Potential invasion of the Atlantic coast of South America by Semimytilus algosus ( Gould , 1850 )

The mytilid Semimytilus algosus (Gould, 1850) was collected from a fishing vessel after an in-water hull cleaning operation at Nuevo Gulf, north Patagonia, Argentina. This species is native to the Pacific coast of South America and had not been detected on the Atlantic coast of this continent. Histological slides from male and female portions of gonads of a subsample of specimens showed spawning activity. The gonad stages observed were: developing stage, ready to spawn, spawning, or had already spawned, suggesting the possibility of establishment of a breeding population in the area. The water temperatures, its seasonal range, and the habitats occupied by S. algosus in its native area are very similar to those present in Nuevo Gulf. The plasticity of this species, and its rapid invasion in other regions of the world, suggest that it could become a new invasive species in the Southwestern Atlantic in the near future. Targeted monitoring of the rocky shores of Nuevo Gulf is recommended to determine whether this non-native species is at an early stage of becoming established.


Introduction
It is widely accepted that many non-native marine species have been transported to new locations in the ballast tanks or attached to hulls of commercial ships (Ruiz and Carlton 2003).Authorities generally focus their attention on the management of ballast water and their associated sediments; however, the hull of vessels, and especially the sea chests, can be densely colonized by marine species, despite the use of antifouling paints (Gollasch 2002;Hopkins and Forrest 2008).Large cargo vessels (e.g.container vessels, >50 m length), bulk carriers, and oil tankers spend about 12-72 hours at each port and chances of being colonized by fouling species can be low.In contrast, smaller vessels, such as fishing ships, can spend weeks or even months at each harbor, which increase the opportunities to be colonized by fouling organisms (Brock et al. 1999;Coutts and Taylor 2004).
Speed and fuel consumption of ships are negatively affected when the hull is colonized by marine species.For this reason, most commercial ships have regular schedules for dry docking, cleaning, and application of antifouling paints (Davidson et al. 2008).Small vessels, however, often are cleaned manually in situ and rotating brushes and scrapers do not retain the defouled material; consequently, viable organisms, fragments, and propagules are thrown into the sea (Hopkins and Forrest 2008).Some countries have no regulations on hull-fouling management; hence, in-water hull cleaning is a common practice (but see the biosecurity regulations of New Zealand and Australia, Campbell 2008;Hopkins and Forrest 2008).In Argentina, small national and international fishing ships usually stop in gulfs, bays, and calmwater harbors for different requirements (medical care, food supplies, hull inspections, etc.) and for widely varying lengths of time.There are few regulations related to the prevention of establishment of marine invasive species in Argentina (see Boltovskoy et al. 2011), and all of them are related to the control and management of ballast water.Regulations about hull cleaning procedures are still under discussion.Within this context, samples of bivalves removed during in-water hull cleaning of a fishing ship in Puerto Madryn were obtained, all specimens were subsequently identified as the non-native Semimytilus algosus (Gould, 1850) and, as documented in this study, many specimens were reproductively active.This study reports the potential introduction of the bivalve S. algosus to the east coast of South America.

Methods
On 23 February 2013 a squid-fishing vessel arrived in Puerto Madryn harbor (42°14'30"S, 65°10'10"W), Argentina, for medical and food supplies.During its visit, an in-water hull cleaning procedure was performed by a local scuba diving company.The sea chests, colonized by unknown bivalves, were cleaned and some of the bivalves were discarded into the harbor.However, a sample of specimens was transported to the Centro Nacional Patagónico (Puerto Madryn, Argentina) for identification.Bivalves were received frozen and stored at -18°C.
The bivalves were identified using the appropriate taxonomic literature and were compared to the type material.To evaluate if the specimens were reproductively active, the sexual maturity and gonadic stages of a subsample were examined histologically.The shell lengths of 20 large specimens were measured with a digital caliper, then each individual was dissected and their gonads fixed for 3 hours in Bouin's solution.Fixed gonads were transferred to 70% ethanol, dehydrated in increasing ethanol concentrations, embedded in paraffin at 58°C, cut into 6-µm sections with a sliding microtome, and mounted on slides.The sections were then stained with hematoxylin and eosin, and examined under a light microscope.Photographs of the different gonadal stages observed were taken with a digital camera.
Gonadic maturity stages were classified by histological slides of the mantle tissues following Bigatti et al. (2005) for the mytilid Perna viridis (Linnaeus, 1758).These stages are: immature stage (gonads are not differentiated and follicles are not developed, therefore sex cannot be differentiated), growing stage (gamete development from the follicle walls, oogonia present in females and spermatocytes visible in males), ready to spawn stage (gonads ripe and gametes mature.In males mature spermatozoon attached to the follicle walls; in females: oocytes occupying the whole follicle), spawning stage (gametes detached from the follicle walls and released into the lumen of the follicles), spent stage (male and female follicles empty and some residual gametes present in the lumen), and resorption stage (atresic cells present in male and female follicles with gametes in the process of degradation).

Taxonomic remarks of the potential invader
All of the specimens taken to the laboratory were identified as Semimytilus algosus (Mytilidae, Figure 1) based on the relevant taxonomic literature (Lamy 1931;1936;Soot-Ryen 1955;Kensley and Penrith 1970) and comparison to the type material originally collected in Callao, Lima (Peru) and deposited at the Museum of Comparative Zoology (MCZ 216829, 154352), Harvard University, USA.Shell morphology of sampled specimens agreed with the diagnostic characters established for the species by Soot-Ryen (1955).These characters were: an elongate mytiliform shell; interiorly nacreous with anterior adductors present and posterior adductors and retractors continuous; hinge plate without teeth and resilial ridge compact; and external surface smooth with concentric and irregular rings from umbo to posterior edge.All specimens collected during this study were deposited at CENPAT General Invertebrate collection (CNP-INV 1783).

Gonadal stages
Shell length of the subsample of 20 specimens examined in detail ranged between 19.5-and 49.5 mm with a mean of 38.8 mm (SD=7.9).All of the specimens studied were mature: the male portion of the gonad was whitish and the female portion was grey-violet.Of the 20 bivalves examined, 14 had hermaphroditic gonads, one had male-only gonads, and five had female-only gonads.Based on the histological sections, these animals were reproductively active.Female gonad sections presented as 40% in growing stage, 10% ready to spawn, 31% spawning, 10% spent, and 9% in resorption (Figure 2 A-B).Sections of the male portion of the gonads presented as 38% in the growing stage, 29% ready to spawn, and 33% spawning (Figure 2 C-D).

Discussion
Semimytilus algosus is native to the Pacific coast of South America, and its distribution ranges from Manta, Ecuador (0°56'S, 80°92'W) to Gulf of Arauco, Chile (37°12'S, 73°20'W) (Osorio and Bahamonde 1968).It is recorded from the intertidal and subtidal rocky shores and as a fouling species in scallop aquaculture facilities (Pacheco and Garate 2005).This species is a common organism living on wave-exposed rocky shores along the Pacific coast (Tokeshi and Romero 1995;Navarrete et al. 2002).However, it is absent from the Atlantic coast of South America but that may well change if the animals detected in this study reproduced successfully.
The fishing vessel carrying S. algosus was anchored in Callao, Peru, for one month from October -November, 2012 and this was the last port-of-call.Callao is a breakwater harbor surrounded by sandy and rocky shores with a mean sea-surface water temperature in summer 2012 of 20-22°C and 16-19°C in winter (IMARPE 2014).At the southern limit distribution of the species in Chile, the sea-surface water temperature ranges from 9-11°C (Castro et al. 2000), while the temperature in Puerto Madryn varies between 9°C in winter to 20°C in summer (Servicio de Hidrografía Naval 2013).Although there are environmental differences between the source and possible recipient regions (nutrients, ocean currents, wave force, upwelling, among others Werlinger 2004;Falabella et al. 2009), the thermal range in Nuevo Gulf is similar to that observed in the native area.It is remarkable that S. algosus was able to recruit and grow on the vessel when it was anchored in Peru and then to survive the long trip to the Atlantic coast.Moreover, the sampled mussels were reproductively active, with some specimens ready to spawn and others spawning.
In its native range, S. algosus is reproductively active throughout the year, recruits are observed year round, and there is a reproductive peak during summer months (Navarrete et al. 2002;Belapatiño 2007).In its native environment, larval development is completed in about 27 days and pediveliger metamorphoses at a maximum size of 150 μm (Ramorino and Campos 1983;Garrido 1996).With a suitable thermal range, and rapid larval development, we think survival of this species on the Atlantic coast is highly likely.
Semimytilus algosus has already been introduced in to the western (Atlantic) coast of Africa.
Specimens of Mytilidae from South Africa in the collection of the South African Museum were tentatively identified as S. algosus by Barnard (1964), a finding later confirmed by Kensley and Penrith (1970).However, this was not the first introduction to the African continent.The species Modiola pseudocapensis was described for the coast of Namibia (Lamy 1931) but subsequent authors (e.g.Kensley and Penrith 1980;Branch et al. 2010;Mead et al. 2011) referred this Namibian population as S. algosus.At present, non-native species are dominant species of some rocky shores on the west coast of South Africa: S. algosus has colonized the lower intertidal along 500 km of coastline; Mytilus galloprovincialis Lamarck, 1819 has invaded the mid-intertidal zone, and Balanus glandula Darwin, 1854 has colonized the high intertidal zone (de Greef et al. 2013).Of these, B. glandula is also an invasive species on the east coast of Argentina (Schwindt 2007).
Semimytilus algosus appears to have a great impact on the native rocky-shore community.Because this species is numerically dominant and forms dense beds, it excludes other species from subtidal areas of the wave-exposed shore (de Greef et al. 2013).At the present, the low intertidal rocky shores in Patagonia are dominated by the blue mussel Mytilus sp. and the ribbed mussel Aulacomya atra (Molina, 1782), and the establishment of Semimytilus would likely affect the ecological interactions within this habitat.With its smaller size and smaller interstitial spaces, Semimytilus might create new refuges for infaunal species not typically found in existing mussel beds (Sueiro et al. 2011).In addition, predator-prey interactions could change.For example, the sea urchin Arbacia dufresnii (Blainville 1825) is a generalist consumer and is very abundant in the subtidal (Penchaszadeh and Lawrence 1999) of Nuevo Gulf and it is unknown how its population might change in response to a new, smaller, prey species.The voracious, opportunist, sea slug Pleurobranchaea inconspicua Bergh, 1897, also is observed in high densities (Muniain et al. 2007) and other organisms such as the sea star Anasterias antarctica (Lütken, 1857), and crabs (including the invasive Carcinus maenas (Linnaeus, 1758)) are also potential predators of S algosus in low shore areas (Hidalgo et al. 2007;Gil and Zaixso 2008).With its small size compared to native mussels, abundances of some predators may actually increase as abundance of this novel prey (S. algosus) of suitable handling-size increases.
Semimytilus algosus has economic value in its native area.In Peru, this species is collected from the wild for human consumption and it is raised in limited quantities in some aquaculture sites in Chile (Gonzalez et al. 1980).In South Africa the economic effects of this non-native species have yet to be evaluated (de Greef et al. 2013).The development of fisheries for invasive species can be a good strategy for mitigation, and fisheries now exist for the invasive green mussel Perna viridis in Venezuela (pers.obs)and the exotic Rapana venosa (Valenciennes, 1846) in Uruguay (Carranza et al. 2013).
The results of this study have identified a problem with current in-water hull-cleaning practices.These operations are common in many regions, especially for small recreational vessels.However, some countries have placed restrictions on this method due to biosecurity risks (Forrest and Hopkins 2008).The absence of legislation addressing hull-cleaning practices in Argentina (Boltovskoy et al. 2011) increases the incentive for large commercial vessels to perform hull inspections and defouling practices outside their dry-docking schedule in, for example, the calm waters of Nuevo Gulf, Argentina.Although Patagonian ports are not the most important in Argentina in terms of shipping traffic, the number of exotic species is increasing (Schwindt et al. 2014) and some of them, like the aggressive kelp Undaria pinnatifida (Harvey) Suringar, likely were introduced as a fouling species and have changed the landscape and affected the native biodiversity in a negative way (Casas et al. 2004, Irigoyen et al. 2011).Thus, there is an urgent need to discuss and to legislate these risky activities.Given the results of this study, targeted monitoring of the rocky shores of Nuevo Gulf and adjacent areas is needed to determine whether Semimytilus algosus has colonized the study area, presumably at an early stage of the invasion when eradication might still be possible.

Figure 1 .
Figure 1.Specimens of Semimytilus algosus sampled from the fishing vessel.A-E: general aspect; F-G: detail of compact resilial ridge and hinge without tooth.Scale bar A-E: 2 cm, F-G: 1 cm.Photographs by JH Signorelli.