Daniel Loebmann¹, Ana Cecília G. Mai² & James T. Lee³

1. Laboratório de Herpetologia, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Instituto de Biociências, Universidade Estadual Paulista, Av. 24 A, 1515, Bairro Bela Vista, CEP 13506-900, Rio Claro, SP, Brazil; contato@danielloebmann.com
2. Embrapa Meio-Norte, Laboratório de Recursos Aquáticos, BR 343, km 35, CEP 64200-970, Parnaíba, PI, Brazil; anacecilia_mai@yahoo.com.br
3. Laboratório de Biologia Pesqueira e Manejo de Recursos Aquáticos, Universidade Federal do Pará, Av. Perimetral, 2651. CEP 66077-830, Belém, PA, Brazil; james.jtlee@gmail.com

Abstract: Marine biological invasions have been regarded as one of the major causes of native biodiversity loss, with shipping and aquaculture being the leading contributors for the introductions of alien species in aquatic ecosystems. In the present study, five aquatic alien species (one mollusk, three crustaceans and one fish species) were detected during dives, shore searches and from the fisheries on the coast of the Delta do Parnaíba Environmental Protection Area, in the States of Piauí and Maranhão, Northeastern Brazil. The species were the bicolor purse-oyster Isognomon bicolor, the whiteleg shrimp Litopenaeus vannamei, the giant river prawn Macrobrachium rosenbergii, the Indo-Pacific swimming crab Charybdis hellerii and, the muzzled blenny Omobranchus punctatus. Ballast water (I. bicolor, C. hellerii, and O. punctatus) and aquaculture activities (L. vannamei and M. rosenbergii) in adjacent areas are the most likely vectors of introduction. All exotic species found have potential impact risks to the environment because they are able to compete against native species for resources (food and habitat). Isognomon bicolor share the same habitat and food items with the native bivalve species of mussels and barnacles. Litopenaeus vannamei share the same habitat and food items with the native penaeids such as the pinkspot shrimp Farfantepenaeus brasiliensis, the Southern brown shrimp Farfantepenaeus subtilis, and the Southern white shrimp Litopenaeus schmitti, and in the past few years L. vannamei was responsible for a viral epidemics in the cultivation tanks that could be transmitted to native penaeid shrimps. Charybdis hellerii is also able to cause impacts on the local fisheries as the species can decrease the populations of native portunid crabs which are commercialized in the studied region. Macrobrachium rosenbergii may be sharing natural resources with the Amazon River prawn Macrobrachium amazonicum. Omobranchus punctatus shares habit with the native redlip blenny Ophioblennius atlanticus and other fishes, such as the frillfin goby Bathigobius soporator. Some immediate remedial measures to prevent further introductions from ballast water and shrimp farm ponds should be: (i) to prevent the release of ballast water by ship/vessels in the region; (ii) to reroute all effluent waters from shrimp rearing facilities through an underground or above-ground dry well; (iii) to install adequate sand and gravel filter which will allow passage of water but not livestock; (iv) outdoor shrimp pounds located on floodable land should be diked, and; (v) to promote environmental awareness of those directly involved with ballast water (crews of ship/vessels) and shrimp farms in the region. Rev. Biol. Trop. 58 (3): 909-923. Epub 2010 September 01.

Key words: exotic species, ballast water, aquaculture, Mollusca, Decapoda, Blenniidae.

Numerous factors have been appointed to explain the disappearance of wild species from their natural habitats. Among them, biological invasions are a leading cause of species extinctions and biotic homogenization in terrestrial and freshwater systems worldwide (Sala et al. 2000, Lockwood & McKinney 2001, but see Gurevitch & Padilla 2004 for marine habitats), ranking second only, to habitat loss as the major threat to biodiversity (Wilson 1992, Wilcove et al. 1998).

The magnitude of the problem is extensive, and invasions frequently interact with other factors such as habitat loss, pollution and climate change compromising the integrity of marine ecosystems. Despite the severity of the implications, studies demonstrating the impacts of introduced species in the marine environment are rare, and most introductions probably go unnoticed (Rilov & Crooks 2009). Other factors have also been suggested as facilitators of the establishment of invasive species, including high reproductive rates, facilitated dispersal, low levels of competition among resident species, tolerance to a wide range of environmental conditions, often, and lacking predators in their new environment (Crawley 1986, Kolar & Lodge 2001, Sakai et al. 2001).

Several studies have summarized the impacts of invasive species on native species, and their community structure (Williamson 1996, Wilcove et al. 1998, Parker et al. 1999, Sala et al. 2000, Stein et al. 2000). These studies attributed the main impacts on native biota to the spread of exotic pathogens and parasites, biological competition for space and food, predation upon native species, and alteration of the genetic makeup in closely related species. Moreover, many species listed as threatened or endangered are considered to be at risk primarily because of competition with and predation by non-indigenous species (Wilcove et al. 1998).

Marine and freshwater ecosystems are particularly vulnerable to invasions of alien species as the dispersion of propagules in water occurs easier than in terrestrial environments. Minchin et al. (2009) provide a wide review of the vectors that contribute to the invasions of aquatic alien species and point out eight main pathways for a non-native organism to arrive in a new location. Among these vectors, shipping and aquaculture have been considered as the most critical pathways for marine invasions globally (Molnar et al. 2008). Burke et al. (2000) estimated that the marine ecosystems in the Mediterranean contain 480 invasive species, the Baltic 89, and Australian waters 124. Considering that the number of invasive species is increasing quickly and that undisturbed natural areas are declining, biological impacts by alien species may become the leading factor of ecological disintegration (Crooks & Soulé 1996).

In Brazil, despite the researchers efforts to try to understand the patterns of dispersion, causes and consequences of bioinvasions, the surveys are very limited. According to Ferreira et al. (2009) there is a clear trend of increasing bioinvasion events in regional coastal ecosystems, but whether invasion rates are actually increasing or are a result of more intensive research efforts in recent years is still an open question. Therefore, to understand and to track the expansion of the bioinvasions in the Brazilian coast, we present new records of occurrence of five aquatic alien species in the Environmental Protection Area and propose guidelines to circumvent further introductions to the coastal zone of the States of Piauí and Maranhão (Northeast Brazil), an ecological sanctuary which supports a rich diversity of aquatic fauna, including commercial and threatened species.

Site characteristics: Established on August 28^th 1996, the Delta do Parnaíba Environmental Protection Area (Delta do Parnaíba, EPA) is located among the pairs of geographical coordinates 02°37’-03°05’ S and 42°29’- 41°09’ W. The area covers 3 138km², which comprises the entire littoral of the State of Piauí and parts of the littorals of the States of Ceará and Maranhão. The tidal variation in the area is classified as mesotidal (Davies 1964), with a maximum range of 3.3m. Water temperature is homogenous throughout the area and averages 28.5±0.9oC (mean±SD). According to Köppen´s climate classification updated (Kottek et al. 2006), the area is classified as Aw (Equatorial climate with dry winter). Temperatures are warm throughout the year ranging from 22 to 33ºC with a marked dry period, when precipitation is lower than 100mm between June and December, and a rainy period in the first months of the year (January-May).

The coastal zone of the Delta do Parnaíba EPA is formed by a complex mosaic of several habitats such as coastal dunes, rocky shores, mangrove forests, estuaries, and sandy beaches. Three estuaries (Parnaíba River Delta, Camurupim/Cardoso and Timonha/Ubatuba) have important roles in the ecology of the coastal communities due to the release of large amounts of sediments and organic matter, especially in the rainy season. In addition, the Parnaíba River Delta is considered the third largest oceanic deltaic formation worldwide.

Sampling methods: Specimens of the non-native species were recorded from February 2005 to April 2009 in the municipalities of Parnaíba, Luis Correia, Cajueiro da Praia (State of Piauí) and Araioses (State of Maranhão). Individuals were obtained by the following methods: (1) Snorkeling; this method was performed sporadically on the beaches of Barra Grande (Cajueiro da Praia) and Coqueiro (Luis Correia) during the low tide (ca. 2 hours each dive); (2) Intensive search for unfamiliar individuals on rocky outcrops, which was conducted monthly on the beaches of Cajueiro da Praia and Barra Grande (Cajueiro da Praia), and Coqueiro (Luis Correia) during the low tide (ca. 3 hours each search); and (3) Monitoring the local fisheries (casting nets) during the season fishery of the white shrimp (May to July). Total length of each specimen collected was measured. Voucher specimens were fixed in 10% formalin, preserved in 70% alcohol, and deposited at the Zoological collection of the Natural History Museum of the Universidade Federal da Bahia (UFBA) and the Crustacean collection of the Fundação Universidade Federal do Rio Grande (FURG). Collecting permits were authorized by the Brazilian Environmental Protection Agency, the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) (Proc. Number 18027-2).

Five aquatic alien species (one mollusk, three crustaceans and one fish) new to the study area were identified during the period of this study (Fig. 1), i.e. the bicolor purse-oyster Isognomon bicolor (C. B. Adams 1845), the whiteleg shrimp Litopenaeus vannamei (Boone, 1931), the giant river prawn Macrobrachium rosenbergii (De Man, 1879), the Indo-Pacific swimming crab Charybdis hellerii (A. Milne-Edwards, 1867) and, the muzzled blenny Omobranchus punctatus (Valenciennes 1836).

Mollusca, Bivalvia, Isognomonidae: Isognomon bicolor. In June 2008, the mats of I. bicolor (Fig. 2) were identified attached on granite rock shores at the Pedra do Sal beach, municipality of Parnaíba, State of Piauí (02º48’10" S, 41º43’46" W) (Table 1). Pedra do Sal is the only beach on the coast of Piauí with granitic rocks permanently exposed. In addition, the beach is typically reflective with high-energy waves acting on the outcrops. The individuals of I. bicolor were found on the same substrates of the native mussels (Mytilus sp.), in small patches (each <2 m²) at the same zone of Mytilus sp.

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Crustacea, Decapoda, Dendrobranchiata, Peneidae: Litopenaeus vannamei. During April and May 2009, four specimens of L. vannamei (Fig. 3) were collected. The individuals were obtained from casting nets of fishermen in the municipalities of Luis Correia (02°53’ S, 41°37’ W) and Cajueiro da Praia (02°55’ S, 41°21’ W) (Fig. 1, Table 2). The individuals of L. vannamei were found along with two native shrimp species, the Atlantic seabob Xiphopenaeus kroyeri (C. Heller, 1862) and the Southern white shrimp Litopenaeus schmitti (Burkenroad, 1936). Individuals collected were adults ranging from 10 to 12.6cm standard length.

Crustacea, Decapoda, Pleocyemata, Caridae: Macrobrachium rosenbergii. In April 2009 three adult males of M. rosenbergii were detected in Delta do Parnaíba EPA: one specimen collected by a fisherman using a casting net at Barra Grande Beach, in the municipality of Cajueiro da Praia, State of Piauí (02º54’06" S, 41º24’25" W) (Fig. 4) (Voucher number: UFBA 260; 26.8cm standard length), one specimen captured by fishermen in Tatus’ pier harbor (02°49’56" S, 41°49’48" W), Ilha Grande de Santa Isabel municipality, Delta do Parnaíba estuary, and a specimen captured by fishermen in the Carnaubeiras, Araioses municipality, border between the States of Piauí and Maranhão (02º49’38" S, 41º57’45" W) (Fig. 1, Table 3).

Crustacea, Decapoda, Pleocyemata, Portunidae: Charybdis hellerii. Three specimens (two males and one female) were collected in the municipality of Cajueiro da Praia, State of Piauí (Fig. 5). All specimens were found occupying rock outcrops during the low water (02º54’10" S, 41º24’21" W) (Fig. 1, Table 4). Vouchers specimens were deposited in the Crustacean collection (3208) of the Fundação Universidade Federal de Rio Grande.

Discussion

Early detection of invasive species is fundamental to develop management actions to avoid the establishment or to control the spreading of invasive populations. This is particularly important because at early time, measures for contention or eradication are most effective. In the present study, five new occurrences of introduced species, varying from three different phyla, gives an indication of the ecological risks the Delta do Parnaíba EPA currently faces. Accordingly, some aspects of the biology of these species and considerations about their distribution in the Delta do Parnaíba EPA are presented, which could form a baseline for monitoring the impacts of these alien species.

Isognomon bicolor: According to Ferreira et al. (2009) I. bicolor is one of the most important species introduced to the benthic realm along the Brazilian coast. Originally from the Caribbean region, I. bicolor has been detected in Brazilian waters since 1994 (Domaneschi & Martins 2002), i.e. in the states of Rio Grande do Norte, Pernambuco, Bahia, Rio de Janeiro, São Paulo, and Santa Catarina (Domaneschi & Martins op cit., Jacobucci et al. 2006, Oliveira & Creed 2008) (Table 1). Ballast water and fouling of commercial vessels are the suggested vectors of introduction (Rocha 2002). Another hypothesis is that I. bicolor could have been introduced into Brazil accidentally on oil or gas platforms from the Caribbean coast (Oliveira & Creed 2008).

At the moment, the impact of this species on native biota in the region seems to be low. However, the species has dominated the midintertidal rocky shores along the Southeastern coast of Brazil (Magalhães 1999, Rapagnã 2004, Breves-Ramos 2004). For example, López (2003) estimated that a population of the native barnacle Tetraclita stalactifera reduced ca. 50% since the invasion of I. bicolor in Cabo Frio, State of Rio de Janeiro. Besides the competition and displacement of barnacle populations, I. bicolor probably competes with a commercial species of Mytilidae, Perna perna, a very abundant mussel found in the region (Rapagnã 2004, Breves-Ramos 2004, Ferreira et al. 2009), which is also an exotic species from Africa that reached the Brazilian coast in the 18^th and 19^th centuries during the slave trade (Ferreira et al. op cit.).

Litopenaeus vannamei: During the rainy season the probability of shrimp escapes increases considerably because the cultivation tanks, especially those near the rivers, cannot always support the excessive rainfalls. Fig. 7 shows two shrimp farms installed in the surroundings of Camurupim River where some tanks are within 30m of the river. Consequently, L. vannamei could be accidentally released from overflowed ponds and lakes into the marine areas.

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Litopenaeus vannamei was imported to Brazil in the 1970’s for aquaculture purposes. The species was considered the most viable for cultivation compared to native species due to the high adaptability to the varying hydrochemical conditions of the tropical estuaries in Northeast Brazil. At the moment, L. vannamei has been reported in Brazilian estuarine and coastal waters from Rio Grande do Norte (Santos & Coelho 2002) to São Paulo (Barbieri & Melo 2005) (Table 2). However, the occurrence of this species in the wild may be larger than documented as it is relatively difficult to distinguish L. vannamei from native penaeid species such as Farfantepenaeus paulensis, Farfantepenaeus brasiliensis and Farfantepenaeus subtilis. To what extent these fugitive specimens of poorly managed shrimp farms will be able to establish self-sustaining populations in the natural environment is still an open question (Ferreira et al. 2009).

Macrobrachium rosenbergii: The giant river prawn M. rosenbergii is the most cultivated freshwater shrimp in the world. It is native to the Indo-Pacific region (Pakistan, Vietnam, Philippines, New Guinea and Australia) (Chan 1998). Macrobrachium rosenbergii was brought to Brazil in 1977 for experimental cultivation purposes by the Department of Oceanography of the Universidade Federal de Pernambuco (Cavalcanti 1998). The species disseminated quickly to the States of Maranhão, Ceará, Pernambuco, Rio de Janeiro, São Paulo, and Santa Catarina (Barros & Silva 1997, Cavalcanti 1998, Valenti & New 2000).

Although Macrobrachium rosenbergii lives almost the entire life cycle in fresh water, it is considered an estuarine-depend species since it depends on brackish water to reproduce. According to Ling (1969), the physiological dependence of the larvae to brackish water is an important factor to contribute to the establishment of this species in natural waters. In the Brazilian coast there appears to be no well- established population of M. rosenbergii, however, records of occurrence in the wild has been observed for the States of Espírito Santo (Valenti & New 2000), São Paulo (Magalhães et al. 2005), Paraná (Gazola-Silva et al. 2007) and Pará (Barros & Silva 1997) (Table 3). The rainy season of 2009 accumulated the highest levels of rain fall since 1974 in coastal zone of Piauí. Considering that this species is cultivated in aquaculture farms around the City of Teresina (05°05’21" S, 43°48’09" W), it is probable that the incidental introduction was made by escapees from these farms.

Charybdis hellerii: The portunid crab Charybdis hellerii is a voracious Indo-Pacific species. The first documented invasion of C. hellerii occurred in Mediterranean Sea after the opening of the Suez Channel in the late 19th century (Galil 1992, Rodriguez & Suárez 2001). In Brazil, the species has been reported since 1995 (Tavares & Mendonça 1996) and thus far, the species has been reported from Maranhão (North) to Santa Catarina (South) (Carqueija & Gouvêa 1996, Calado 1996, Negreiros-Fransozo 1996, Mantelato & Dias 1999; Tavares & Mendonça 1996, Carqueja 2000, Ferreira et al. 2001, Almeida et al. 2003, Coelho & Santos 2003, Bezerra & Almeida 2005; Braga et al. 2005, Almeida et al. 2006, Reigada et al. 2006, Feres et al. 2007, Frigotto & Serafim-Junior 2007, Coelho et al. 2008, Lima-Junior et al. 2008) (Table 4). According to Ferreira et al. (2009) two hypotheses should be considered for the presence of C. hellerii in Brazilian waters. First, the possibility that the species arrived in Brazil as a result of natural dispersion from populations inhabiting the Caribbean Seas since the mid-1980s. Second, the invasion of Brazilian waters through secondary introduction with ballast water.

Furthermore, Charybdis hellerii might have economic impacts to local fisheries as this species may become a competitor of the native portunid crabs (Callinectes spp.) which are commercialized in the region. Although C. hellerii is similar in size with the native portunids, this exotic species has no commercial value (Lima-Junior et al. 2008).

Omobranchus punctatus: The original distribution of the muzzled blenny O. punctatus was presumed to be the Indo-Pacific region, ranging from Japan and Australia to the Persian Gulf (Golani 2004). In Brazil, the first occurrences were registered in the States of Bahia, Rio de Janeiro and Santa Catarina (Mendonça et al. 2005, Gerhardinger et al. 2006) (Table 5).

Omobranchus punctatus arrived into Brazilian waters by ballast or bilge water, hidden inside the fouling of ships (Gerhardinger et al. 2006). However, records presented here may have been an effect of the species dispersion since the maritime transport in the region is restricted to small vessels with limited use of ballast water.

Conservation implications: The introduction of exotic and allochtonous species to local communities and ecosystems has been leading to relevant modifications in the food webs, steady-state populations and changes in the ecosystems functional processes (Rocha et al. 2005).

Environmental impacts associated with the implementation of non-sustainable practices in shrimp farms have been neglected in favor to immediate socio- economic benefits. Mangrove deforestation for the establishment of cultivation tanks, outflow of highly eutrophic effluents into natural water bodies, and the potential dissemination of shrimp virus diseases to native crustacean populations are among the main impacts caused by aquaculture (Boeger et al. 2005, Ferreira et al. 2009).

Tavares & Mendonça (2004) have reported the introduction of at least 18 species of exotic decapods in the Brazilian coastline. Five species (28%) have managed to keep reproductively active populations, Charybdis hellerii, Rhithropanopeus harrisi (Gould, 1841), Pyromaia tuberculata (Lockington, 1877), Macrobrachium rosenbergii (De Man, 1879), and Procambarus clarkii (Girard, 1852). Two species have probably reproduced in Brazilian waters, Pilummoides perlatus (Poeppig, 1836) and Penaeus monodon (Fabricius, 1798); and the remaining 11 species (61%) had few individuals recorded in natural environments.

All exotic species recorded in this study have high potential to compete for natural resources against native fauna. Isognomon bicolor share the same habitat and food items with the native species of mussels and barnacles (López 2003, Fernandes et al. 2004). Litopenaeus vannamei share the same habitat and food items with the native penaeids such as the pinkspot shrimp Farfantepenaeus brasiliensis (Latreille, 1817), the Southern brown shrimp Farfantepenaeus subtilis (Pérez Farfante, 1967), and the Southern white shrimp Litopenaeus schmitti (Burkenroad, 1936). Charybdis hellerii share resources (space and food) on rocky shores with several brachyurans such as the masked swimming crab Callinectes larvatus Ordway, 1863, the Rugose swimming crab Callinectes exasperatus (Gerstaecker, 1856), the Dana swimming crab Callinectes danae, the Cuban stone crab Menippe nodifrons (Stimpson, 1859), and the narrowback mud crab Panopeus americanus Saussure, 1857. Macrobrachium rosenbergii may be sharing natural resources with the Amazon River prawn Macrobrachium amazonicum (Heller, 1862). Omobranchus punctatus shares habit with the native redlip blenny Ophioblennius atlanticus (Valenciennes, 1836) and other fishes, such as the frillfin goby Bathigobius soporator (Valenciennes, 1837).

Litopenaeus vannamei brought other threats to native crustacean species. In the past few years, almost all farms with cultivated shrimps in the State of Piauí and adjacent states were suffering from a high incidence of viral epidemics, such as the White spot syndrome (WSS), the Taura Syndrome Virus (TSV), the Infectious Myonecrosis Virus (IMNV) and the Necrotizing Hepatopancreatitis (nhp) (Pantoja & Lightner 2008). These pathogens are highly lethal to cultivated Litopenaeus vannamei (Briggs et al. 2005) and could be transmitted to native penaeid shrimp populations (Overstreet et al. 1997, Briggs et al. 2005). Many species have been reported as susceptible hosts (Penaeus merguiensis De Man, 1888 and Metapenaeus monoceros (Fabricius, 1798), while Palaemon setiferus Olivier, 1811, Euphausia superba Dana, 1852, Metapenaeus dobsoni (Miers, 1878), Parapenaeopsis stylifera (H. Milne Edwards, 1837), Solenocera indica Nataraj, 1945, Squilla mantis L., 1758, Macrobrachium rosenbergii and other crustaceans can act as latent carriers (Flegel et al. 1997, Hossain et al. 2001).

The release of non-native organisms is a federal offense according to Brazilian legislation and ballast water/aquaculture in Brazil should be conducted strictly in accordance with specific regulations, control and effective inspections (Alves et al. 2007). Some immediate remedial measures to prevent further introductions from ballast water and shrimp farm ponds should be: (i) to prevent the release of ballast water by ship/vessels in the region; (ii) to reroute all effluent waters from shrimp rearing facilities through an underground or above-ground dry well; (iii) to install adequate sand and gravel filter which will allow passage of water but not livestock; (iv) outdoor shrimp pounds located on floodable land should be diked, and; (v) to promote environmental awareness of those directly involved with ballast water (crews of ship/vessels) and shrimp farms in the region.

In order to understand the real impacts that alien species may cause after introduction to new environments, biological and ecological studies are still necessary. Therefore, the data presented in this study is of notable importance to environmental institutions of the government (Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis and Instituto Chico Mendes de Conservação da Biodiversidade) which are the managers of the Delta do Parnaíba EPA.

Acknowledgments

En el Área de Protección Ambiental del Delta Del Río Parnaíba, noreste de Brasil fueron detectadas cinco especies acuáticas invasoras (un molusco, tres crustáceos y un pez): la ostra de dos colores Isognomon bicolor, el camarón patiblanco Litopenaeus vannamei, el camarón gigante de río Macrobrachium rosenbergii, el cangrejo nadador del Indo-Pacifico Charybdis hellerii y el blenio hocicudo Omobranchus punctatus. El agua de lastre (I. bicolor, C. hellerii, y O. punctatus) y la acuicultura (L. vannamei y M. rosenbergii) en áreas adyacentes son los vectores de introducción más probables. Todas las especies exóticas encontradas son potencialmente riesgosas para el ambiente ya que son aptas para competir con las nativas por recursos como alimento y hábitat. Charybdis hellerii también podría causar impacto en el recurso pesquero local, al reducir las poblaciones de cangrejos portúnidos nativos, comercializados en el área de estudio.

Palabras clave: especies exóticas, agua de lastre, acuicultura, Mollusca, Decapoda, Blenniidae.

Received 20-IX-2009. Corrected 26-II-2010. Accepted 25-III-2010.

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