Invasion of the Indo-Pacific blenny Omobranchus punctatus ( Perciformes : Blenniidae ) on the Atlantic Coast of Central and South America

We examined 308 specimens of the Indo-Pacific blenniid Omobranchus punctatus deposited in four museum collections, and analyzed data on their collection locations to assess its invasion on the Atlantic coast of Central and South America. This species occurs in shoreline estuarine and marine habitats in the Indo-West Pacific. Previous sampling and recent records in the Tropical West Atlantic from 1930 to 2004 produced 20 records for: Panamá, Colombia, Venezuela, Trinidad and Brazil. In this work, we provide data on 17 new records for the Gulfs of Venezuela and Paria in Venezuela, as well as four records for Maranhão and Pará states in NE Brazil. The temporal pattern of collections (1930 2009) and the proximity of most localities to ports and zones of ship traffic indicate that O. punctatus was initially introduced to the Atlantic by ships travelling from India to Trinidad. Within Brazil the introduction is linked to shipping connected to petroleum platforms. In Maranhão and Pará the introduction may have occurred as a result of fish sheltering in fouling on hulls of ships moving between ports around the mouth of the Amazon River. Alternatively, the spread of this species along of the American coast may reflect the expansion of the range of O. puntactus through larval dispersal in northward flowing currents. We recommend monitoring of this introduced species, and studies of its ecology in West Atlantic areas.


Introduction
Biological invasions are closely related to the history of humanity (Cavalcante & Major, 2006) and are among the main agents of environmental changes in the world (Occhipinti-Ambrogi, 2007).There is a relationship between environments altered by mankind and the existence of invasive species (Sax & Brown, 2000).Among marine environments, estuaries are among the ecosystems most altered by anthropogenic actions and are the sites of the greatest number of records of invasions (Moyle et al., 1999).Wonham et al. (2000) proposed that the invasion of a new environment by an exotic species includes three phases: dispersion, introduction and settlement These phases, along with the survival capacity of the species to its new environment, influence its success as an invader.According to these authors, Blenniids, Gobiids, and Pleuronectids dominate the records of introductions to exotic locations via ballast water because such water provides conditions resembling normal habitats used by them.
The blennies(Blenniidae), comprised about 360 species in 56 genera, are cosmopolitan in tropical and subtropical marine habitats (Nelson, 2006).The natural geographic range of Omobranchus punctatus (Valenciennes, 1836) spans from the northern Indian Ocean to the Western Pacific Ocean.In the 1960s, records of specimens collected in the Atlantic began to be reported, and currently the species is known from the Caribbean and eastern Africa (Cervigón, 1966;Springer & Gomon, 1975;Cervigón, 1994), Suez Canal and Mediterranean Sea (Bath, 1980;Golani, 2004) and Brazil (Gerhardinger et al., 2006).Omobranchus punctatus is regarded as an exotic species introduced in the Atlantic.
This work was aimed to elucidate the historical information on records of O. punctatus on the Central and South Western Atlantic coast, adding new information in order to understand the process of invasion by this species in the region.

Material and Methods
Two approaches were selected in order to determine the invasion of O. punctatus: (1) field work collections and (2) Museum analyses.For (1) various samplings were done using different fishing methods, such as hand nets and, in some cases, fish poison (Rotenone and Mentol).For (2) an exhaustive bibliographic survey was conducted along, with recisions of fish collections of the following Venezuelan museums such as: Museo de Historia Natural La Salle, Caracas (MHNLS); Museo Oceanológico Hermano Benigno Román, Isla de Margarita, Nueva Esparta State (MOBR-EDIMAR), and Museo de Ciencias Naturales de Guanare, Guanare, Portuguesa State (MCNG).In addition, the following fish collections were reviewed in Brazil: Deparmento de Oceanografia e Limnologia, Universidade Federal de Maranhão, Maranhão (CPDOL-UFMA); Grupo de Ecologia Aquática, Pará (GEA/UFPA), and Museu Nacional, Rio de Janeiro (MNRJ).The following collections of fishes from the United States were consulted via internet: Academy of Natural Sciences of Philadelphia, Philadelphia, (ANSP); National Museum of Natural History, Smithsonian Institution, Washington (USNM); Natural History Museum of Florida, Gainesville, Florida (UF); Oceanography Institute Scripps, La Jolla, California (SIO); Laboratory of Coastal Investigations of the Gulf Ocean Springs, Mississippi (GCRL); American Museum of Natural History, New York (AMNH), and Natural History Museum, London (BMNH).The other institutional abbreviations mentioned in this essay follow Leviton et al. (1985), except MHNLS, MOBR-EDIMAR, EBRG, CPDOL-UFMA and Laboratório de Biologia Pesqueira, Universidade Federal do Pará (LBP-UFPA).Other acronyms mentioned in this paper correspond to the ones from Institute of Investigations and Natural Museum Senckenberg (SMF), Frankfurt, Germany and from Hebraic University of Jerusalem (HUJ), Jerusalem, Israel.

Results and Discussion
A description of Omobranchus genus can be found at Williams (2002).Omobranchus punctatus (Fig. 1) is characterized by having a very elongate rounded head lacking a longitudinal crest on its top; almost always 3 (2-4) pores between the eyes; lateral line with 2-8 double-pored tubes; the gill opening is restricted to above the level of the pectoral fin; dorsal fin XII (XI-XIII), 19-24; anal fin II, 20-26, 1 or both spines imbedded, not visible externally; tail fin with 13 (11-14) segmented rays, none filamentous; a paleedged dark bar across the nape, a little before the origin of the dorsal fin, about 11 dark saddles across the top of the back; 3 dark bars on the lower part of the head and another on the pectoral fin base; and 4-5 slender dark stripes along the upper side of the front half of the body.
The natural range of O. punctatus includes the northern Indian Ocean and western Pacific, from the Persian Gulf (Iraq) to India, Japan, the northern Australian coast and the Fiji Islands (Springer & Gomon, 1975).
In the Caribbean, the first records of O. punctatus was in 1930, when Fowler (1931) described a new species of blenny, Poroalticus sewalli, with specimens captured on the western coast of Trinidad (Brighton beach, Gulf of Paria) (Table 1).In 1975, this species was recognized as a synonym of O. punctatus (Springer & Gomon, 1975). In 1961, Cervigón (1966) recorded O. punctatus (as O. dasson), at the Guiria on the Venezuelan coast of the same Gulf.After Fowler's initial record (1931), more specimens were collected from Trinidad in 1933Trinidad in , and between 1960Trinidad in and 1968 (Table 1) for both the Atlantic and Paria coasts of that Island, and the western coast of the Gulf of Paria (Figs. 2a and b).
In Central America, this species has been recorded from Panama, with records of collections between 1967 and 1974 (Fig. 2a, Table 1) 1).Springer & Gomon (1975) and Carlton (1985) suggested that it is likely that specimens of muzzled blenny from Panama originate via shipping movements from the population at Trinidad.This hypothesis was supported by strong similarities in the morphology of specimens collected from those two countries.
The Caribbean coast of Colombia has been intensively sampled over the past 30 years, and as a consequence its shore-fish fauna is well known.Intensive sampling by Garzón-Ferreira (1989) on the Colombian coast revealed no specimens of O. punctatus.To date, the only record of this species (Table 1) on that coast of Colombia is a single specimen from Portete Bay, on Guajira Peninsula, in the eastern end Colombia, just west of the Gulf of Venezuela (Fig. 2c).
There are various records of O. punctatus collected in the Gulf of Venezuela, adjacent to the east of Guajira Peninsula (Fig. 2c, Table 1).These include the Gulf itself, and several sites in the channel connecting lago de Maracaibo to the Gulf of Venezuela.Such specimens were captured between 1978 and 2007 and represent new records from this study.The first record of O. punctatus from eastern Venezuela was taken by Cervigón (1966) from the Gulf of Paria in 1961 (Table 1).Subsequently, Lasso et al. (2004) collected specimens from a rocky beach of the Orinoco Delta river, in 2002 (Table 1).Other new records from Venezuela are five lots (36 specimens) collected at that same site and a nearby sandy beach in 2004 and 2006 (Table 1).An additional specimen was found in the mouth of Caño Macareo (68 km east of the previous location) in 2008 (Table 1), together with 14 specimens from four locations from the eastern end of South coast of the Paria Peninsula.(Fig. 2a; Table 1).One of us (RR), while snorkeling at one of the latter sites, saw dozens of O. punctatus darting around a rocky point within 1 m of the surface of the water.Most recently (April 2009), a specimen was captured inside the shell of a dead barnacle attached to the hull of the ship Boca Grande, 7 km north of the outfall from Caño Macareo.
The two regions of Venezuela where the populations of O. punctatus evidently are established, the (western) Gulf of Venezuela and the (eastern) Gulf of Paria include the most extensive and important estuary areas of the northern coast of South America.Extensive sampling using small rotenone stations of shallow estuarine and marine habitats between Paria Peninsula and the Gulf of Venezuela by JP, JVT and DRR, between 2005 and 2008 failed to record any specimens of O. punctatus.The entrance of lago de Maracaibo and the Gulf of Paria were the only two locations in which O. punctatus was collected.
In Brazil, the records of O. punctatus date from 2002 and 2008 (Figs. 1 and 2d, Table 1).In 2002, 90 specimens were captured in the Bahia State (Gehardinger et al. 2006).In 2004, Gehardinger et al. (2006) found two specimens in Rio de Janeiro State, and six specimens were collected from fouling organisms on the hull of a ship in Santa Catarina State (Table 1).Here we report new records from the vicinity of the mouth of the Amazon River in 2005 and 2006 (Figs. 1 and 2d Table 1).Most recently, a population was found in Pará State (Fig. 2d, Table 1).Springer & Gomon (1975), on the basis of a morphological and historical analysis of the species in the west Atlantic concluded that the populations of O. punctatus are the result of an introduction to Trinidad via shipping from India between 1538 and 1914 that transported immigrant workers to Trinidad Island.They thought that ballast water or hull fouling organisms were involved in supporting O. punctatus individuals during the voyages.
Information we presented and summarized here, based on collections of O. punctatus at additional sites in the Central and NE South American coast also implicates shipping movements in subsequent expansions of that species range.All new collection sites are at or very near to, ports and seaways that support heavy shipping activity: the Gulf of Venezuela and Lago de Maracaibo and the sites in NE Colombia.In this regard, the absence of records of O.  Hostim et al. (2002) linked recent records of this species at sites on the east coast of Brazil to ship movements and shipping supply of offshore oil platforms.On the NE coast of Brazil, the collection sites reported here support heavy shipping.However, some expansion of the geographic range of O. punctatus through larval dispersal on nearshore ocean currents may well be involved in expansions along the eastern coast of South America: the south Equator Current flowing across the Atlantic bifurcates when it meets the hump of Brazil, with the North Brazil Current flowing along the coast to the Caribbean, and the South Brazil current flowing south to about the tropic of Capricorn.These currents are thought to be important in promoting dispersal of reef fishes (e.g.Rocha, 2003).The former could be involved in spreading O. punctatus along the NE coast of Brazil and the latter in spreading it along the southern Brazilian coast.
Other exotic species have been introduced to the southern Caribbean Sea.Pezold & Cage (2002) found Eleotris picta (Eleotridae), from western Venezuela.Its natural distribution encompasses the Pacific coast of the America between Mexico and Ecuador.Lasso-Alcalá et al. (2005a) and Lasso-Alcalá et al. (2005b) found the eleotrid Butis koilomatodon and the gobiid Gobiosoma bosc, near the capture points of O. punctatus on the north side of the Orinoco Delta River.Butis koilomatodon, which naturally occurs from east Africa to the West Pacific (Papua New Guinea) (Dawson, 1973;Miller & Wongrat, 1990), had also been collected from the Pacific side entrance (Miraflores locks) to the Panama Chanel (Dawson, 1973), Western Central Atlantic: Port Harcourt, Nigerie (Miller et al., 1989), Boffa, Guine (Harrison et al., 2003) and mouth of Ndian river in Cameron (Stiassny et al., 2008).The natural range of Gobiosoma bosc is the north west Atlantic, from the western Gulf of México to Massachusetts, on the Atlantic coast of the US (Bohlke & Robins, 1968;Castro-Aguirre et al., 1999;Williams, 2002).
In the last ten years, the Indo-Pacific lionfishes Pterois volitans (Linnaeus, 1758) and P. miles (Bennett, 1828) have been recognized as the most alarming cases of introduction  1); c) Localities with records of Omobranchus punctatus in western Venezuela (Gulf of Venezuela) and Colombia (Guajira Peninsula) (see Table 1) and d) Localities with records of Omobranchus punctatus from Maranhão and Pará states, northern Brazil (see Table 1).
. All records of the species in Panama come from the Caribbean entrance of the Panama Chanel.Fish collections made between 1935 and 1937 at the Pacific side of the Chanel (Miraflores locks) by Hildebrand (1939) yielded no specimens of O. punctatus.Also, the species was not recorded in these areas by McCosker & Dawson (1975).To date, there is no evidence of its occurrence on the Pacific coast of Panama.The Chanel first began operation in 1914.The first record of O. punctatus in Trinidad dates from the 1930s.The first records of O. punctatus in Panama, at the Caribbean entrance to the canal, are from 1967, much later than the first record from Trinidad (1930) (Table

Fig. 2 .
Fig. 2. Distribution of Omobranchus punctatus in Central and South American coasts.a) Full circle represents new records and open circle represents records from literature; b) Catch sites of Omobranchus punctatus in the eastern coast of Venezuela (Gulf of Paria) and Trinidad (see Table1); c) Localities with records of Omobranchus punctatus in western Venezuela (Gulf of Venezuela) and Colombia (Guajira Peninsula) (see Table1) and d) Localities with records of Omobranchus punctatus from Maranhão and Pará states, northern Brazil (see Table1).