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. 2016 Jun 29;11(6):e0154476.
doi: 10.1371/journal.pone.0154476. eCollection 2016.

The Path towards Endangered Species: Prehistoric Fisheries in Southeastern Brazil

Mariana Samôr Lopes  1 , Thayse Cristina Pereira Bertucci  1 , Luciano Rapagnã  1 , Rafael de Almeida Tubino  1 , Cassiano Monteiro-Neto  1 , Acácio Ribeiro Gomes Tomas  2 , Maria Cristina Tenório  3 , Tânia Lima  3 , Rosa Souza  1 , Jorge Domingo Carrillo-Briceño  4 , Manuel Haimovici  5 , Kita Macario  6 , Carla Carvalho  6 , Orangel Aguilera Socorro  1
Affiliations

The Path towards Endangered Species: Prehistoric Fisheries in Southeastern Brazil

Mariana Samôr Lopes et al. PLoS One. .

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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Study area along the southeastern Brazilian coast showing shellmound locations.
Fig 2
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.
Fig 3
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).
Fig 4
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).
Fig 5
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.
Fig 6
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.
Fig 7
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.
Fig 8
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).
Fig 9
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.
Fig 10
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.
Fig 11
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.
Fig 12
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.
Fig 13
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.
Fig 14
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.
Fig 15
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.
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