Discovery of an alien crab , Scylla serrata ( Forsskål , 1775 ) ( Crustacea : Decapoda : Portunidae ) , from the Caribbean coast of Colombia

A specimen of the swimming crab Scylla serrata, a species native to the tropical Indo-West and South Pacific, is reported from Cartagena Bay, Colombia, in the southern Caribbean. It is the third alien decapod crustacean documented from the Caribbean coast of Colombia. Analyses of genetic sequences points to a northern Indian Ocean origin of this specimen. Presence of this specimen is considered an isolated case, most likely kept alive for human consumption on board ship and discarded in the Bay.


Introduction
The "giant mud crab" Scylla serrata (Forsskål, 1775) is perhaps the largest member of the family Portunidae with a maximum carapace width of 280 mm, and a weight of 3.5 kg (Ng 1998;Poore 2004).This commercially important species, also known by other common names such as "mangrove crab", "muddie" or "Shri Lanka crab" (Davie 2002;Ng et al. 2008a,b), is native to the Indo-West and South Pacific Oceans, from South Africa and the Red Sea to Tahiti, and from Japan to northern and eastern Australia (Keenan et al. 1998;Brockerhoff and McLay 2011).The reported depth range is intertidal to 7 m (Poore 2004), but specimens are known to occur to depths of 60 m, and 3 to 95 km offshore in shrimp fishing grounds (e.g., Hill 1974Hill , 1994;;Knuckey 1996).An ovigerous specimen in the National Museum of Natural History, Smithsonian Institution (USNM 127095), was collected in the Bay of Bengal, Indian Ocean, from a depth of 82 m.This giant mud crab was intentionally introduced to the Hawaiian Islands between 1926 and 1935, where it is now commercially fished (Carlton and Eldredge 2009;Brockerhoff and McLay 2011).In the western Atlantic, attempts to introduce it to Florida's Gulf Coast failed (Park 1969, Masterson 1999;Fofonoff et al. 2003).Two specimens of S. serrata recorded off São Paulo and Rio de Janeiro, Brazil, are thought to have arrived in ballast water or as adults carried live for human consumption (Melo 1983;Tavares and Mendonça 2011).This species has failed to establish along the Brazilian coast (Junqueira et al. 2009;Tavares and Mendonça 2011;Tavares 2011).
The capture of Scylla serrata in Cartagena Bay, in the Caribbean coast of Colombia, is reported and relevant information about the geographical setting and its biology is briefly summarized.

Capture and environmental setting
On April 27, 2013, Mr. P. Berrío captured a large, unfamiliar, swimming crab in his gillnet on the southwestern portion of Cartagena Bay (Figure 1A) at a depth of 6.5 m.The crab was given to Mr. E. Berrío, a field aid working for the "Instituto de Investigaciones Marinas y Costeras" (INVEMAR).The specimen (Figure 1B-E 2010).Two faunistic reports of decapod crustaceans from the Caribbean coast of Colombia have been published (Campos et al. 2003(Campos et al. , 2005)), and one on decapod larvae (Medellín-Mora et al. 2009), but no detailed taxonomic studies exist of the crustacean fauna from Cartagena Bay and vicinity except for Lemaitre's (1981) study of the shallow-water brachyuran crabs, where he reported the presence of 96 species, none of which were alien species.

Taxonomy and ecology
There are four known species of Scylla, all with a natural distribution in the tropical regions of the Indo-West and South Pacific Oceans (Keenan et al. 1998).Scylla serrata can be recognized from other congeners primarily by the larger development and height of the four frontal lobes relative to the frontal width of the carapace, the narrow anterolateral carapace spines with outer margins concave, and well developed spines on the outer surface of the cheliped carpus and palm (Figure 1B-E).Modern diagnoses, color patterns, keys for identifications, summaries of taxonomy and distributions, biological information, and fisheries of Scylla species, can be found in Keenan et al. (1998), Ng (1998), Davie (2002), Poore (2004), and Ng et al. (2008a).
Scylla serrata is inhabits estuaries, mangrove swamps and sheltered bays where it is known to dig deep burrows in shallow to intertidal waters.It can be found in nearly fresh waters, although prefers salinities ≥ 34 in offshore waters (Keenan et al. 1998).It remains buried during the day, and emerges at night to feed on a diet of mollusks, crustaceans, other small invertebrates, and rarely plant materials and fish (Ng 1998;Fratini and Vannini 2002;Fofonoff et al. 2003;FAO 2013).Scylla serrata is considered to be a highly aggressive species (Motoh 1980).Most of its life cycle is spent in coastal waters but after mating, females migrate to the open sea where eggs hatch and larvae are released to spend three or four weeks in the plankton before adopting a benthic existence (Hill 1994;Knuckey 1996;Fratini and Vannini 2002).The larvae do not tolerate temperatures below 12°C or salinities below 17.5 (Hill 1974).

Origin, possible vectors, and significance
To establish the origin of our specimen, tissue was removed for molecular analysis.The cytochrome oxidase subunit I (COI) barcode region (658 bp) was sequenced and deposited in GenBank under accession number KF827821.A BLAST ® search of existing sequences revealed a 100% match to four sequences of Scylla serrata (KC200562, JN085428, JN085429, JN805434) from two unpublished studies originating in India.Our sequence was also a match to the COI barcode region of an unpublished mitochondrial genome of S. serrata from Thailand (FJ827758).While the precise collection localities of the specimens in GenBank cannot be confirmed, this evidence points to a northern Indian Ocean origin of our specimen.
The means of arrival of the specimen of Scylla serrata to Cartagena Bay can only be speculated upon.Introduction of crab species is most commonly attributed to larvae or juveniles transported in ship ballast water or on hull fouling (Brockerhoff and McLay 2011).In the absence of long-term monitoring studies, it is not possible to conclude in our case that larvae or juveniles of this species may have been discharged into the Bay or nearby offshore.As our specimen appears to be an isolated case, it seems unlikely that it arrived as larva or juvenile and then grew to such large size and weight.The large mariculture operations that exist south of the Bay do not culture S. serrata, and furthermore they are far removed and not directly connected to the Bay, so that vector is discounted.A more plausible explanation is that the specimen was kept live aboard ship for human consumption, and intentionally or unintentionally discarded near the entrance channel to the Bay where it was then collected by the fisherman.This method of introduction of alien species, is increasingly being reported (e.g., Abelló and Hispano 2006;Stebbing et al. 2012).Although a high volume of shipping does not necessarily translate to a higher rate of invasions (Ruiz et al. 2013), it is significant to note that Cartagena Bay receives heavy commercial and passenger cruise ship traffic originating from numerous ports in the Atlantic and Pacific, with 13,700 ships entering the Bay during the 5-year period of 2006-2010(Cañón Paez et al. 2010).The irresponsible practice of discarding living organisms that are carried on board ships for human consumption should be a concern to local authorities, as it could lead to establishment of alien populations.
Scylla serrata is the third Indo Pacific decapod introduced in the Caribbean coast of Colombia.Charybdis hellerii (A.Milne-Edwards, 1867) was recorded from Portete Bay, Guajira (Campos and Türkay 1989), and Penaeus monodon Fabricius, 1798, found on the Guajira coast and Ciénaga Grande de Santa Marta (Álvarez-León and Gutiérrez-Bonilla 2007;Gómez-Lemos and Campos 2008;EAVM, pers. obs.).The former presumably arrived in ship ballast water or hull fouling, whereas the latter was released, intentionally or not, by the local mariculture industry.Both species are considered locally established (RL, pers.obs.).
The spread of marine alien species is considered one of the most significant global modifiers of biodiversity of the oceans, and brachyuran crabs in particular, are a major component of bioinvasions (Cohen and Carlton 1998;Ruiz et al. 2000;Galil et al. 2002;Galil, 2007Galil, , 2009;;Brockerhoff and McLay 2011).Yet, many tropical coastal areas with high density of maritime traffic remain poorly studied, making timely detection of alien species difficult or unlikely.Given the recent exponential increase in traffic of commercial and tourist ships to major ports of the Caribbean coast of Colombia (Cañón Paez et al. 2010), it is likely that more than just the three alien species currently known from this coast (i.e., Charybdis helleri, Scylla serrata, Penaeus monodon) are present.Along the coast of Brazil alone, for example, 13 marine alien decapod species have been documented so far, five of which, all brachyurans, have become established (Tavares and Mendonça 2011).Only with careful field surveys of this important Bay will it be possible to first detect and then study the extent of ecological impacts from any alien species that arrives and becomes established.Ecological impacts of S. serrata, if it were to become established, to the local environment or fisheries are difficult to predict.Based on what is known about the life cycle and behavior of this crab species, it would seem appropriate to consider not just monitoring Cartagena Bay, but also nearby offshore oceanic areas where females theoretically would need to migrate and release their eggs.
), identified as Scylla serrata, measured 20.75 cm in carapace width, 13.20 cm in carapace length, and weighed 2 kg.It is deposited in the collections of Museo de Historia Natural Marina de Colombia (INV-CRU-8280), INVEMAR.Cartagena Bay is considered an estuary strongly affected by freshwater outflow and sediments from Canal del Dique, a man-made canal forced into the Bay since 1933.Outside the Bay, salinities vary from 35.7 to 35.9.Salinity inside the Bay depends upon whether it is the rainy or dry season and ranges from 3.1 to 36.1 and occasionally drop to 0 at the mouth of the Canal del Dique.Surface water temperatures range between 27 and 31°C (Vivas-Aguas et al.