Epifauna Associated with the Asian Green Mussel Perna viridis (Mytiloida: Mytilidae) in Cienfuegos Bay, Cuba  

Alexander Lopeztegui - Castillo1 , Adriana Artiles - Valor1 , Yuliesky Garcés - Rodríguez1 , Roberto - Castelo Báez1 , Ninieska Castro - Graña2
1. Fisheries Research Center, 5th. Ave. and 246, Barlovento, Playa, Havana, Cuba
2. Fishery of Cienfuegos, Fertilizers Street, Industry Zone Number 2. Obourke, Cienfuegos, Cuba
Author    Correspondence author
International Journal of Marine Science, 2014, Vol. 4, No. 14   doi: 10.5376/ijms.2014.04.0014
Received: 28 Nov., 2013    Accepted: 29 Dec., 2013    Published: 02 Feb., 2014
© 2014 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Lopeztegui - Castillo et al., 2014, Epifauna Associated with the Asian Green Mussel Perna viridis (Mytiloida: Mytilidae) in Cienfuegos Bay, Cuba, International Journal of Marine Science, Vol.4, No.14: 134-142 (doi: 10.5376/ijms.2014.04.0014)


In this study we explored the species composition, space and temporary variations of the epifauna associated with the invasive species Perna viridis (Asian green mussel) in Cienfuegos Bay. Epifauna was collected by scraping shells surface of 577 P. viridis individuals extracted from four sites where greater abundance: the wharves Pablo Guzmán (PG), Siete Cuadras (M7), Punta La Cueva (PC), and the Barco Hundido (BH). The first three sites were located near to human population establishments while BH was relatively far from such establishments. Barnacles (Cirripedia) were the most important group among sampled epifauna, followed by bryozoans and ascidians. Other groups as sponges, anemones, polychaetes, non-sessile crustaceans like brachyurans and anomurans, turbellaries, ophiuroids, bivalves and gasthropods, were also represented. A total of 39 species were identified as components of epifauna, which coexist naturally with mussels without demonstrating ecosystem affectations or mutual exclusion effects (displacement of species). The total biomass values decreased from February to May and increase toward November at all sampling sites. Significant differences were found for the main groups of the epifauna when comparing on temporal scale. Total biomass values showed significant differences on spatial scale. BH was the site with less value, only vegetal elements were found. Those differences could be related with anthropogenic impact, which is greater near to human population establishment (Cienfuegos City). The information providing by this study seems to be against the hypothesis that P. viridis represents an ecological damage in Cienfuegos Bay at least for the current mussel densities, but it is not enough to reject that hypothesis.

Perna viridis; Asian green mussel; Invasive species; Cienfuegos Bay

As expressed in the Convention on Biological Diversity (2002), an exotic species could be considered as invasive when its propagation threats ecosystems, habitats or other species, and consequently produces socio-cultural, economic, environmental or human health damages. The presence of exotic or invasive species usually causes changes on ecosystem dynamics to which they integrate (Ruiz et al., 1997; Albins and Hixon, 2008). Commonly, these changes imply a negative impact based on the displacement of species or the broken balance on predatory relationships. However, the spread of exotic or invasive species sometimes do not significantly affect the ecosystems or could even be profitable for them. That is mainly due to their bioengineering character (Kelaher et al., 2007; Darrigran and Damboreana, 2011) or their assimilation for certain substances like hydrocarbons (Núñez et al., 2010).  

Asian green mussels Perna viridis (Linnaeus, 1758) are thought to have been accidentally introduced in Cienfuegos Bay through the ballast water or biofouling of international commercial ships, similar to what is known to have occurred in other regions of the Caribbean (Carlton and Hodder, 1995; McGuire and Stevely, 2009). When the first scientific report of this species took place (Fernández-Garcés and Rolán, 2005), density was already up to 18 000 individuals per square meter. After eight years, studies on mussels have been focused in abundance and distribution pattern (Lopeztegui-Castillo et al., 2014), and the use of mussels as bio monitoring organochlorine pesticides (Alonso - Hernández et al., 2012) and Polycyclic hydrocarbons (Vega - Bolaños et al., 2014) and heavy metal concentrations in the body tissues, as well as their microbiological quality (Martínez et al., 2014). Recently, another research about the survivals of mussels has been developed. Unfortunately, most of these studies are now in press or have not been published yet.
Similarly to what happened in Florida (Benson et al., 2001; McGuire and Stevely, 2009), Asian green mussels population has continued to spread quickly in Cienfuegos Bay and economic problems have resulted because of mussels growth at pipes of the local power plant “Carlos Manuel de Céspedes”. Nevertheless, the biology of mussel has not been studied yet for this new habitat and there is a lot of speculation, but little has been demonstrated about the ecological impact of that species in the bay. In Venezuela, for instance, has been proved that the dominance of P. viridis on certain ecosystems causes negative impacts and makes decrease the diversity (species richness) and the system productivity (Fernández and Jiménez, 2007). The knowledge about the damages that P. viridis could cause to biodiversity and to the ecosystems dynamics in Cuba is urgent and vital, even more when this species has been recently reported also in Mariel Bay (Lopeztegui et al., 2013), at the north - west of Cuba . It exist a big project on exotic invasions that includes several species, plants and animals that are carefully observed and handle in our country, directed by CITMA and CNAP (Environmental and Technological Research Agency and National Centre for Protected Areas, abbreviations are respectively from Spanish), a Cuban organization that regulates and design this kind of policies. The Asian green mussel is one of those species.
In the case of Cienfuegos, this topic requires particular attention because of the high contamination levels due to the anthropogenic action. This contaminationdeteriorates general conditions in the Bay and it is reflected in loss, decrease or displacement of species (Rey-Novoa, 2004). Those events could be facilitated by the current presence of mussels. The aim of this study was to determine the composition by groups and space-temporary variations of the epifauna associated to P. viridis in Cienfuegos Bay. Based on this, the ecological impact of mussels in the Bay could be partly inferred.
1 Results
1.1 Qualitative composition of epifauna associated to P. viridis
Both biomass and occurrence frequency (on spatial and temporary scale) were highest for Barnacles. This group represented about 90 % of total biomass justly because it was the most numerous group. Balanus eburneus (Gould, 1841) was the best represented species. Although in November nor ascidians or bryozoans where found at PG and M7, in February and May those groups followed the barnacles in order of importance based on the biomass values (Figure 1).



Figure 1 Biomass percentages of the main groups of epifauna associated to the Asian green mussel Perna viridis in Cienfuegos Bay.


The bryozoans were represented by three species belonging to the families Smittinidae (Levinsen, 1909), Membraniporidae (Busk, 1852) and Bugulidae (Gray, 1848). Bugula neritina (Linnaeus, 1758) was the species of highest biomass and occurrence frequency. The ascidians were represented by three species belonging to the families Ascidiidae and Styelidae. In this case, the occurrence frequency was similar for the three species. The highest biomass was Phallusia nigra (Savigny, 1816).
Less represented in the three wharves were some other groups such as sponges, anemones, polychaetes, amphipods, not sessile crustaceans (e.g. brachyuran and anomuran), turbellarians, ophiuroids, and other mollusks such as gastropods and bivalves.All identified species or groups are listed on Table 1.



Table 1 List per sites of epifauna species (or groups) associated to the Asian green mussel P. viridis in Cienfuegos Bay. 

Note: Mussels were the cleanest (with no epifauna associated) at BH site. Only vegetal elements were registered as components of associated community. NI: not identified. *: mollusk species reported by Diaz-Asencio et al. (2005) in similar sites of this bay. 


1.2 Temporary variations of the biomass of epifauna associated to P. viridis
The total biomass values decreased from February to May and increase toward Novemberat all sampling sites (Table 2). Significant differences were found for the main groups of the epifauna. However, not significant differences were detected between months when comparing the total mean values (Figure 2). Based on the biomass of epifauna associated to each mussel, it was demonstrated that May shows a lower mean value (1.13 g/m). February and November show 1.77 g/m and 2.81 g/m respective values.



Table 2 Total biomass (g) per sites and months of the biological community associated to the Asian green mussel P. viridis in Cienfuegos Bay. At BH (Sunk Boat) only vegetal elements were registered.



Figure 2 Biomass per months of epifauna associated to the Asian green mussel P. viridis in Cienfuegos Bay. SD: standard deviation.


1.3 Spatial variations of the biomass of epifauna associated to P. viridis
In spatial scale, the applied ANOVA detected differences (p<0.05) being BH the site where the total biomass value was significantly less (Figure 3). At that site the associated biomass was constituted by vegetal elements only. Biomass of epifauna associated to each mussel at the other sites had the following mean value: 2.74 g/m at PG, 4.31 g/m at M7 and 1.77 g/m at PC.

Figure 3 Figure 3 Biomass per sites of the epifauna associated to the Asian green mussel P. viridis in Cienfuegos Bay. SD: standard deviation.


At PC wharf, the species richness was the least (S=17). However, at the sampled piles there were several species characteristic of relative clean waters, which were not registered in the rest of the sites. These species were found cohabiting with P. viridis, but not as epibiontes. This is the case of several individuals of lion fish, Pterois volitans (Linnaeus, 1758), spiny lobster juveniles, Panulirus argus (Latreille, 1804), crab Menippe mercenaria (Say, 1818), and some gastropods such as Melongena melongena and Cerithium atratum. The species richness of the associated epifauna for PG and M7 warves, presented values of S=28 and S=33 respectively. Species richness for total area sampled in the bay it was S=39.

2 Discussion
The epifauna associated to P. viridis is not too much diverse (almost 40 species only) but dominated by few groups such as barnacles, bryozoans and ascidians. In a study regarding only the malacological fauna associated with Asian green mussel in Araya Peninsula, Venezuela, 50 species were reported (Villafranca and Jiménez, 2004). Based on the occurrence frequency on temporal scale, barnacles, as well as polychaetes and braquiuran (of less biomass), appeared in the 100 % of samplings. These groups could be classified as constants. Although no significant differences were found when comparing the total biomass values between sampling months, the main groups showed significant differences. In November, bryozoans and ascidians were seen surrounding mussels but they were not found on mussels shells (they did not contributed to the biomass). This fact might be related to the salinity decrease reported for that month (Garcés et al., 2012).
In the spatial scale, significant differences were found on total biomass values because of mussels at BH, the site far away of the Cienfuegos City (source of contamination and eutrophization), were cleanest. It is possible that variations in the abundance of all these epifauna groups were influenced by nutrients concentration or other characteristics of the circulating waters such as dissolved oxygen, pollutant agents or salinity variations. The North lobule of the Bay has more antropic influence and hence a highest level of eutrophization (Díaz-Asencio et al., 2005; Seisdedo, 2006), which could facilitate the development not only of Asian green mussels but also of the associated fauna. Both, total biomass and biomass of epifauna associated to each mussel were greater at those sites (PG and M7) near to Cienfuegos City. Based on the information given by specialists of the local environmental office, the city of Cienfuegos contributes the most to the bay contamination with around 1936 tons of BOD (biochemical oxygen demand) per year (C Baute-Álvarez pers. comm. March 4, 2013).
Generally, the sites in which Asian green mussels have been reported as an invasive species are considered trophically enriched. The source of such enrichment could be mainly antropic, like in Bays (Buddo et al., 2003) or natural due to any upwelling process (Villafranca and Jiménez, 2006). Such sites could then be identified, for the Caribbean and Central Atlantic region as ¨high risk sites¨ to be invaded by P. viridis or other species with similar characteristics; mostly if these sites were exposed to high boats traffic. Other bays in Cuba could be some of these ¨high risk sites¨. The high growth rate of Asian green mussel is related to a high filtration rate of organic material, and so its development is favored in those environments trophically enriched (Hawkins et al., 1998).
Polychaetes semi-sessile forms eventually may not appear within the sampling units or even escape when removing mussels. That is why further analysis is recommended in future studies especially designed to find out all this non-sessile forms. Liñero-Arana (1999) reports at least 11 species of polychaetes associated to P. viridis in Araya peninsula, Venezuela. In this study, only six species belonging to families Nereididae, Syllidae, Sabellidae, Terebellidae y Cirratulidae, were present. Some of this species have been associated to soft sediments with organic material accumulations (Díaz-Díaz et al., 2009).
Specimens of P. viridis and I. alatus were seen cohabiting in many sampling times. Although this study does not provide enough evidences to discard at all the possibility that both species could compete for substrate, the hypothesis of mutualism seems to be more plausible at least for the current mussel densities. It was well established that other mollusks (bivalves or gastropods), as well as barnacles, sponges, sea squirts and bryozoans, grow and develop together with mussels without noticeable stressful effects. The species richness values ​​recorded in the PG and M7, added to what was found in PC regarding the characteristics of the members of the epifauna associated to P. viridis, suggest a little or no exclusive ecologicalinteractions.
After more than eight years of the first report, the mussels in Cienfuegos bay cohabit with other 39 epifauna species, many of which were also observed in areas devoid of mussels inside the bay. More than 50 % of the mollusks species that were found have existed for several years in the coastal area of ​​the bay, particularly in the same biotopes where P. viridis are currently reported (Díaz-Asencio et al., 2005). Most of the species that make up the remaining percentage (not found in the present study but reported by those authors) are species characteristic of certain biotopes not sampled because they are not invaded.
Irregularities created by shells when mussels are developing, serve up as shelter for other species that sit or crawl on them, thereby increasing the diversity of associated biological community. A similar result was obtained by Villafranca and Jiménez (2004, 2006), studying the mollusk communities associated to P. viridis in Araya peninsula, Venezuela. Those authors also argument that the retained water between mussels, and feces and pseudofeces depositions around them, stimulate trophic enrichment and increase abundance and diversity of associated species. From this point of view, P. viridis might acts as an engineer species as well as can be seen with the mussel Limnoperna fortunei (golden mussel) in southern South America (Darrigran and Damborenea, 2011). One of the three barnacle species (Amphibalanus reticulatus) has been reported for first time for Cuban waters (Lopeztegui and Varela, 2012); it was found fixed on mussels shells.
The information providing by this study seems to be against the hypothesis that P. viridis represents an ecological damage to the ecosystem, but it is not enough to reject that hypothesis. Maybe the mussel density at the sampled year, around 156 ind/m2 (Lopeztegui - Castillo et al., 2014), was not great enough to cause a significant negative impact on ecosystem. A negative environmental impact including species displacement has been reported in Florida, but mussels densities are up to thousand individuals per square meter (Baker et al., 2002; Baker et al., 2007; McGuire and Stevely, 2009). A similar situation has been described for Venezuela, where this species has become in a fishery product (Penchaszadeh and Vélez, 1996; Segnini et al., 1998; García et al., 2005). Obviously, if there is not statistical comparison between invaded and non-invaded areas, and if there is not routine monitoring, then there is no way to ensure if and how those associated species were affected by mussel presence. Nevertheless, the present study contributes to create a base line on that topic and helps to identify objectives for future studies.
3 Materials and Methods
Cienfuegos Bay is located in the central part of the southern coast of Cuba.Its centre is nearby at 22°08´04.5´´ N and 80°28´50.4´´ W. The total surface area is 88.46 km2 and a mean depth of 9.5 m, which determine a mean volume of 810 millions of m3. The Bay is oriented from NW to SW, with a maximum longitude of 19 km, and a maximum wide of 7.5 km. It is naturally divided in two lobules, commonly known as North and South lobules (Muñoz-Caravaca et al., 2008; Seisdedo and Moreira, 2007). To collect the associated epifauna, mussels were extracted from four sites registered as those with greatest relative density (Lopeztegui - Castillo et al., 2014), they were all situated in the North lobule of the Bay (Figure 4).



Figure 4 Location of the four sampling sites for Asian green mussels Perna viridis and associated epifauna: 1-) Pablo Guzman wharf (PG), 2-) Siete Cuadras wharf (M7), 3-) Punta La Cueva wharf (PC), and 4-) Sunk Boat (BH).


Sampling was carried out on February, May and November, 2011. Those months are characteristic of dry season (February) and rainy season (May) while November is a transition month between these two main seasons in our country. Besides, Temperature, Dissolved Oxygen and salinity for Cienfuego´s Bay was previously reported for that period (Garcés et al., 2012). The collection of Asian green mussels was made manually by free or autonomous (SCUBA) diving. At Pablo Guzmán (PG) and Siete Cuadras (M7) the substrate consisted of a series of metallic pilings. At Punta Las Cuevas Wharf (PC) the pilings of the wharf are made of concrete. Mussels at these three sites were collected from pilings, between 1-3 meters of depth. The BH site was a sunk metal boat at a depth of 1.5 meters; mussels were colleted form the hull of the boat. AtPG, M7 and BHthe existent plain surfaces allowed the use of a quadrat of 25 × 25 cm (0.0625 m2) as unit sample. It was placed randomly three times at the same depth and specimens inside were collected each time. In PC sampling was done from piles. In that case, specimens of three different piles were extracted each time. The epifauna associated to each mussel was collected by scraping the shell surface (valves). The obtained sample was fixed in neutralized formaldehyde solution (4%) and stored in plastic bags previously tagged. Visual monitoring around P. viridis was also considered.
Epifauna were collected from a total of 577 individuals as it is shown in Table 3. The organisms (those classified as megabenthos, > 4 mm) were identified under the stereoscopic microscope with the help of taxonomic literature (Abbott, 1974; Williams, 1984; De Jong and Coomans, 1988; Espinosa et al., 1994; Mikkelsen and Bieler, 2008) and taking in account the criteria of different specialists.



Table 3 Number of Perna viridis collected each month at each sampling site. 


The species richness values (S=number of species) was estimated for Asian green mussels epifauna associated, by sites and for the bay. Wet biomass values were also determined, by using a technical balance (±0.01 g). In every case they were normalized by mussel quantity and were expressed as grams of biomass per mussel (g/m). Those values were compared among sites and months by a unifactorial ANOVA, using post-hoc Fisher LSD test (F, p≤0.05) in order to know between which pairs significant differences were established.
The authors want to thank Gema Hidalgo, Norberto Capetillo, José Espinosa and Carlos Varela for their help identifying organisms. Also we want to express our gratitude to colleagues from Fishery of Cienfuegos (EPICIEN) because of the logistic support for sampling and to Johanna Fernández for the supplied literature. We really appreciate the helpful comments of anonymous reviewers that improved the quality of the manuscript.
Authors’ contributions
ALC conceived and design the study. Also collected the mussels, classified most of the species and drafted the manuscript with AAV. YGR, NCG and AAV processed and analyzed the data. RCB collected and conserved the epifauna, and made biomass determinations. All authors took action in cruises and also all of them read and approved the final manuscript.
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