Zooarchaeological evidence that the brown mussel ( Perna perna) is a bioinvader of coastal Brazil

Abstract

Interactions between invader species and the local biota may lead to disequilibria in regional ecosystems. For such reason, the cultivation of nonnative species may be prohibited in specific regions, as a means of protecting native species. On the other hand, the question of whether a species is a bioinvader or not may not be straightforward. This is the case of the mollusc Perna perna, presently naturalized and widely distributed along Brazilian coast, from the Bay of Vitória, in the state of Espírito Santo (ES), to the state of Rio Grande do Sul (RS). Following previous works that explored the hypothesis that P. perna invaded the coast of Brazil at the colonial period, attached to slave ships, we discuss zooarchaeological data, radiocarbon dating, and molecular genetics analyses. Out of the 578 archeological shellmounds investigated, 542 (93.8%) had no records of P. perna. From the radiocarbon dating results, it is possible to infer that the presence of the two P. perna specimens from the Saquarema shellmound, in Rio de Janeiro, as well as the other shells from the top layer, is likely related to a recent occupation of the site in the colonial period, with a great probability of being from the XVII or XVIII centuries. Data on genetic population structure of P. perna along the Brazilian coast showed higher genetic identities between the African and the Brazilian populations than among the Brazilian populations, while haplotypic diversity shows a pattern which relates to trade routes of slaves (XVII and XVIII centuries) between Africa and Brazil. These data reinforce the argument that the appearance of P. perna along the Brazilian coast is due to invasion during historical time.

Keywords

mollusc naturalized species sambaquis slave trade zooarchaeology

Introduction

The Perna perna mussel is widely distributed in tropical and subtropical regions of the Atlantic and Indian Oceans as well as in the Mediterranean (Figure 1) (Hicks et al., 2001; Siddall, 1980; Vakily, 1989). On the Atlantic coast of Africa, this mussel can be found from the Strait of Gibraltar to Namibia in the south and east of South Africa to the Red Sea and Madagascar. According to Siddall (1980), Perna picta is a synonym used for this species in the Mediterranean; in southern India and Sri Lanka, the synonym employed is Perna indica. On the Atlantic coast of the Americas, P. perna is commonly found on the rocky shores of the Gulf of Mexico. In Venezuela, its distribution extends across the northern coast of the Paria and Araya Peninsula, and it is found in Isla Margarita and Turpialito (Tejera et al., 2000). Although Silveira et al. (2006) recorded the occurrence of this species in the state of Rio Grande do Norte (RN), well-established populations along the Brazilian coast are found only from the Bay of Vitória, in the state of Espírito Santo (ES), to the state of Rio Grande do Sul (RS); from there, the distribution of this species extends through Uruguay to Maldonado, in Punta del Leste, going no further than de la Plata River (Acuna, 1977; Berry, 1978; Fernandes, 1981; Fernandes et al., 2008; Grant et al., 1992; Kensley and Penrith, 1970; Mandelli and Acuna, 1975; Rios, 1994, 2009; Schurink and Grifftiths, 1990, 1991; Shafee, 1989; Siddall, 1980; Souza et al., 2004).

Figure 1.

Geographical distribution of Perna perna.

In Africa, P. perna shells are present in large quantities in archeological deposits from 60,000 to 115,000 yr BP, the oldest date obtained for this species (Souza et al., 2004). Thus, P. perna can be considered a native species of the African continent. In Brazil, however, the archeological records of the species is scarce and/or dubious, showing evidences of present-day interference, and shells (the rarely found) dating from historical times (Souza et al. 2003). Due to that and after reviewing the literature on the 206 shellmounds, Souza et al. (2003, 2004, 2010a, 2010b, 2012) claimed that P. perna is a bioinvader and hypothesized that the species originated from Africa and have arrived in Brazil attached to the hulls of slave ships.

In a review of studies on the genetics of populations of P. perna along the Brazilian coast, Weber and Silva (2008) reported that comparisons between Brazilian populations and one population from Africa showed higher genetic identities than among Brazilian populations. The authors saw this as consistent with a continent-island model (Wright, 1978) in which, possibly, a single population from Africa was the founder of several other populations in Brazil. In the same way, a recent study of five populations along 2500 km of the Brazilian coast using mitochondrial COI gene sequences and nuclear sequence of rRNA 18 S-ITS1 found patterns of haplotypic diversity and genetic structure which seem to relate to trade routes of slaves (XVII and XVIII centuries) between Africa and Brazil (Oliveira et al., 2017). These data reinforce the argument that the appearance of P. perna along the Brazilian coast is due to invasion during historical time.

Since the studies of Souza et al. (2003), the bioinvasion hypothesis of P. perna along the Brazilian coast has been explored by several studies (Fernandes et al., 2008; Oliveira et al., 2017; Rios, 2009; Silveira et al., 2006; Souza et al., 2004, 2010a, 2010b, 2012; Weber and Silva, 2008) and contested by one (Pierri et al., 2016). Perna is a relevant income source for Brazilian families, who both fish and farm it. The hypothesis of the recent arrival of this species to the Brazilian coast was responsible for a ban on its cultivation in some states.

In order to test the bioinvasion hypotheses, we studied the content of the sambaquis (the Tupi language designation for shellmounds), found throughout the distribution range of P. perna along the Brazilian coast (578 sites), and dated some shells of P. perna.

Materials and methods

Archeological survey

The 578 archeological sites analyzed are distributed over 2000 km along the Brazilian coast from the states of Espírito Santo to Rio Grande do Sul (Figure 2; for details on midden records and depository archives, see Souza et al., 2011).

Figure 2.

Geographical location of the archeological sites analyzed along the Brazilian coast. The number of sites for each state is given in brackets and the localizations of the 578 sites is shown from the states of Espírito Santo to Rio Grande do Sul giving the number of sambaquis analyzed for each locality.

Initially, a survey of the archeological sites was made integrating the collections of nine institutions: IPHAN-21ªSR, Museu do Sambaqui da Tarioba (MST)-RJ, Museu Nacional/UFRJ, Instituto de Arqueologia Brasileira (IAB)-RJ, Museu Arqueológico de Itaipu-RJ, Museu de Arqueologia e Etnologia-UFPR, Museu Arqueológico de Sambaqui de Joinville-SC, Museu Universitário Oswaldo Rodrigues Cabral-UFSC and Museu do Homem do Sambaqui ‘Padre João Alfredo Rohr, SJ’-SC. All the malacological materials pertaining to the coastal sites of the shellmound type were analyzed.

The boxes containing archeological material were located and the material was sorted, shell matter being separated from the sediment and other faunal remains by means of a 0.5 mm sieve and/or brush. Shells were identified at the lowest possible taxonomic level (i.e. species level) based on Abbott (1974), Amaral et al. (2005), Garcia-Cubas (1981), Merlano and Hegedus (1994), Mikkelsen and Bieler (2007), and Rios (1994, 2009)

In order to find additional mentions, a survey of all publications related to shellmounds from the central–southern Brazilian coast was carried out in the libraries of the institutions where the collections were examined since they are the repository of all documents related to the shellmound there studied. This survey aimed to find malacological mentions for additional sites within the studied area lacking collections of archeological material. Excavation of four new sites were carried out (Sambaqui da Tarioba, Usiminas and Sampaio I, all of them in Rio de Janeiro; Souza et al., 2010a, 2010b). Besides excavations, in situ observations were done at four other sites with exposed layers of mollusc shells (Ilha de Cabo Frio, Novo Portinho, Sítio do Forte, and Toca do Cassununga, all of them in Rio de Janeiro; Souza et al., 2010a).

Materials of 15 of the 36 sites where P. perna was reported were located and retrieved from the technical reserves of the Museu Nacional/UFRJ, the IAB-RJ, the MST-RJ, the Museu do Homem do Sambaqui ‘Padre João Alfredo Rohr, SJ’-SC, and the Museu Universitário Oswaldo Rodrigues Cabral-UFSC. In addition, malacological material from the Sambaqui do Forte and Toca do Cassununga sites, both in Paraty (RJ), was observed in situ. Materials on the Sambaqui da Tarioba (Rio das Ostras, RJ) were retrieved from the technical reserves of the IAB-RJ and the MST-RJ and were acquired from excavations. Thus, the records of 17 of the 36 sites were checked.

Radiocarbon dating

Saquarema shellmound was the only site where P. perna shells were actually located and retrieved from the technical reserves of the Museu Nacional/UFRJ; therefore, the only two individuals belonged to the top layer (0–30 cm) samples were selected for radiocarbon analysis, as did specimens of Anomalocardia brasiliana and Stramonita haemastoma. We chose to collect not only the two specimens of interest but also other species from the same layer as well as specimens of Iphigenia brasiliana and Lucina pectinata from 30 to 60 cm. Samples were prepared and analyzed at the Physics Institute of the Universidade Federal Fluminense at the Radiocarbon Laboratory (LAC-UFF). Calibration was performed with OxCal software v4.2.4 (Bronk Ramsey, 2009) using the Marine13 calibration curve (Macario et al., 2013; Reimer et al., 2013) with an offset of −140 ± 66 ¹⁴C yr (Alves et al., 2015a) to account for local corrections.

Details on sites excavated, observed in situ as well as the specimen used for radiocarbon dating are presented in Figure 3. Figure 3 also presents details on the stratigraphy of the Sambaqui de Saquarema as described by Kneip (2001) just before being completely destroyed by the urbanization process.

Figure 3.

Details on archeological sites, Perna perna shells and a diagram of stratigraphy. (a) Tarioba shellmound showing the five archeological stratigraphic layers marked with strings. (b) Usiminas shellmound where can be seen three archeological stratigraphic layers evident by their different colors. (c) Exposed layers of mollusc shells from Usiminas shellmound. (d) Modern shells of the species P. perna. (e) The specimen of P. perna used for radiocarbon dating (in the pack is labeled from top to bottom: the name of the species, archeological layer, depth, and shellmound name). (f) Diagram showing details on the stratigraphy of the Sambaqui de Saquarema as described by Lina Kneip, the archeologist who studied the site during the 1960s (Modified from Kneip, 2001). Photos from the authors.

Results

Archeological sites

Out of the 578 archeological sites investigated, 542 (93.8%) had no records of P. perna. The presence of this species was recorded for 36 sites (6.2%), 29 of which were in the state of Rio de Janeiro (RJ), 1 in the state of São Paulo (SP), 5 in Santa Catarina (SC), and 1 in Rio Grande do Sul (RS). Table 1 summarizes these results, which are described as follows.

Table 1.

Archeological sites for which Perna perna is cited.

Name of the site	FU	Conservation state	Origin of data	Presence of Perna perna	References
Sítio do Meio	RJ	D	B	–	I, II
Sambaqui da Vila Nova	RJ	D	B	–	I
Sambaqui do Ury	RJ	D	B	–	I
Sambaqui de Sernambetiba	RJ	D	T (MN)	1	I, III
Sambaqui do Amourins	RJ	D	T (MN)	0	I, IV
Sambaqui do Arapuan	RJ	D	T (MN)	0	I
Sambaqui do Cordovil	RJ	D	B	–	I
Sambaqui do Fernando	RJ	D	B	–	I
Sambaqui do Guapi	RJ	D	B	–	I
Sambaqui do Imenezes	RJ	D	T (MN)	0	I
Sambaqui do Rio das Pedrinhas	RJ	D	T (MN)	0	I
Sítio Saracuruna	RJ	D	B	–	I
Abrigo Paratimirim I	RJ	D	B	–	I
Abrigo Ponta do Leste II	RJ	D	B	–	I
Sambaqui do Araújo	RJ	D	T (MN)	1	V
Sambaqui do Forte	RJ	D	O	0	I, VI
Sambaqui do Pouso	RJ	D	B	–	I
Sambaqui Mamanguá	RJ	D	B	–	I
Sítio Ilha Comprida II	RJ	D	B	–	I
Toca do Cassununga (Sítio Jabaquara)	RJ	D	O	0	I
Sítio Trindade I (Sambaqui do Severo)	RJ	D	B	–	I
Sítio Trindade II	RJ	D	B	–	I
Sítio Trindade III (Sambaqui da Trindade)	RJ	D	B	–	I
Sambaqui da Tarioba	RJ	D	E (IAB/MST)	0	I
Sítio Botafogo (Corondó)	RJ	D	T (IAB)	0	I, VII
Sambaqui de Saquarema	RJ	D	T (MN)	1	I, VIII
Sambaqui do Moa	RJ	D	T (MN)	0	I, VIII
Sambaqui Manitiba I	RJ	P	T (MN)	0	I, VI, VIII
Sambaqui Yatch Club	RJ	D	T (MN)	0	I, VIII
Mar Virado	SP	D	B	–	IX
Pântano do Sul	SC	D	T (MHS)	0	X, XI
Ponta das Almas	SC	D	B	–	XII, XIII, XIV
Rio do Meio	SC	D	T (MU-UFSC)	1	XV, XVI
Enseada I	SC	D	T (MU-UFSC)	0	XIV, XVII
Congonhas I	SC	D	B	–	XIV
Capão D’Areia	RS	P	B	–	XVIII

FU: federation unit; RJ: Rio de Janeiro; SP: São Paulo; SC: Santa Catarina; RS: Rio Grande do Sul; D: destroyed; P: preserved; B: bibliographic; T: triad; MN: Museu Nacional; IAB: Instituto de Arqueologia Brasileira; MST: Museu do Sambaqui da Tarioba-RJ; MHS: Museu do Homem do Sambaqui ‘Padre João Alfredo Rohr, SJ’-SC; MU-UFSC: Museu Universitário Oswaldo Rodrigues Cabral/UFSC; O: Observed; E: Excavated; 0: absent; 1: present; - - not checked; I – Mendonça de Souza (1981); II – Gaspar (1991); III – Beltrão et al. (1981); IV – Heredia et al. (1981); V – www.iphan.gov.br; VI – Beltrão et al. (1978); VII – Carvalho (1984); VIII – Kneip (2001); IX – Nishida (2001); X – Rohr (1977); XI – Schmitz and Bitencourt (1995); XII – Piazza (1966); XIII – Neves (1988); XIV – Beck (2007); XV – Coutinho (1999); XVI – Fossari (2004); XVII – Tiburtius (1996); XVIII – Silva et al. (2000).

Valves of P. perna were only found in the Araújo (Paraty, RJ), Saquarema (Saquarema, RJ), Sernambetiba (Magé, RJ), and Rio do Meio (Florianópolis, SC) sambaquis. The Sambaqui do Araújo is located in an area of great anthropogenic interference, with banana plantations, houses, and a cemented path. This Sambaqui is formed by black earth with molluscs, fish bones, human bones, and fire pits (www.iphan.gov.br). From the malacological evidence analyzed, three valves of P. perna were found complete.

In the case of the Sernambetiba site, the two valves of P. perna found were well preserved, which is evidence of a recent shell. Surely, this constitutes a good example of contamination of the archeological record as, at the time of excavation, the site was in extremely poor condition due to agriculture, opening of new roads, earthwork, land division, sand mining, construction work, and the installation of transmission towers for a power company (Mendonça de Souza, 1981).

The P. perna valves found at the Rio do Meio site were packed in bags from ‘Level 1’, that is, the surface layer. The same shell packages contained plastic seals from cigarette packs, fragments of nylon ropes, bottle caps, broken glass, and assorted plastics. No record of this species was found in the materials referring to lower layers. This site was used to dump waste and suffered the intervention of earthworks carried out prior to the excavation. After the collection, the site was covered (Fossari, 2004).

Records could not be checked for 19 sites, of which the technical reserves of 16 could not be located, preventing the sorting of their malacological material. However, the Cordovil, Fernando, Guapi, and Sítio Saracuruna sambaquis, all located in the municipality of Magé-RJ, showed an advanced state of destruction at the time of the survey due to agriculture, opening of new roads, earthworks and land division, indicating contamination of the archeological record (Mendonça de Souza, 1981). Likewise, the Sambaqui Ury (Macaé-RJ) and the Sambaqui da Vila Nova (Casimiro de Abreu-RJ) suffered anthropogenic erosion in 1969 and are currently in poor condition (Mendonça de Souza, 1981). The eight sites in Paraty (Paratimirim I, Ponta do Leste II, Pouso, Mamanguá, Ilha Comprida II, Trindade I and II and Sítio Trindade III) have also suffered some type of anthropogenic erosion, such as construction activity, landfills, depredation, and land division.

When studied, the Ponta das Almas site (Florianopolis, SC), located on the rocky jetty known as Ponta das Almas showed evidence of destruction from agriculture and construction activities. Beck (2007) reported ‘… lenses with fragmented shells of Mytilus perna (clams). This latter species also occurs in abundance in the area, including on the rocky shore where the sambaqui is located’. The Sambaqui de Congonhas I (Tubarão, SC) has also suffered intense destruction over the course of many years because of a ‘caieira’ (a particular type of kiln used for calcining lime) next to the site. Beck (2007) reported that at this site ‘… predominated, largely, the species … and M. perna (clams). These species whose shells were found in larger quantities are those that, at present, can still be found on the beaches, river mouths, and rocky shores of the South Coast’. In both cases, the researcher seemingly attempted to associate the malacological material from the site to a taxonomic group present and abundant now.

Although the archeological material from Sítio do Meio (Cabo Frio-RJ) is deposited at the Casa de Pedra (Museu Nacional/UFRJ), it could not be analyzed because the technical reserve was under renovation and the material could not be accessed. Although Gaspar (1991) recorded the presence of P. perna at this site, which is currently in an area of environmental preservation, the site experiences anthropogenic interference because the area is targeted by tourists and city residents for picnicking and collecting mussels from the adjacent rocky shores. In the neighboring sites, Boca da Barra and Salinas Peroano, P. perna mussels were not found.

The Mar Virado site (Ubatuba-SP), as explained by Nishida (2001), underwent an intense occupation by the Caiçara people (a traditional ethnic group of the Brazilian coast) until the 1960s, which resulted in great disturbance to the stratigraphy of the site. The valves of P. perna found in the samples were from a recent period, as a cottier was living on the island and vestiges of that occupant were found on the surface of the site.

At the Capão D’Areia sambaqui (São José do Norte-RS), P. perna shells were found in the upper stratigraphic levels (Silva et al., 2000) and the valves were whole and well preserved showing signs of recent deposition (Flavio Callipo of the Museu de Arqueologia e Etnologia da Universidade de São Paulo – MAE-USP, personal communication).

The Sambaqui de Saquarema used to be located in an urban area of the city of Saquarema-RJ, next to the hill where the Igreja de Nossa Senhora de Nazaré (22°56′05′ S, 42°29′33′ W) is located. In 1932, this site was considered destroyed, and part of the material was distributed among unidentified private individuals (Beltrão et al., 1978; Mendonça de Souza, 1981). Nevertheless, in the 1960s, a team led by archeologist Dr Lina Kneip conducted an excavation that recovered polished axe blades, pitted anvil stones, quartz chips, fish and mammal bones, human bones, dye, shells, scrapers, and adornments made with the bivalve Lucina pectinata (Kneip, 2001; Mendonça de Souza, 1981). Many excavated materials in the technical reserves of the National Museum of Rio de Janeiro were analyzed. Two partially fragmented valves of P. perna were found in the upper levels, between 0 and 30 cm of excavation sector E. These valves and the other shells recovered with them, as well as samples from other stratigraphic layers, were identified and dated along with the other species recovered.

Radiocarbon dating

The results for the ¹⁴C dates obtained from the marine molluscs collected at the Saquarema shellmound are presented in Figure 4 and Table 2. From the results from 30 to 60 cm and those from the top layer (0–30 cm) it is possible to infer that the top layer is related to a reoccupation of the site, possibly after the arrival of the Europeans in AD 1500 years. The archeological occupation period agrees with the results of Alves et al. (2015a).

Figure 4.

Conventional (non-calibrated) radiocarbon dates of marine molluscs from the Saquarema shellmound.

Table 2.

Conventional (non-calibrated) and calibrated radiocarbon dates, mollusc species and depth within the Saquarema shellmound (LAC-UFF ID stands for the standard labeling of the material given by The Radiocarbon Laboratory fro Universidade Federal Fluminense-LAC-UFF. This identification permits the specific result to be checked by independent researchers).

Species	LAC-UFF ID	Depth (cm)	¹⁴C age (yr BP)	Cal BP from (95.4%)	Cal BP to (95.4%)
Anomalocardia brasiliana	150386	0–30	747 ± 61	642	325
Anomalocardia brasiliana	150387	0–30	631 ± 83	606	149
Anomalocardia brasiliana	150388	0–30	543 ± 64	498	109
Perna perna	150389	0–30	559 ± 51	492	145
Stramonita haemastoma	150390	20–30	415 ± 58	360	Modern
Stramonita haemastoma	150391	20–30	356 ± 75	304	Modern
Perna perna	150392	20–30	477 ± 34	429	Modern
Lucina pectinata	150393	40–50	3929 ± 39	4344	3886
Lucina pectinata	150394	40–50	3873 ± 40	4259	3816
Lucina pectinata	150395	40–50	3895 ± 39	4284	3837
Lucina pectinata	150396	50–60	3903 ± 40	4296	3842
Lucina pectinata	150397	50–60	3889 ± 42	4280	3830
Lucina pectinata	150398	50–60	4125 ± 48	4649	4150
Lucina pectinata	150399	70–80	3996 ± 41	4410	3973
Lucina pectinata	150400	70–80	3847 ± 43	4229	3772
Lucina pectinata	150401	70–80	3960 ± 41	4384	3930
Iphigenia brasiliana	150402	70–80	4050 ± 47	4505	4049
Iphigenia brasiliana	150403	80–90	3997 ± 43	4412	3971
Iphigenia brasiliana	150404	80–90	3745 ± 45	4077	3634
Lucina pectinata	150405	80–90	4023 ± 42	4435	3990
Lucina pectinata	150406	80–90	3967 ± 42	4394	3941
Lucina pectinata	150407	80–90	3806 ± 41	4151	3705
Lucina pectinata	150408	90–100	4023 ± 42	4435	3990
Lucina pectinata	150409	90–100	3856 ± 42	4241	3791
Lucina pectinata	150410	90–100	4168 ± 40	4685	4205
Iphigenia brasiliana	150411	90–100	4031 ± 42	4448	3999

For the Saquarema shellmound, individual calibration of each of the ¹⁴C dates is presented in Table 2. Based on such results, the archeological occupation may have lasted from 4.6 to 3.7 ka cal. BP. Probability distributions for samples from the top layer are presented in Figure 5. All such results reinforce the hypothesis of bioinvasion.

Figure 5.

Probability distributions of calibrated dates for the top 30 cm of Saquarema shellmound.

Discussion

Absence of P. perna in Pre-Columbian Times

The absence of a specific organism from the archeological record does not necessarily mean that this species was absent in the environment (Lyman, 1995). People may avoid a particular animal for various reasons, and the possibility that this species was not identified in the archeological remains must be considered. Assumptions that currently relevant resources were also relevant in the past should be avoided. The absence can also indicate that people at that particular time considered the species a taboo food, thus avoiding it (Lima, 1984; Reitz and Wing, 2008). However, the number of sites analyzed in this study is considerable, covering more than 2000 km of coastline, and the persistence of a food taboo across such a large geographic area and among so many different human groups is unlikely.

Another consideration is that most sites suffered multiple occupations at different periods. Hence, a variation of hundreds of years might exist between the layers of a single site and thousands of years among the various sites studied. Consequently, if this species was present in the environment at the time these sites were being constructed, at some point, the species should have been captured for use as construction material or even by chance.

A possible argument for methodological problems that could have led to the failure to identify this species in the studied archeological remains is that the shells of P. perna could degrade easily and therefore not be preserved in the archeological record. However, other species of Mytilidae that had a structure, shape, and chemical composition very similar to that of P. perna shells were recovered in the malacological content at most of the investigated sites. Complete shells of the bivalves Atrina seminuda, Cyrtopleura costata, and Pholas campechiensis, much more fragile than P. perna, can be found in the archeological record. Thus, it seems clear that this argument does not hold.

At this point, based on the results, records of the species P. perna cannot be confirmed. Therefore, this species can be considered absent in the pre-Columbian time of the Brazilian coast and thus may be considered a bioinvader. This conclusion corroborates the hypothesis of Lima et al. (1986), Souza et al. (2003), and Weber and Silva (2008).

Perna perna and its bioinvader history

In the Gulf of Cariaco, Venezuela, the species was introduced in the 1960s while being commercially farmed. Currently, along the north-eastern coast of Venezuela, P. perna is a commercially relevant bivalve (Jory et al., 2000). In the Gulf of Mexico, bioinvasion by this species began in 1990 in Port Aransas, Texas (Hicks and Tunnell, 1993), where the species was likely introduced by hull fouling of Venezuelan ships and in ballast water. The species is already distributed throughout the Gulf of Mexico (Hicks and Mcmahon, 2002; Hicks and Tunnell, 1995; Holland, 1997; Holland et al., 1999; Magee, 1997).

How did the invasion process of P. perna in Brazil occur? Souza et al. (2003) explained considered the presence of this species in African historical and archeological records, and speculated that the species although native to Africa, probably invaded the Brazilian coast at the time of the slave trade, by attaching to ship hulls. The route followed by slave ships is shown in Figure 6 based on Alencastro (2000), Borucki et al. (2015), and Eltis and Halbert (2008). In the 15th, 16th, and 17th centuries, the ships departed from the region of Senegal and Gambia and docked in north-eastern Brazil. Neither the origins nor the destinations coincide with the distribution of P. perna. Starting in the 18th century, ships came from the region of the Congo, Angola, Mozambique, and Tanzania, places where the presence of P. perna has been recorded, and docked in the states of Bahia (BA) and Rio de Janeiro. In the years of prohibition of the slavery trade, the exchange of Africans for silver was made through Rio de Janeiro. A ‘caravelão’ (a smaller caravel, which is a small, fast Spanish or Portuguese sailing ship of the 15th–17th centuries) connected the two ports in a journey of 10–15 days of navigation. On the way back, the ships brought ‘patacas’ (Portuguese for ‘pieces of eight’), silver and gold. This trade was intensified in the 19th century, when approximately 1,927,576 slaves were transported to Brazil. As slave ships were able to carry an average of 335 slaves per journey, in the period between AD 1514 and 1866 when the abolition of slavery was taking place, ships docked in Brazilian ports approximately 12 thousand times over the course of three centuries to sell approximately four million slaves (Alencastro, 2000; Borucki et al., 2015; Eltis and Halbert, 2008).

Figure 6.

The slavery routes from Africa to Brazil. The arrows indicate slave trade routes (a) from 15th to 17th centuries and (b) from 18th and 19th centuries (Alencastro, 2000; Borucki et al., 2015; Eltis and Halbert, 2008).

Souza et al. (2003) also reported that this information agrees with Ihering’s (1897, 1900) observations on the occurrence of P. perna in Rio de Janeiro and highlights the expansion of the species toward Santa Catarina. Later, P. perna was reported by Klappenbach (1965) in the state of Rio Grande do Sul and in Uruguay. Indeed, this information not only supports this first form of globalization but also strengthens the bioinvasion hypothesis.

Other interesting data recorded by Souza et al. (2003) are the observation that Phaulopsis imbricata was abundant in the sambaquis where it occurred (12.1%) and rare in adjacent rocky shores, what could indicate that this bivalve was found in greater quantities in pre-Columbian times than in current times. That associated with the decrease in the abundance of Perna due to the introduction of Isognomon bicolor (a bivalve mollusc that arrived in Brazil in the 1990s from the Caribbean via ballast water and fouling) suggested an evolutionary scenario of these species in the rocky shores along the Brazilian coast. Thus, after its arrival, the invasive species P. perna began to replace a native species, the pearl oyster P. imbricata, on the Brazilian rocky shores. This ingenious scenario is supported by a similar event that occurred in Venezuela in historical times. As mentioned earlier, the farming of P. perna in 1960 (Jory et al., 2000) depleted the natural banks of P. imbricata (Martinez, 1971).

A common feature of the hypotheses presented for the current geographic distribution of Perna canaliculus and P. perna is the presence of at least one long-distance dispersal event. In the case of P. canaliculus, the arrival of this organism in New Zealand from South Africa would take approximately 1 year (assuming a west drift wind with a speed of 1 km/h and a distance of at least 8000 km to overcome). In the case of P. perna, its arrival in South America from Africa would take approximately 6 months (a distance of at least 4000 km, in this case). Although Perna has a long pelagic larval phase (varying between 2 and 4 weeks) and is able to delay its settlement for several weeks in the absence of a suitable substrate, travel for more than 1000 km in this manner seems unlikely. Therefore, an alternative explanation for larval dispersal would be dispersal mediated by drifting materials (macroalgae, wood, etc.) by juveniles and adults. The low genetic divergence between geographic populations of P. perna from Africa and South America inferred from mitochondrial DNA (COI) sequences points to a recent dispersal, occurring between 0.17 and 0.57 Ma (Wood et al., 2007).

Thus, the arrival of P. perna mussels in the Brazilian coast would have occurred in historic times, just over 400 years ago, and the vector, as suggested by Wood et al. (2007), would have been hull fouling, in this case, of slave ships. Therefore, this study offers further evidence that the arrival of P. perna in South America was not by larval dispersal but by fouling. However, time estimates of when this happened differ between older (0.17 and 00.57 Ma; Wood et al., 2007) and later times (400 years; Souza et al., 2003).

In a recent study, Pierri et al. (2016) used molecular data and ¹⁴C dating as evidence that the species was native to Brazil, but the results of that study cannot be considered conclusive. The molecular data were obtained by sequencing the mitochondrial DNA (cytochrome oxidase subunit I gene – COI) of 10 specimens of P. perna mussels obtained from an experimental farm located in the city of Florianópolis, Santa Catarina (SC), Brazil (Pierri et al., 2016). The sequences generated were analyzed together with sequences obtained from GenBank for other regions (Africa and Venezuela) where the species is distributed. Sequences of Mytilus edulis, Mytilus galloprovincialis, and Aulacomya atra maoriana were used as outgroups. The results pointed to divergence occurring between the Brazilian and African populations at approximately 0.2 Ma (million years ago). However, in the same study, divergence times for populations with extensive gene flow (the two populations sampled in Santa Catarina) were as great as 1400 years.

Pierri et al. (2016) conducted a survey of the archeological material deposited at the technical reserve of the Museu de Arqueologia e Etnologia Oswaldo Rodrigues Cabral – MArquE of Universidade Federal de Santa Catarina – UFSC and collected fragments and shells of P. perna at the archeological site Rio do Meio in north-western Florianópolis. The samples were analyzed by Beta Analytic Inc. (Miami, USA) using accelerator mass spectrometry (AMS) ¹⁴C dating. Dating of the shells showed ages between 720 ± 30 and 780 ± 30 yr BP which Pierri et al. (2016) claim to be prior to the arrival of Europeans in Brazil. However, these results are expressed in conventional radiocarbon ages and need to be calibrated. Applying the marine calibration curve Marine13 (Reimer et al., 2013) and the recommended value for the local offset ΔR = 22 ± 62 ¹⁴C yr (Alves et al., 2015b), the calibrated results for such dates are AD 1448–1675 years (95.4%) for Rio do Meio I and AD 1462–1801 years (95.4%) for Rio do Meio II, most likely to be from the period post colonization, contrary to the conclusions reached by Pierri et al. (2016). The probability distributions are presented in Figure 7.

Figure 7.

Probability distributions for calibrated dates of Perna perna samples from Rio do Meio (Pierri et al., 2016).

The aquaculture in Brazil is mainly based on the cultivation of the brown mussel. However, as a bioinvader, its cultivation has been banned in some parts of the country based on rules from Ministry of Aquiculture and Fisheries in Brasil (SEAP, 2005). However, the possible invasion of the species along the Brazilian shores is dated from the colonial times. Therefore, the species can be considered naturalized along the Brazilian shores, what means that any impact of the species on the native fauna is not anymore present and the species cause no ecological impact whatsoever. Unfortunately, these considerations were not so far taken in consideration by Brazilian authorities or legislation.

In conclusion, the results described herein confirm the scenario proposed by Souza et al. (2003, 2004, 2010a, 2010b, 2012) in their studies. Furthermore, in what concerns the radiocarbon dating of the very few specimens of P. perna found so far within an archeological context, on one hand, it is not possible to prove the inexistence of such species in the pre-colonial period, and on the other hand, all the evidence from the present work supports the hypothesis of bioinvasion. Nonetheless, the species is already naturalized along Brazilian shores, which should prevent any restriction to its use in aquaculture initiatives.

Footnotes

Funding

This work was supported by financial agencies CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, 307771/2017-2 and INCT-FNA, 464898/2014-5), FAPERJ (Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro, E-26/110.138/2014 and E26/203.019/2016), and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, 23038.007340/2011-09). MRD and RCCLS were supported by CAPES’ Post-doctoral Scholarships (Programa Nacional de Pos-Doutorado-PNPD).

ORCID iD

Kita D Macario

References

Abbott

(1974) American Seashells. New York: Van Nostrand Reinhold Co.

Acuna

(1977) Crecimento y idice de engorda del mejillon Perna perna (L.) cultivado en el Golfo de Cariaco, Venezuela. FAO Fisheries Reports 200: 1–9.

Alencastro

(2000) O trato dos viventes: formação do Brasil no Atlântico Sul - Séculos XVI e XVII. São Paulo: Companhia das Letras.

Alves

Macario

Souza

RCCL

, et al. (2015a) Marine reservoir corrections on the Southeastern Coast of Brazil: Paired samples from the Saquarema shellmound. Radiocarbon 57: 517–525.

Alves

Macario

Souza

RCCL

, et al. (2015b) Radiocarbon reservoir corrections on the Brazilian coast from pre-bomb marine shells. Quaternary Geochronology 29: 30–35.

Amaral

ACZ

Rizzo

Arruda

(2005) Manual de identificação dos invertebrados marinhos da região sudeste-sul do Brasil. São Paulo: Editora da Universidade de São Paulo.

Beck

(2007) A variação do conteúdo cultural dos sambaquis do litoral de Santa Catarina. Rio de Janeiro: Sociedade de Arqueologia Brasileira.

Beltrão

Heredia

Neme

SMN

, et al. (1978) Coletores de moluscos litorâneos e sua adaptação ambiental: O sambaqui de Sernambetiba. Arquivos do Museu de História Natural 3: 97–115.

Beltrão

Heredia

Rabello

AMC

, et al. (1981) Pesquisas arqueológicas no sambaqui de Sernambetiba. Arquivos do Museu de História Natural 6–7: 145–155.

10.

Berry

(1978) Reproduction, growth, and production in the mussel Perna perna, on the East Coast of South Africa. Investigational Reports of Oceanography Research Institute 48: 1–28.

11.

Borucki

Eltis

Wheat

(2015) Atlantic history and the slave trade to Spanish America. American Historical Review 120: 433–461.

12.

Bronk Ramsey

(2009) Bayesian analysis of radiocarbon dates. Radiocarbon 51: 337–360.

13.

Carvalho

(1984) Estudo arqueológico do Sítio Corondó. Boletim Série Monografias, Instituto de Arqueologia Brasileira 2: 1–243.

14.

Coutinho

(1999) Identificação e biometria dos restos conchíferos presentes no sítio arqueológico do Rio Do Meio, Ilha de Santa Catarina, SC (Monograph). Florianópolis: Universidade Federal de Santa Catarina.

15.

Eltis

Halbert

(2008) Voyages: Trans-Atlantic slave trade database. Available at: http://slavevoyages.org (accessed 19 April 2017).

16.

Fernandes

FCR

(1981). Aspectos biológicos e ecológicos do mexilhão Perna perna (Linneaus, 1758) da região de Cabo Frio/RJ – Brasil. PhD Thesis, Universidade de São Paulo.

17.

Fernandes

FCR

Souza

CCL

Junqueira

AOR

, et al. (2008) Distribuição mundial e o impacto de sua introdução no Brasil. In: Resgalla

C Jr

Weber

Conceição

(eds) O mexilhão Perna perna (L.): Biologia, Ecologia e Aplicações. Rio de Janeiro: Editora Interciência, pp. 25–30.

18.

Fossari

(2004) A população pré-colonial jê na paisagem da Ilha de Santa Catarina. PhD Thesis, Universidade Federal de Santa Catarina.

19.

Garcia-Cubas

(1981) Moluscos de un sistema lagunar tropical en el sur del golfo de México (Laguna de Términos, Campeche) ( Publicaciones Especiales). Mexico City: Instituto De Ciências Del Mar Y Limnologia, Universidad Nacional Autônoma De México, vol. 5, pp. 1–209.

20.

Gaspar

(1991) Aspectos da organização social de um grupo de pescadores, coletores e caçadores que ocupou o litoral do Estado do Rio de Janeiro. PhD Thesis, Universidade de São Paulo.

21.

Grant

Schneider

Leslie

, et al. (1992) Population genetics of the brown mussel Perna perna in Southern Africa. Journal of Experimental Marine Biology and Ecology 165: 45–58.

22.

Heredia

Beltrão

Oliveira

MDG

, et al. (1981) Pesquisas arqueológicas no sambaqui de Amourins, Magé, RJ. Arquivos do Museu de História Natural 6/7: 175–188.

23.

Hicks

Mcmahon

(2002) Respiratory responses to temperature and hypoxia in the nonindigenous brown mussel Perna perna (Bivalvia: Mytilidae), from Gulf of Mexico. Journal of Experimental Marine Biology and Ecology 277: 61–78.

24.

Hicks

Tunnell

(1993) Invasion of the south Texas coast by the edible brown mussel Perna perna (Linnaeus 1758). Veliger 36: 92–97.

25.

Hicks

Tunnell

(1995) Ecological notes and patterns of dispersal in the recently introduced mussel, Perna perna (Linnaeus, 1758), in the Gulf of Mexico. American Malacological Bulletin 11: 203–206.

26.

Hicks

Tunnell

Mcmahon

(2001) Population dynamics of the nonindigenous brown mussel Perna perna in Gulf of Mexico compared to other world-wide populations. Marine Ecology Progress Series 211: 181–192.

27.

Holland

(1997) Field notes on the southward dispersal of the exotic brown mussel Perna perna, in the Western Gulf of Mexico. Texas Conchologist 34: 1–9.

28.

Holland

Gallagher

Hicks

, et al. (1999) Cytotaxonomic verification of a non-indigenous marine mussel in the Gulf of Mexico. Veliger 42: 281–282.

29.

Ihering

(1897) Os molluscos marinos do Brazil. Revista do Museu Paulista 2: 73–113.

30.

Ihering

(1900) On the South American species of Mytilidae. Proceedings of Malacological Society 4: 84–98.

31.

Jory

Cabrera

Polanco

, et al. (2000) Aquaculture in Venezuela: Perspectives. Aquaculture Magazine 25: 1–5.

32.

Kensley

Penrith

(1970) New records of Mytilidae from the northern South West African coast. Annual South African Museum 57: 15–24.

33.

Klappenbach

(1965) Lista preliminar de los Mytilidae brasileños com claves para su determinación y notas sobre su distribución. Anais da Academia Brasileira de Ciências 37: 327–352.

34.

Kneip

(2001) O Sambaqui de Manitiba I e outros sambaquis de Saquarema, RJ (Documento de Trabalho, Série Arqueologia). Rio de Janeiro: Museu Nacional – UFRJ, vol. 5, pp. 1–91.

35.

Lima

(1984) Zooarqueologia: Alguns resultados para a pré-história da Ilha de Santana. Revista de Arqueologia 2: 10–40.

36.

Lima

Mello

BEM

Silva

RCP

(1986) Analysis of molluscan remains from the Ilha de Santana site, Macaé, Brazil. Journal of Field Archaeology 13: 83–97.

37.

Lyman

(1995) Determining when rare (zoo-)archaeological phenomena are truly absent. Journal of Archeological Method and Theory 2: 369–424.

38.

Macario

Gomes

PRS

Anjos

, et al. (2013) The Brazilian AMS Radiocarbon Laboratory (LAC-UFF) and the intercomparison of results with CENA and UGAMS. Radiocarbon 55: 325–330.

39.

Magee

(1997) Mussels throwing painless punches at the Texas coast-so far. Bays Foundation News 3: 1–7.

40.

Mandelli

Acuna

(1975) The culture of the mussel Perna perna and the mangrove oyster Crassostrea rhizophorae in Venezuela. Marine Fisheries Review 37: 15–18.

41.

Martinez

(1971) Estado atual de la biologia y cultivos de moluscos comestibles en Venezuela. FAO Fisheries Reports 71: 173–181.

42.

Mendonça

Souza

(1981) Pré-história Fluminense. Rio de Janeiro: Instituto Estadual do Patrimônio Cultural.

43.

Merlano

JMD

Hegedus

(1994) Moluscos Del caribe colombiano (Um catálogo ilustrado). Santafé de Bogotá: Colciencias; Fundación Natura; Invemar.

44.

Mikkelsen

Bieler

(2007) Seashells of Southern Florida: Living Marine Bivalves of the Florida Keys and Adjacent Regions. Princeton, NJ: Princeton University Press.

45.

Neves

(1988) Paleogenética dos grupos pré-históricos do litoral sul do Brasil (Paraná e Santa Catarina) ( Pesquisas - Série Antropologia). São Leopoldo: Instituto Anchietano De Pesquisas, vol. 43, pp. 1–178.

46.

Nishida

(2001) Estudo zooarqueológico do Sítio Mar Virado, Ubatuba, SP. MSc Dissertation, Universidade de São Paulo.

47.

Oliveira

MJS

Beasley

Barros

NGV

, et al. (2017) Two African origins of naturalized brown mussel (Perna perna) in Brazil: Past and present bioinvasions. Hydrobiologia 794: 59–72.

48.

Piazza

(1966) Estudos de sambaquis (Nota Prévia) (Série Arqueologia). Florianópolis: Instituto de Antropologia, Universidade Federal de Santa Catarina, vol. 2, pp. 1–72.

49.

Pierri

Fossari

Magalhães

ARM

(2016) O mexilhão Perna perna no Brasil: Nativo ou exótico? Arquivo Brasileiro de Medicina Veterinária e Zootecnia 68: 404–414.

50.

Reimer

Bard

Bayliss

, et al. (2013) IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55: 1869–1887.

51.

Reitz

Wing

(2008) Zooarchaeology. Cambridge: Cambridge University Press.

52.

Rios

(1994) Seashells of Brazil. Rio Grande: Fundação Universidade Federal Rio Grande.

53.

Rios

(2009) Compendium of Brazilian Sea Shells. Rio Grande: Editora Evangraf.

54.

Rohr

(1977) O sítio arqueológico pântano do Sul SC-F-10. Florianópolis: Imprensa Oficial do Estado de Santa Catarina.

55.

Schmitz

Bitencourt

ALV

(1995) O sítio arqueológico Pântano do Sul, SC. Pesquisas – Série Antropologia, Instituto Anchietano de Pesquisas 52: 77–123.

56.

Schurink

Griffiths

(1990) Marine mussels of southern Africa: Their distribution patterns, standing stocks, exploitation, and culture. Journal of Shellfish Research 9: 75–85.

57.

Schurink

Griffiths

(1991) A comparison of reproductive cycles and reproductive output in four southern African mussel species. Marine Ecology Progress Series 76: 123–134.

58.

SEAP (2005) Instrução normativa SEAP n° 17, de 22 de setembro de 2005. Dispõe sobre critérios e procedimentos para formulação e aprovação de Planos Locais de Desenvolvimento da Maricultura - PLDMs. Available at: http://www.icmbio.gov.br/cepsul/images/stories/legislacao/Instrucao_normativa/2005/in_seap_17_2005_criterios_pldm_parques_aquicolas_altrd_in_seap_9_2006_15_2006_11_2008.pdf (accessed 11 July 2018).

59.

Shafee

(1989) Reproduction of Perna picta (Mollusca: Bivalvia) from the Atlantic coast of Morocco. Marine Ecology Progress Series 53: 235–245.

60.

Siddall

(1980) A clarification of genus Perna (Mytilidae). Bulletin of Marine Science 30: 858–870.

61.

Silva

Calippo

Ribeiro

PAM

(2000) A fauna Molusca do sambaqui RS-LC:59 - Capão D’Areia. Resumos, XIII Semana Nacional de Oceanografia, pp. 115–116.

62.

Silveira

Souza

RCCL

Fernandes

, et al. (2006) Occurrence of Perna perna, Modiolus carvalhoi (Mollusca, Bivalvia, Mytilidae) and Megabalanus coccopoma (Crustacea, Cirripedia) off Areia Branca, Rio Grande do Norte state, Brazil. Biociências 14: 89–90.

63.

Souza

RCCL

Fernandes

Silva

(2003) A study on the occurrence of the brown mussel Perna perna on the sambaquis of the Brazilian coast. Revista do Museu de Arqueologia e Etnologia da USP 13: 3–24.

64.

Souza

RCCL

Fernandes

Silva

(2004) Distribuição atual do mexilhão Perna perna no mundo: Um caso recente de bioinvasão. In: Silva

JSV

Souza

RCCL

(eds) Água de Lastro e Bioinvasão. Rio de Janeiro: Editora Interciência, pp. 157–172.

65.

Souza

RCCL

Lima

Silva

(2010a) Holocene molluscs from Rio de Janeiro state coast, Brazil. Check List 6: 301–308.

66.

Souza

RCCL

Lima

Silva

(2011) Conchas Marinhas de Sambaquis do Brasil. Rio de Janeiro: Technical Books Editora.

67.

Souza

RCCL

Lima

Silva

(2012) Remarks on the biodiversity of marine molluscs from late-Holocene Brazilian shell mounds. In: Lefèvre

(ed.) Proceedings of the General Session of the 11th International Council for Archaeozoology Conference. Oxford: Archaeopress, pp. 245–256.

68.

Souza

RCCL

Trindade

Decco

, et al. (2010b) Archaeozoology of marine mollusks from Sambaqui da Tarioba, Rio das Ostras, Rio de Janeiro, Brazil. Zoologia 27: 363–371.

69.

Tejera

Oñate

Nuñez

, et al. (2000) Crecimiento inicial del mejillón Marrón (Perna perna) y verde (Perna viridis) bajo condiciones de cultivo suspendido en el Golfo de Cariaco, Venezuela. Boletín del Centro de Investigaciones Biológicas 34: 81–304.

70.

Tiburtius

GAE

(1996) Sambaqui Enseada (Arquivos de Guilherme Tiburtius I). Joinville: Museu Arqueológico de Sambaqui de Joinville.

71.

Vakily

(1989) The biology and culture of mussel of the genus Perna. ICLARM Studies and Reviews 17. Manila, Philippines and Eschborn: International Center for Living Aquatic Resources Management and Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ) GmbH.

72.

Weber

Silva

(2008) Sistemática molecular e Genética de populações de Perna perna. In: Resgalla

C Jr

Weber

Conceição

(Eds) O mexilhão Perna perna (L.): Biologia, Ecologia e Aplicações. Rio de Janeiro: Editora Interciência, pp. 121–149.

73.

Wood

Apte

Macavoy

, et al. (2007) A molecular phylogeny of the marine mussel genus Perna (bivalvia: mytilidae) based on nuclear (ITS1&2) and mitochondrial (COI) DNA sequences. Molecular Phylogenetics and Evolution 44: 685–698.

74.

Wright

(1978) Evolution and the Genetics of Populations, Volume 4: Variability within and among Natural Populations. Chicago, IL: The University of Chicago Press.