UFF laboratorial facilities. Thanks also to Werner Schwarzhans for reviewing the otolith identification and Marcelo Ricardo Souza for helping with statistics in the R software. Orangel A. Rodrigues helped us with image editing, Filipe Leite Rufato with the macrophotography of Acaiá samples and Thodoris Argyriou with the first English revision of the draft manuscript. The authors wish to especially thank Eduardo Agelvis for the remarkable artwork. Special thanks Aaron O′Dea, Anastasia Yutseva and anonymous reviewers who has greatly improved the manuscript.

Author Contributions

Conceived and designed the experiments: MSL TCPB RAT CMN OA. Performed the experiments: MSL TCPB RAT CMN ARGT JDCB MH KM OA. Analyzed the data: MSL TCPB RAT CMN ARGT JDCB MH KM OA. Contributed reagents/materials/analysis tools: LR MCT TL RS MH KM CC OA. Wrote the paper: MSL TCPB OAS. Revised and edited the manuscript: MSL TCPB RAT CMN ARGT JDCB TL OA.

References

  1. 1. Wagner G, Hilbert K, Bandeira D, Tenório MC, Okumura MM. Sambaquis (shell mounds) of the Brazilian coast. Quat Int. 2011; 239: 51–60.
  2. 2. Lima TA. Dos mariscos aos peixes: um estudo zooarqueológico de mudança de subsistência na pré-história do Rio de Janeiro. M.Sc. Thesis, Universidade de São Paulo. 1991. Available: http://www.worldcat.org/title/dos-mariscos-aos-peixes-um-estudo-zoo-arqueologico-de-mudanca-de-subsistencia-na-pre-historia-do-rio-de-janeiro/oclc/46754734.
  3. 3. Dos Santos CMC. A Ictiofauna do sambaqui de Camboinhas, Niterói, RJ. Documento de trabalho: Sér Arqueol. 1995; 3: 65–72.
  4. 4. Magalhaes RMM, Curvelo MA, Mello EMB. O sambaqui de Manitiba I e outros sambaquis de Saquarema, RJ. In: A fauna na alimentação. Documentos de Trabalho, Sér Arqueol Mus Nac, UFRJ. 2001; 5: 55–69.
  5. 5. Kneip LM. O sambaqui de Manitiba I e outros sambaquis de Saquarema, RJ. Sér Arqueol Mus Nac. UFRJ. 2001; 5–91.
  6. 6. Gonzalez MMB. Use of Pristis spp. (Elasmobranchii: Pristidae) by hunter-gatherers on the coast of São Paulo, Brazil. Neotrop. Ichthyol. 2005a; 3: 421–426.
  7. 7. Gonzalez MMB. Tubarões e raias na pré-história do litoral de São Paulo. PhD thesis, Universidade de São Paulo, Brasil. 2005b. Available: http://www.teses.usp.br/teses/disponiveis/71/71131/tde-29092006-114551/pt-br.php
  8. 8. Gonzalez MMB. Utilização de ferrões de raias pelos grupos de pescadores-coletores do litoral de São Paulo. Cad. CEON Cult. Mater. 2014; 24: 99–122.
  9. 9. Guimarães MB. A ocupação pré-colonial da região dos Lagos, RJ: Sistema de assentamento e relações intersocietais entre grupos sambaquianos e grupos ceramistas Tupinambá e de tradição Una. PhD Thesis. Universidade de São Paulo. 2007. Available: http://www.teses.usp.br/teses/disponiveis/71/71131/tde-05092007-111015/pt-br.php
  10. 10. Klokler D, Villagrán XS, Giannini PCF, Peixoto S, DeBlasis P. Juntos na costa: zooarqueologia e geoarqueologia de sambaquis do litoral sul catarinense. Rev. Mus. Arqueol. Etnol. 2010; 20: 53–75.
  11. 11. Hilbert LM. Análise ictioarqueológica dos sítios: Sambaqui do Recreio, Itapeva e Dorva, municípios de Torres e Três Cachoeiras, Rio Grande do Sul, Brasil. M.Sc. Thesis, Pontifícia Universidade Católica do Rio Grande do Sul. 2011. Available: http://tede2.pucrs.br/tede2/bitstream/tede/204/1/430797.pdf.
  12. 12. Fossile T. Peixes na alimentação de povos pré-coloniais: Estudo ictioarqueológico do sambaqui Cubatão I. M.Sc. Thesis, Universidade da Região de Joinville. 2013. Available: https://www.academia.edu/7820800/PEIXES_NA_ALIMENTA%C3%87%C3%83O_DE_POVOS_PR%C3%89-COLONIAIS_ESTUDO_ICTIOARQUEOL%C3%93GICO_DO_SAMBAQUI_CUBAT%C3%83O_I.
  13. 13. Baisre JA. Setting a baseline for Caribbean fisheries. JICA. 2010; 5: 120–147.
  14. 14. Wing SR, Wing ES. Prehistoric fisheries in the Caribbean. Coral Reefs. 2001; 20: 1–8.
  15. 15. Erlandson JM, Rick TC, Braje TJ, Steinberg A, Vellanoweth RL. Human impacts on ancient shellfish: a 10,000 year record from San Miguel Island, California. J Archaeol Sci. 2008; 35: 2144–2152.
  16. 16. Fitzpatrick SM. Viewing the sea from the reefs. Comment and forum synthesis on Julio Baisre’s “Setting a baseline for Caribbean fisheries. JICA. 2010; 5: 173–178.:
  17. 17. McClenachan L, Hardt M, Jackson J, Cooke R. Mounting evidence for historical overfishing and long-term degradation of Caribbean marine ecosystems: comment on Julio Baisre’s “Setting a baseline for Caribbean fisheries”. JICA. 2010; 5: 165–169.
  18. 18. Jones S. Considerations for advancing a dialogue on pre-modern marine exploitation in the Caribbean and beyond: comment on Julio Baisre’s “Setting a baseline for Caribbean fisheries”. JICA. 2010; 5: 159–161.
  19. 19. Cramer KL. History of human occupation and environmental changes in western and central Caribbean Panama. Bull Mar Sci. 2013; 89(4): 955–982.:
  20. 20. Polis GA, Anderson WB, Holt RD. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst. 1997; 28: 289–316.
  21. 21. Reitz E. Fishing down the food web: A case study from St. Augustine, Florida, USA. Am Antiq. 2004; 69: 63–83.
  22. 22. Erlandson JM, Rick TC. Archaeology meets marine ecology: the antiquity of maritime cultures and human impacts on marine fisheries and ecosystems. Ann Rev Mar Sci. 2010; 2:165–185.
  23. 23. Rick TC, Kirch PV, Erlandson JM, Fitzpatrick SM. Archeology, deep history, and the human transformation of island ecosystems. Anthropocene. 2013.
  24. 24. Prous A. Arqueologia brasileira. 1st ed. Brasil: Editora da Universidade de Brasilia, Brasília Press. 1992.
  25. 25. Gaspar MD. Análises das datações radiocarbônicas dos sítios de pescadores, coletores e caçadores. Bol Mus. Paraense Emilio Goeldi. 1996; 8: 81–91.
  26. 26. Lima TA. Em busca dos frutos do mar: os pescadores-coletores do litoral centro-sul do Brasil. Rev USP. 1999–2000; 44: 270–332.
  27. 27. Lima TA, Macario KD, Anjos RM, Gomes PRS, Coimbra RS, Elamore E. AMS dating of early shellmounds of the southeastern Brazilian coast. Braz J Phys. 2003; 33(2): 276–279.
  28. 28. Lima TA, Macario KD, Anjos RM, Gomes PRS, Coimbra MM, Elmore D. The earliest shellmounds of the central-south Brazilian coast. Nucl Instr Meth Phys Res. 2004; 691–694.
  29. 29. Tenório MC, Afonso MC, Pinto D. Arqueologia do Arraial do Cabo com foco nos sítios da Ilha do Cabo Frio. Rev Mus Arqueol Etnol. 2010; 20: 127–145.
  30. 30. Guimarães MB. Fishing strategies among prehistoric populations at Saquarema lagoonal complex, Rio de Janeiro, Brazil. An Acad Bras Ciênc. 2013; 85(1): 415–429. pmid:23460437
  31. 31. Macario KD, Souza RCCL, Trindade DC, Decco J, Lima TA, Aguilera AO, et al. Chronological model of a Brazilian Holocene shellmound (sambaqui da Tarioba), Rio de Janeiro, Brazil Radiocarbon. 2014; 56: 489–499.
  32. 32. Scartascini FL, Charo M, Volpedo A. Caracterización de las estrategias de obtención de recursos ícticos a partir del análisis de otolitos. El caso de la costa norte del Golfo San Matías. In: Salemme M, Santiago F, Álvarez M, Piana E, Vázquez M, Mansur E, editors. Arqueología de Patagonia: una mirada desde el último confín, Tomo II. Utopias. 2009. pp. 845–852.
  33. 33. Favier CM, Scartascini FL. Intensive fishery scenarios on the North Patagonian coast (Río Negro, Argentina) during the Mid-Holocene. Quat Int. 2012; 256: 62–70.
  34. 34. Scartascini FL, Volpedo AV. White croaker (Micropogonias furnieri) paleodistribution in the Southwestern Atlantic Ocean. An archaeological perspective. J Archael Sci. 2013; 40: 1059–1066.
  35. 35. Scartascini FL, Sáez M, Volpedo AV. Otoliths as a proxy for seasonality: The case of Micropogonias furnieri from the northern coast of San Matías Gulf, Río Negro, Patagonia, Argentina. Quat Int. 2014.:
  36. 36. Calippo FR. O surgimento da navegação entre os povos dos sambaquis: argumentos, hipóteses e evidências. Rev Mus Arqueol Etnol. 2011; 21: 31–49.
  37. 37. Okumura MMM, Boyadjian CHC, Eggers S. Análise da exostose do meato auditivo externo como um marcador de atividade aquática em restos esqueletais humanos da costa e do interior do Brasil. Rev Mus Arqueol Etnol. 2005–2006; 15(16): 181–197.
  38. 38. Okumura M. Populações Sambaquianas Costeiras: saúde e afinidades biológicas dentro de um contexto geográfico e temporal. Rev Temp Acad Arq Pré-Histórica. 2013; 11: 38–53.
  39. 39. Frayer DW. Auditory exostoses and evidence for fishing at Vlasac. Curr Anthropol, 1988; 29: 346–349.
  40. 40. Hurst W, Bailey M, Hurst B. Prevalence of external auditory canal exostoses in Australian surfboard riders. J Laryngol Otol, 2004; 118: 348–351. pmid:15165308
  41. 41. Litu MLA, Al mamun A, Alam Z, Haque R, Hanif A, Hossain A. Exostoses of the external auditory canal. Bangladesh J Otorhinolaryngol. 2012; 18: 91–95.
  42. 42. Villagran XS, Klokler D, Peixoto S, DeBlasis P, Giannini PCF. Building coastal landscapes: Zooarchaeology and Geoarchaeology of Brazilian shellmounds. JICA. 2011; 6: 211–234.
  43. 43. Wagner GP, Silva LA. Prehistoric maritime domain and Brazilian shellmounds. Archaeol. Disc. 2014; 2 (1): 1–5.:
  44. 44. Barbosa-Guimarães MS. Análise espacial intra-sítio: Um estudo de caso no sítio Ilha da Boa Vista, Cabo Frio, RJ. BRMN/A. 2006; 64(4): 271–286.
  45. 45. Gaspar MD, Klokler D, Bianchini GF. Arqueologia estratégica: abordagens para o estudo da totalidade e construção de sítios monticulares. Boletim do Museu Paraense Emílio Goeldi. Ciências Humanas, 2013; 8(3): 517–533.
  46. 46. Kneip LM, Pallestrini L, Crancio F, Machado LMC. As estruturas e suas inter-relações em sítios de pescadores-coletores pré-históricos do litoral de Saquarema, RJ. B IAB. 1991; 5: 1–42.
  47. 47. Turcq B, Martin L, Flexor JM, Suguio K, Pierre C, Tasayco-Ortega L. Origin and evolution of the Quaternary coastal plain between Guaratiba and Cabo Frio, State of Rio de Janeiro, Brazil. In: Knoppers BA, Bidone ED, Abrãao JJ, editors. Environmental geochemistry of coastal lagoon systems of Rio de Janeiro. UFF/FINEP. 1999; 6: 25–46.
  48. 48. Souto DD, Lessa DVO, Albuquerque ALS, Sifeddine A, Turcq BJ, Barbosa CF. Marine sediments from southeastern Brazilian continental shelf: A 1,200 year record of upwelling productivity. Palaeogeogr Palaeoclimatol Palaeoecol, 2011; 299: 49–55.
  49. 49. Coelho-Souza SA, López MS, Guimarães JRD, Coutinho R, Candella RN. Biophysical interactions in the Cabo Frio upwelling system, Southeastern Brazil. Braz J Oceanogr, 2012; 60: 353–365.
  50. 50. Belem AL, Castelao RM, Albuquerque ALS. Controls of subsurface temperature variability in a western boundary upwelling system. Geophys Res Lett, 2013; 40: 1362–1366.
  51. 51. Cordeiro LGM, Belem AL, Bouloubassi I, Rangel B, Sifeddine A, Capilla R, et al. Reconstruction of Southwestern Atlantic Sea Surface Temperatures during the last Century: Cabo Frio Continental Shelf (Brazil). Palaeogeogr Palaeoclimatol Palaeoecol, 2014.
  52. 52. Macario KD, Souza RCCL, Aguilera OA, Carvalho C, Oliveira FM, Alves EQ, et al. Marine reservoir effect on the Southeastern coast of Brazil: results from the Tarioba shellmound paired samples. J Environ Radioact, 2015; 143: 14–19. pmid:25703433
  53. 53. Alves E, Macario K, Souza R, Aguilera O, Goulart AC, Scheel-Ybert R, et al. Marine reservoir corrections on the southeastern coast of Brazil: paired samples from the Saquarema shell mound. Radiocarbon, 2015; 57: 1–9.
  54. 54. Aguilera OA, Angelica R, Macario K, Crapez M, Belem A, Monteiro-Neto C, et al. Fish bone diagenesis in Southeastern Brazilian shell mounds: Paleoenvironmental approach. Quat Int. 2015.
  55. 55. Carvalho C, Macario K, Oliveira MI, Oliveira F, Chanca I, Alves E, et al. Potential use of archaeological snail shells for the calculation of local marine reservoir effect. Radiocarbon, 2015; 57(3): 1–9.
  56. 56. Soares de Sousa G. Tratado descriptivo do Brasil em 1587. Tipografia Universal Laemmert, Rio de Janeiro. 1851; 1: 518. Available: http://www.brasiliana.com.br/brasiliana/colecao/obras/9/Tratado-descritivo-do-Brasil-em-1587.
  57. 57. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, et al. Historical overfishing and the recent collapse of coastal ecosystems. Science. 2001; 293–629.:
  58. 58. Bender MG, Machado GR, Silva PJA, Floeter SR, Monteiro-Netto C, Luiz OJ, et al. Local ecological knowledge and scientific data reveal, overexploitation by multigear artisanal fisheries in the Southwestern Atlantic. Plos One. 2014; 9 10: 110–332.
  59. 59. McClenachan L, Jackson JBC, Newman MJH. Conservation implications of historic sea turtle nesting beach loss. Front. Ecol. Environ. 2006; 4: 290–296.
  60. 60. Antczak A, Buitrago J, Mackowiak de Antczak MM, Guada HJ. A Contribution to the history of marine turtles exploitation in Venezuela. 59th Gulf Caribb. Fish. 2007; 63–73.
  61. 61. McClenachan L, Coope A. Extinction rate, historical population structure and ecological role of the Caribbean monk seal. Proc Math Phys Eng Sci. 2008; 275: 1351–1358.
  62. 62. Castilho PV. Utilization of cetaceans in shell mounds from the southern coast of Brazil. Quat Int. 2008; 180: 107–114.
  63. 63. Castilho PV, Simões-Lopes PC. Zooarqueologia dos mamíferos aquaticos e semi-aquaticos da ilha de Santa Catarina, sul do Brazil. Rev Bras Zool. 2001; 18: 719–727.
  64. 64. Castilho P, Simões-Lopes PC. Sea mammals in archaeological sites on the southern coast of Brazil. Rev Mus Arqueol Etnol. 2008; 18: 101–113.
  65. 65. Savi DC, Tenório MC, Calippo FR, Toledo FAL, Gonzalez MMB, Afonso MC. Beachrock e o sambaqui da Ilha do Cabo Frio. ABEQUA, 2005; 10: 29–32.
  66. 66. Plew MG. Explorations in American archaeology. Essays in honor of Wesley R. Hurt. Universidade Press of America. 1 st ed. Inc. Boston Press; 1998.
  67. 67. Eirado LG, Heilbron M, Almaeida JCH. Os terrenos tectonicos da faixa ribeirana na serra da Bocaina e na baía da Ilha Grande, Sudeste do Brasil. Rev Bras Geoc, 2006; 36(3), 426–436.
  68. 68. Dias GTM, Kjerfve B. Barrier and beach ridge systems of the Rio de Janeiro coast. In: Dillenburg SR, Hesp P, editors. Geology and Geomorphology of Holocene Coastal Barriers of Brazil Lectures Notes in Earth Sciences 107. Springer-Verlag Berlin Heidelberg. 2009. pp. 225–252.
  69. 69. Motoki A, Sichel SE, Savi DC, Aires JR. Mecanismo de intrusão dos corpos tabulares de colocação sub-horizontal discordantes, Município de Arraial do Cabo, RJ. UNESP Geociências, 2008; 27 (2): 207–218.
  70. 70. Castro JWA, Suguio K, Cunha am, Guedes , Tâmega FTS, Rodriguez RR. Rochas de Praia (Beachrocks) da Ilha do Cabo Frio, Arraial do Cabo: Registro Geológico Ímpar da Transição Pleistoceno—Holoceno no Estado do Rio de Janeiro. Anu. Inst. Geociênc—UFRJ, 2012; 35(1): 236–241.
  71. 71. Tenório MC, Afonso MA, Savi D, Pinto DC, Gonzalez MMB, Amenomori SN, et al. O sítio ou os sítios da Ilha do Cabo Frio: primeiros resultados. In: An XIII Congr SAB, 2005, Campo Grande-MS.
  72. 72. Kneip LM. O sambaqui de Saquarema, RJ: estrutura e estratigrafia. Rio de Janeiro, Sér Arqueol Mus Nac UFRJ, 1995; 3:39–52.
  73. 73. Kneip LM. O sambaqui de Manitiba I e outros sambaquis de Saquarema, RJ. Sér Arqueol Mus Nac UFRJ. 2001; 1:5–91.
  74. 74. Beltrão M. Pré-História do Estado do Rio de Janeiro. Forense Universitária, Rio de Janeiro, 2001; 1996 p.
  75. 75. Kneip LM, Pallestrini L, Cunha FL. Pesquisas arqueológicas no litoral de Itaipu, Niterói, RJ. Rio de Janeiro, 1981.
  76. 76. Lima TA. Dos mariscos aos peixes: um estudo zooarqueológico de mudança de subsistência na pré-história do Rio de Janeiro. M.Sc. Thesis, Universidade de São Paulo. 1991. Available: http://www.worldcat.org/title/dos-mariscos-aos-peixes-um-estudo-zoo-arqueologico-de-mudanca-de-subsistencia-na-pre-historia-do-rio-de-janeiro/oclc/46754734.
  77. 77. Tubino RA, Monteiro-Neto C, Moraes LES, Paes ET. Artisanal fisheries production in the coastal zone of Itaipu, Niterói, RJ, Brazil. Braz J Oceanogr, 2007; 55(3): 187–197.
  78. 78. Gottschalk S, Kahlert M. Shifts in taxonomical and guild composition of littoral diatom assemblages along environmental gradients. Hydrobiologia, 2012; 694(1): 41–56.
  79. 79. Rábago-Quiroz CH, López-Martínez J, Valdez-Holguín JE, Nevárez-Martínez M. O, Acevedo-Cervantes A. Fish assemblages in the bycatch of bottom shrimp trawls on the west side of the Gulf of California, Mexico. Mar Biol, 2012; 8(9): 865–876.
  80. 80. Hughes RM, Herlihy AT, Sifneos JC. Predicting aquatic vertebrate assemblages from environmental variables at three multistate geographic extents of the western USA. Ecol Indic, 2015; 57: 546–556.
  81. 81. Hammer O, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica, 2001; 4(1): 9.
  82. 82. Goldman KJ, Branstetter S, Musick JA. A re-examination of the age and growth of sand tiger sharks, Carcharias taurus, in the western North Atlantic: the importance of ageing protocols and use of multiple back-calculation techniques. Environ Biol Fishes, 2006; 77: 241–252.
  83. 83. Kotas JE, Mastrochirico V, Petrere M Jr.. Age and growth of the Scalloped Hammerhead shark, Sphyrna lewini (Griffith and Smith, 1834), from the southern Brazilian coast. Braz J Biol, 2011; 71: 755–761. pmid:21881801
  84. 84. Allen BR, Wintner SP. Age and growth of the spinner shark Carcharhinus brevipinna (Muller and Henle, 1839) off the KwaZulu-Natal coast, South Africa. Afr J Mar Sci, 2002; 24: 1–8.
  85. 85. Natanson LJ. Preliminary investigations into the age and growth of the shortfin mako, Isurus oxyrinchus, white shark, Carcharodon carcharias, and thresher shark, Alopias vulpinus, in the Western North Atlantic Ocean. Col. Vol. Sci. Pap. ICCAT, 2002; 54(4): 1280–1293.
  86. 86. Desmarest AG. Première décade ichthyologique, ou description complète de dix espèces de poissons 1823 nouvelles, ou imparfaitement connues, habitant la mer qui baigne les côtes de l'île Cuba. Mém Soc Linn Paris, 1983; 2: 163–210.
  87. 87. Menezes NA, Buckup PA, Figueiredo JL, Moura RL. Catálogo das espécies de peixes marinhos do Brasil. São Paulo: Museu de Zoologia, 2003, 159 p.
  88. 88. Froese R, Pauly D, editors. FishBase. 2012; version 06–2012. Available: http://www.fishbase.org
  89. 89. Carneiro MH, Castro PMG, Tutui SLS, Bastos GCC. Micropogonias furnieri (Desmarest, 1823): Estoque sudeste. In: Cergole MC, Ávila-da-Silva AO, Rossi-Wongtschowski CL. Análise das principais pescarias comerciais da região Sudeste-Sul do Brasil: Dinâmica populacional das espécies em explotação. São Paulo, Instituto Oceanográfico-USP; 2005, pp 94–100. Available: http://www.mma.gov.br/estruturas/revizee/_arquivos/revizee_analise_prin_pes.pdf
  90. 90. Haimovici M, Ignácio JM. Micropogonias furnieri (Desmarest, 1823): Estoque sul. In: Cergole MC, Ávila-da-Silva AO, Rossi-Wongtschowski CL. Análise das principais pescarias comerciais da região Sudeste-Sul do Brasil: Dinâmica populacional das espécies em explotação. São Paulo, Instituto Oceanográfico-USP; 2005. pp. 101–107.
  91. 91. Mulato IP, Corrêa B, Vianna M. Distribuição espaço-temporal de Micropogonias furnieri (Perciformes, Sciaenidae) em um estuário tropical no sudeste do Brasil. Bol. Inst. Pesca, 2015; 41(1): 1–18.
  92. 92. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2012. ISBN 3-900051-07-0, Available: http://www.R-project.org.
  93. 93. Netto EB, Gaelzer LR. Associações de peixes bentónicos e demersais na região do Cabo Frio, RJ, Brasil. Nerítica, 1991; 6(1–2): 139–156.
  94. 94. Silva PJA. Onze anos de produçao pesqueira na regiao de Arraial do Cabo-RJ. M.Sc. Thesis, Universidade Federal Fluminense, Brasil. 2004.
  95. 95. Monteiro-Neto C, Tubino RA, Moraes LES, Neto JPM, Gustavo V, Esteves GV, et al. Associações de peixes na região costeira de Itaipu, Niterói, RJ. Iheringia, Sér Zool, 2008; 98(1): 50–59.
  96. 96. Andreata JV, Meurer BC, Baptista MGS, Manzano FV, Teixeira DE, Longo MM, et al. Composiçao da assembleia da Baía da Ribeira, Angra dos Reis, Rio de Janeiro, Brasil. Rev Bras Zool, 2002; 19(4): 1139–1146.
  97. 97. Macario KD, Gomes PRS, Anjos RM, Carvalho C, Linares R, Alves EQ, et al. The Brazilian AMS radiocarbon laboratory (LAC-UFF) and the intercomparison of results with CENA and UGAMS. Radiocarbon, 2013; 55: 325–330.
  98. 98. Castro MD. Espectrometria de massa com aceleradores. Software para análise de dados e efeito reservatório em Cuba. PhD Thesis, Universidade Federal Fluminense, Instituto de Física, Brasil. 2015.
  99. 99. Bronk Ramsey C, Lee S. Recent and planned developments of the program OxCal. Radiocarbon, 2013; 55(2–3): 720–730.
  100. 100. Reimer RW, Richards DA, Scott EM, Southon JR, Staff RA, Turney CSM, et al. IntCal13 and marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon, 2013; 55: 1869–1887.
  101. 101. Alves E, Macario K, Souza R, Pimenta A, Douka K, Oliveira F, et al. Radiocarbon reservoir corrections on the Brazilian cost from pebomb marine shells. Quat Geochronol, 2015b; 29:30–35.
  102. 102. Tenório MC, Pinto DC, Afonso MC. Dinamica de ocupação, contatos e trocas no litoral do Rio de Janeiro no período de 4000 a 2000 anos antes do presente. Arq Mus Nac, 2008; 66(2): 311–321.
  103. 103. Burgess GH. Carcharhinus brevipinna. The IUCN red list of threatened species. 2009; version 2014.3. Available: http://www.iucnredlist.org
  104. 104. Pollard D, Smith A. Carcharias taurus. The IUCN red list of threatened species. 2009; version 2014.3. Available: http://www.iucnredlist.org
  105. 105. Denham J, Stevens J, Simpfendorfer CA, Heupel MR, Cliff G, Morgan A, et al. Sphyrna mokarran. The IUCN red list of threatened species. 2007; version 2014.3. Available: http://www.iucnredlist.org.
  106. 106. Fergusson I, Compagno LJV, Marks M. Carcharodon carcharias. The IUCN red list of threatened species. 2009; version 2014.3. Available: http://www.iucnredlist.org
  107. 107. Heupel MR, Carlson JK, Simpfendorfer CA. Shark nursery areas: concepts, definition, characterization and assumptions. Mar Ecol Prog Ser, 2007; 337: 287–297.
  108. 108. Hueter RE, Heupel MR, Heist EJ, Keeney DB. Evidence of Philopatry in Sharks and Implicationsfor the Management of Shark Fisheries. J Northwest Atl Fish Sci, 2004; 35: 239–247.
  109. 109. Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE. There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Ann Rev Mar Sci, 2015; 7:547–704. pmid:25251267
  110. 110. Holmes BJ, Pepperell JG, Griffiths SP, Jaine FRA, Tibbetts IR, Bennett MB. Tiger shark (Galeocerdo cuvier) movement patterns and habitat use determined by satellite tagging in eastern Australian waters. Mar Biol, 2014; 161: 2645–2658.
  111. 111. Vaudo JJ, Wetherbee BM, Harvey G, Nemeth RS, Aming C, Burnie N, et al. Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic. Ecol Evol, 2014; 4(10): 1768–1786. pmid:24963376
  112. 112. Werry JM, Planes S, Berumen ML, Lee KA, Braun CD, Clua E. Reef-fidelity and migration of tiger sharks, Galeocerdo cuvier, across the Coral Sea. PlosOne, 2014; 9(1): 1–18.:
  113. 113. Jorgensen SJ, Arnoldi NS, Estess EE, Chapple TK, Rückert M, Anderson SD, et al. Eating or Meeting? Cluster Analysis Reveals Intricacies of White Shark (Carcharodon carcharias) Migration and Offshore Behavior. PLoS ONE, 2012; 7(10): 47819.:
  114. 114. Domeier ML, Nasby-Lucas N. Migration patterns of white sharks Carcharodon carcharias tagged at Guadalupe Island, Mexico, and identification of an eastern Pacific shared offshore foraging área. Mar Ecol Prog Ser, 2008; 370: 221–237.
  115. 115. Gonzalez MMB. Use of Pristis spp. (Elasmobranchii: Pristidae) by hunter-gatherers on the coast of São Paulo, Brazil. Neotrop. Ichthyol. 2005; 3: 421–426.
  116. 116. Bornatowski H. A parturition and nursery area for Carcharhinus limbatus (elasmobranchii, carcharhinidae) off the coast of Paraná, Brazil. Braz J Oceanogr, 2008; 56(4), 317–319.
  117. 117. Yokota L, Lessa RP. A nursery area for sharks and rays in Northeastern Brazil. Environ Biol Fish, 2006; 75: 349–360.
  118. 118. Musick JA. Criteria to define extinction risk in marine fishes. The American Fisheries Society initiative. Fisheries, 1999; 24(12): 6–14.
  119. 119. Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK. Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett, 2010; 13: 1055–1071. pmid:20528897
  120. 120. Ward-Paige CA, Mora C, Lotze HK, Pattengill-Semmens C, McClenachan L, Arias-Castro E, et al. Large-Scale absence of sharks on reefs in the Greater-Caribbean: A footprint of human pressures. PLoS One, 2010; 5(8): 11968.:
  121. 121. Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman D, Heithaus MR, et al. Global catches, exploitation rates, and rebuilding options for sharks. Mar Policy, 2013; 40: 194–204.
  122. 122. Sadovy Y, Eklund AM. Synopsis of biological data on the Nassau grouper, Epinephelus striatus (Bloch, 1792), and the Jewfish, E. itajara (Lichtenstein, 1822). NOAA Tech Rep NMFS, 1999; 146: 1–65.
  123. 123. Starr RM, Sala E, Ballesteros E, Zabala M. Spatial dynamics of the Nassau grouper Epinephelus striatus in a Caribbean atoll. Mar Ecol Prog Ser, 2007; 343: 239–249.
  124. 124. Morris AV, Roberts CM, Hawkins JP. The threatened status of groupers (Epinephelinae). Biodivers Conserv, 2000; 9: 919–2000.
  125. 125. Aguilar-Perera A. Disappearance of a Nassau grouper spawning aggregation off the southern Mexican Caribbean coast. Mar Ecol Prog Ser, 2006; 327: 289–296.
  126. 126. Gonzalez MMB. Tubarões e raias na pré-história do litoral de São Paulo. PhD thesis, Universidade de São Paulo, Brasil. 2005. Available: http://www.teses.usp.br/teses/disponiveis/71/71131/tde-29092006-114551/pt-br.php
  127. 127. Drew J, Philipp C, Westneat MW. Shark tooth weapons from the 19th century reflect shifting baselines in central Pacific predator assemblies. PLoS One, 2013; 8(4): 59855.:
  128. 128. Gadig OBF, Rosa RS. Occurrence of the white shark along the Brazilian coast. In: Kimley AP, Ainley DG, editors. Great white sharks: The biology of Carcharodon carcharias. Academic Press. 1998. 517 pp.
  129. 129. Mazzoleni RC, Schwingel PR. Elasmobranch species landed in Itajaí harbor, Southern Brazil. Notas Téc. FACIMAR, 1999; 3:111–118.
  130. 130. Pons M, Domingo A. Standardized CPUE of porbeagle shark (Lamna nasus) caught by the uruguayan pelagic longline fleet (1982–2008). Collect. Vol. Sci. Pap. ICCAT, 2010; 65(6): 2098–2108.
  131. 131. Salls R. To catch a fish: some limitations on prehistoric fishing in southern California with special reference to native plant fiber fishing line. J Ethnobiol, 1989; 9(2): 173–199.
  132. 132. Walker KJ. The material culture of Precolumbian fishing: artifacts and fish remains from coastal Southwest Florida. Southeast Archaeol, 2000; 19(1): 24–45
  133. 133. O’Connor S, Ono R, Clarkson C. Pelagic fishing at 42,000 years before the present and the maritime skills of modern humans. Science, 2011; 334: 111–121.
  134. 134. Erlandson JM, Rick TC, Braje TJ, Casperson M, Culleton B, Fulfrost B et al. Paleocoastal seafaring, maritime technologies and coastal foraging on California’s Channel Islands. Science, 2011; 331: 1181–1185. pmid:21385713
  135. 135. Cione AL, Bonomo M. Great white shark teeth used as pendants and possible tools by Early-Middle Holocene terrestrial mammal hunter-gatherers in the Easter Pampas (Southern South America). Int J Osteoarchaeol, 2003; 13: 222–231.