Cover and colonization of commercial oyster (Crassostrea gigas) shells by fouling organisms in San Quintin Bay, Mexico.

ABSTRACT Fouling communities of commercial oyster crops in San Quintin Bay (Baja California, Mexico) were investigated to understand patterns of shell cover, species composition, and colonization. Historically dominated by soft sediment systems, San Quintin Bay currently supports a large oyster (Crassostrea gigas) aquaculture industry. Oyster shells are the main source of hard substratum in the bay, without which fouling communities would be mostly absent. Fouling communities are a nuisance to oyster farming because they result in increased handling time in cleaning and packaging oysters. To investigate the previously undocumented fouling communities of San Quintin, 3 sites within the bay were surveyed for 18 mo (2004 to 2005). Every month between July 2004 and December 2005 samples were deployed and collected so as to obtain shells that had been submerged for either 1, 2, 3, 6, or 12 mo. The majority of the fouling organisms were ascidians, with bryozoans, sponges, hydrozoans, and algae also present. Results show that fouling cover increases with length of time shells were submerged, with an average of ~75% of shell surfaces covered by fouling organisms after 12 mo, the maximum time oysters are grown before harvest. Colonization in the system is variable throughout the year, with ascidian colonization being positively correlated with warmer water temperatures. Several of the species, mostly ascidians, of the fouling community are nonindigenous to the Pacific coast of North America and account for up to 40% of the total fouling cover. Fouling community cover and colonization is similar to what has been documented in other bivalve aquaculture systems. But, because most aquaculture ventures in San Quintin are small, family-based artisanal enterprises, the socio-economic impact of fouling is larger and more difficult to manage. Understanding patterns of fouling cover, colonization, and species outbreaks is necessary to develop feasible rearing solutions that can reduce the impact of fouling.

KEY WORDS: ascidian, Baja California, bryozoan, Crassostrea gigas, fouling, invasive species, oyster, recruitment, San Quintin Bay

INTRODUCTION

Shell fouling of commercial bivalve species has deleterious impacts on product growth, marketability, and profitability (Braithwaite & McEnvoy 2005). Fouling can reduce growth of bivalves caused by decreased water flow or food competition (Enright 1993, Claereboudt et al. 1994, Lodeiros & Himmelman 1996, Pit & Southgate 2003). Further, fouling organisms can cause shell deformities that decrease the marketability of the product (Taylor et al. 1997). Fouling also severely increases the weight and drag on aquaculture installations. The increased labor needed to clean the product and the infrastructure can decreases the profit margin of aquaculture ventures.

San Quintin Bay, on the Pacific coast of Baja California (Mexico), is a shallow lagoon that supports an important artisanal oyster aquaculture industry. Oyster farming is the second largest economic activity in the area after terrestrial agriculture (Aguirre-Munoz et al. 2001). Historically, San Quintin Bay was dominated by soft sediment habitats. The only substratum that was available for the development of fouling communities was the volcanic rock debris that lines the central peninsula of the bay (Barnard 1964). Oyster aquaculture in San Quintin was developed in the 1970s and is practiced with a rope/rack system where oysters are suspended from ropes vertically in the water column for ~12 mo until harvest. The oyster aquaculture industry provides a large amount of novel substrata for the development of fouling communities, mainly in the form of live oysters, oyster shells, ropes and racks. Currently there is no available information on the fouling communities of San Quintin Bay.

During the summer of 2002, the oyster farmers of San Quintin Bay reported an infestation of their oysters and rack systems by an unusual "sponge." A preliminary visit to the study site found the organism in question to be the nonindigenous ascidian Microcosmus squamiger. Oyster farmers reported that this species had been a significant nuisance since 2001, when oyster ropes and shells were first noted to be infested with M. squamiger. Any fouling cover that develops on the shells of oysters is logistically problematic for oyster farmers because each oyster has to be manually cleaned, representing a large labor cost for the small artisanal enterprises of San Quintin. Also, the fouling communities can overgrow the entire shell of the oyster, sometimes causing deformities that decrease the market value of the product (J. Guerrero, pers. comm.). In response to the concerns voiced by the local farmers, and in preparation for future manipulative experiments, shell fouling in San Quintin was examined monthly over 18 mo from 2004 to 2005 to identify the dominant fouling species, and to quantify fouling cover over time, relative cover of different taxonomic groups, patterns of colonization, and dominance of invasive species in the communities.

METHODS

Study Area

San Quintin Bay is a shallow lagoon on the Pacific Coast of Baja California, Mexico (30[degrees]27'N, l l6[degrees]00'W). The lagoon is 54.4 [km.sup.2] and is split into two arms, locally known as False Bay (western subbasin) and Sail Quintin Bay (eastern subbasin) (Fig. 1a). Three sites were sampled (Fig. 1a), which were chosen because they are within the oyster aquaculture lease areas of Juan Guerrero and Ana Salazar, whom provided logistic support. The average depth of the bay is approximately 2 m, with tidal channels not exceeding 10 m in depth (Millan-Nunez et al. 1982, Aguirre-Munoz et al. 2001). Oceanographic trends of the outer coast include strong upwelling currents in the summer, and semidiurnal tide regimes, with a tidal range that can exceed 2 m during spring tides, uncovering upwards of 20% of the bay (Millan-Nunez et al. 1982). There are no significant freshwater inputs to the bay, besides the limited precipitation the region receives each year (~150 mm) during winter rainstorms (Millan-Nunez et al. 1982, Aguirre-Munoz et al. 2001). Salinity values are slightly hypersaline, with ranges from 33 34 ppt at the mouth, to 34-37 ppt in the upper reaches of the bay (Millan-Nunez et al. 1982). Oyster aquaculture leases dominate the western subbasin of the bay (Fig. l b).

[FIGURE 1 OMITTED]

Artisanal Oyster Farming Techniques of San Quintin Bay

The rope/rack system used by most artisanal farmers in San Quintin utilizes old oyster shells hung on ropes as substrata for live oyster growout. Spat is purchased from commercial producers in the United States, and allowed to settle onto oyster shells. After an initial period of subtidal deployment for 2-4 wk, the ropes are transferred to intertidal or shallow subtidal racks where they remain for approximately 12 mo until they are harvested. At harvest they are broken off the substrate shell, and then if necessary, individually cleaned. The intertidal and shallow subtidal racks used are constructed out of PVC tubes and arranged in long rows (lines of >100 racks), with each rack supporting 120 ropes. Thus a large amount of biological (oyster) and man made (racks) hard substrata is available for colonization by fouling species.

Sampling Design

At each site, oyster shells were suspended from ropes for colonization. To examine short-term colonization and long-term community development, shells were deployed according to the following scheme. Every month between July 2004 and December 2005 samples were deployed and collected so as to obtain shells that had been submerged for either 1, 2, 3, 6, or 12 mo. Water temperature data was taken with dataloggers deployed at a seagrass bed centrally located in the bay. Two Ibutton temperature loggers were submerged and replaced every 3 mo.

Data Collection

Every month, sample shells were cut from the racks, and immediately placed in buckets filled with seawater for storage until analysis. Shells were destructively sampled, with each shell representing an independent sample of each treatment for each site. Analysis of shell cover and fouling community composition was conducted as soon as possible alter collection, with time to analysis not exceeding 24 h. For analysis, each sample was placed in a small plastic container (12 x 12 cm) filled with seawater. First, all species were described and vouchered as morphotypes. To quantify cover, a grid with 100 points (points spaced 1 cm apart) was placed over each sample, and at each point the primary space holder was noted.

Ascidians were the dominant species (numerically and abundantly), and were identified to species, and as native or nonindigenous. Species identity was confirmed with the help of taxonomic experts. Other organisms were categorized as morphotypes, and vouchered for future identification to species level.

Data Analysis

Because all of the shells are slightly different sizes, percent cover was calculated as the total number of points fouled divided by the total number of points of the entire shell. Means were calculated across either treatments, or months, depending on the analysis. Because some of the analyses compare treatments with different replication, standard errors were used in all analyses and graphs for uniformity. Statistical analyses were conducted using JMP 5.1 statistical software (SAS Institute). For statistical analyses, all data was first checked for normality, and if assumptions of normality were not met, transformations were conducted (either with a arcsine square root transformation, or with the transformation calculated through the Box-Cox Y transformation in JMP). All data was analyzed with either one- or two-Way ANOVAs, and posthoc tests.

For shell cover analyses "Total Fouling Cover" was calculated as the total percent cover of all fouling species (i.e., any point on the shell that is fouled). For a subsequent analysis, "Total Fouling Cover'" data were split into three taxa groups: "'Ascidians," "Bryozoans," and "Other" fouling species. "Other" fouling species encompasses a diverse group (sponges, hydrozoans, algae, etc), which typically represented a smaller proportion of the total cover. Finally, for the last analysis, "Total Fouling Cover" was split into two groups: "Invasive" species (species positively identified as nonindigenous species), and "Native/Unidentified" species (species which are either native, of cryptic origin, or were not identified).

Colonization was analyzed using the two-month percent cover values per taxa group as a proxy, because one-month values were extremely low in the system (see discussion). Plotted are means across the three sample sites for each month. Also plotted are the average temperatures for the two months that the samples were deployed. A regression was performed of ascidian colonization (=2 mo cover) against the average temperature for the two months the samples were submerged.

RESULTS

Fouling communities of San Quintin are diverse, comprised mainly of ascidians and bryozoans, but other benthic species present included sponges, hydroids, algae, polychaetes, anemones, and native oysters. In total, 13 species of ascidians were found, of which 3 are native, and 10 are nonindigenous (Table 1). Other species present included the invasive bryozoan Water sipora subtorquata/arctuata as well as 6 other bryozoan morphotypes. Also, 8 sponge, 7 algal, lanemone, 1 hydroid, 1 spirorbid polychaete morphotypes, and the native oyster Ostreola conchaphila fouled the commercial oyster shells. Finally, several motile species are associated with the benthic fouling communities including isopods, amphipods, polychaetes, and even fish, which were observed to use the oyster valves as substratum for their eggs. The most conspicuous organisms are ascidians, which often were seen overgrowing entire shells, with some colonies growing to >0.5 m in length, suspended from individual oyster shells. Besides the oysters and aquaculture structures, the only natural substrata available for development of fouling communities are volcanic rocks and rubble that line certain areas of the bay. But most of these rocky substrata are located in the middle to upper intertidal, and are covered mostly by filamentous algae. Hence, the communities that develop on the oyster shells are completely different from the communities that develop on the local hard substrata.

Although there is variation across the months of the survey, total cover of fouling organisnas on oyster shells increased with time submerged (Fig. 2). After being submerged for two months, fouling covered an average of 23% of the shell, increasing to 38% cover after three months submerged, 55% cover after 6 too, and 71% cover after 12 too. Across all treatments there was lower average cover during the winter months of December 2004 to April 2005.

The subsequent analysis to compare cover of different taxa groups (Fig. 3) shows that although there is a significant difference in percent cover across time (P < 0.0001), cover also varies significantly depending on the taxa group considered (P < 0.0001), and there is also a significant interaction between these two factors (P = 0.001) (Table 2). For example, after being submerged for two months, ascidians increased in abundance compared with one month, but is also significantly more abundant that either bryozoans or other taxa groups. Bryozoans and other taxa increase in abundance over time, but never account for as much cover as ascidians do (40% at 12 mo), and both tend to account for approximately the same percent cover (~15% at 12 mo).

Colonization, measured by 2-mo samples, was highest for ascidians, and varied significantly across months of the survey (Fig. 4). Bryozoan colonization, as well as colonization of other species, was on average much lower than ascidian colonization. Colonization was lowest during January, February, and March 2005 concomitant with the lowest water temperatures recorded during the survey. Further analysis showed that there is a significant positive correlation (P = 0.0041) between warmer water temperatures and higher ascidian colonization (Fig. 5).

A total of 11 invasive species were identified in San Quintin (10 ascidian species listed in Table I, and the invasive bryozoan Watersipora subtorquata/arctuata) accounting for 27% of the 40 species and morphotypes of fouling species. These 11 invasive species contributed ~40% of total cover on oyster shells (Fig. 6), making them a large proportion of the average cover for any length of time submerged.

DISCUSSION

The previously undocumented fouling communities on oysters in San Quintin Bay were investigated to determine the extent and variability in fouling and to monitor the population fluctuations of individual species. In the span of 12 mo, the time an oyster is grown before harvest, the majority of the shell is usually covered by fouling species. Fouling communities are diverse and dominated by several species of ascidians, many of which are not native to San Quintin Bay. Any fouling cover has to be manually cleaned before the oysters can be sold. For the artisanal farmers of San Quintin, extensive fouling cover is of concern because it requires more labor for cleaning and because severe infestations cause growth deformities, which reduce the value of their product (J. Guerrero, pers. comm.) and may reduce oyster growth.

[FIGURE 2 OMITTED]

Although to date there is no quantitative information regarding the impact of fouling organisms on oyster growth in San Quintin Bay, it is likely that infestations of fouling species can have impacts on bivalve growth as have been found in other aquaculture systems, for example with giant scallops (Placopecte, magellanicus) (Claereboudt et al. 1994) or silver-lip pearl oysters (Pinctada maxima) (Taylor et al. 1997). Oysters and ascidians are filter-feeding organisms and exploit a common resource because of overlap in the size of particles they filter from the water column. Oysters feed by selecting particles from the water with complex ciliary structures (Ward et al. 1998). Crassostrea gigas filters particles in the range of 2-12/[micro]m, with maximum retention of particles in the 6-8 [micro]m range (Ward et al. 1998, Ropert & Goulletquer 2000). Ascidians feed by filtering particles out of the water with a mucus net, which has a mesh-like structure with pore sizes approximately 0.5 [micro]m in width and 2 [micro]m in length (Sawada et al. 2001, Petersen & Svane 2002), this structure is known to be highly conserved within the Ascidiacea (Flood & Fiala-Medioni 1981). Because the feeding structure of ascidians is nonselective, that is, all the water that is pumped through the siphon is processed through the mucus net, all of the particles larger than ~2 [micro]m will be filtered. Although oysters filter at a higher rate, because ascidians settle on top of the valves they likely have better access to the flow stream, and hence could preemptively filter suspended food particles, especially when in dense infestations.

[FIGURE 3 OMITTED]

Understanding cover and colonization patterns of fouling species is likely to help develop targeted rearing solutions to manage fouling cover. But the oyster fouling communities of San Quintin Bay are temporally variable, making fouling infestation predictions difficult. Variability occurs not only within populations of adult fouling species, but also within the abundance of colonizing species. This variability is the result of temporal and spatial heterogeneity in oyster rearing methods. Spatially, racks are harvested and seeded as whole units, which create a mosaic of racks that have been submerged for different lengths of time. Temporally, oyster shells and other substrata are harvested or cleaned after approximately 12 mo. Hence this regional disturbance selects for species that reach sexual maturity within that time span. This leads to heterogeneity in age and species composition of fouling communities across racks. Because ascidians have a relatively short larval period (hours to days), the propagule pool within the bay is most likely locally produced and mirrors the adult communities that were reproductive. Temporal and spatial variability of available fouling space and adult fouling communities leads to a stochastic production of propagules and heterogeneous development of fouling communities in the bay.

Heterogeneity in colonization rates and adult communities can also be caused by abiotic influences. Water temperature has been found to have strong effects on ascidian colonization (Stachowicz 2002), growth (McCarthy et al. 2007), and mortality (Grosholz 2001). In San Quintin Bay, ascidians colonization peaks are positively correlated with warmer water temperatures. Also, because of the desert terrestrial environment of the San Quintin area there is typically very little rain, and hence no fresh water input into the bay. But some years, there are larger rainstorms, which do result in fresh water run off that might affect the survival of some fouling species.

Ascidians, common components of fouling communities, have been especially successful at establishing populations outside their native range (Lambert 2001). For example, a recent survey of Southern California fouling communities found 13 different species of nonindigenous ascidians, but only 9 native species (Lambert & Lambert 1998). On the Atlantic coast of the United States several nonindigenous ascidians have established themselves as dominant space holders (Carlton 1989, Bullard et al. 2007, Dijkstra et al. 2007). Invasive ascidians have detrimental ecological effects on other filter feeders because of food competition and hence economic effects on filter-feeding aquaculture species (Lambert & Lambert 1998). For example, the clubbed tunicate (Styela clava) has been documented to have severe impacts on mussel rope cultures in Prince Edward Island, Canada (LeBlanc et al. 2003, LeBlanc et al. 2007). Also, the colonial ascidian Didemhum vexillum, a recent invader to the waters of New Zealand, was documented to spread from the hull of a barge and spread to infect commercial mussel lines (Coutts 2002).

The invasion of San Quintin Bay by nonindigenous marine fouling species has two likely sources. First, oyster farmers in San Quintin have introduced other bivalve species from Southern bays to test as possible products. These other bivalves are transported live, and likely have fouling species attached to their shells, which are subsequently introduced to the bay. Because of the rural, artisanal nature of the industry in San Quintin Bay, there is no knowledge of the dangers of translocating species across natural biogeographic boundaries and the subsequent impacts of nonindigenous species. Further, there is little compliance to the minimal existing environmental regulations.

Second, it is likely that some nonindigenous species were transported to the bay on the hull of boats. Historically, before an overland route was built, 19th century missionaries and settlers to the area exported wheat, salt, and other local crops via ships, enough to warrant the construction of a small dock. This ship traffic likely represented the first inoculation of invasive species to the bay. Presently, San Quintin Bay has very little boat traffic, but most boats are recreational sailboats that come from southern California marinas (S. Ibarra-Obando & L. Rodriguez, unpub, data). The fouling communities of San Diego are characterized by having a large percentage of invasive species (Lambert & Lambert 1998, Lambert & Lambert 2003). Hence, the present source pool for species that might be transported via hull fouling to San Quintin is likely mainly nonindigenous.

Microcosmus squamiger, the invasive ascidian which was of main concern to oyster farmers at the start of this study, is a species native to Australia that was likely introduced to the Pacific Coast of Baja California via hull fouling. This species was first reported as an invader to the coast of California in 1986, (Lambert & Lambert 1998) and has since become a dominant member of the fouling communities in Southern California harbors (Lowe 2002). Reflecting the variability in the fouling communities of San Quintin Bay, during this survey M. squamiger was present, but it did not infest the oysters. Microcosmus squamiger is tolerant of a wide range of salinities, has a lifespan of 2-3 y, and a long breeding season (Lambert & Lambert 1998, Lowe 2002). It is possible that the infestation that was observed in 2001 did not have successful propagule production, and because the adults were harvested from the bay, there has not been another population boom in the system. Such population fluctuations have been found for other invasive species as well (Simberloff & Gibbons 2004).

[FIGURE 4 OMITTED]

Solutions to try to reduce the amount of fouling in bivalve aquaculture systems have been tested. For example, in some systems, manual cleaning during growout has been found to be effective if it can be performed on a monthly basis (Enright 1993). Also, acetic acid treatments have shown to be successful in reducing the cover of the invasive ascidian Styela clara (LeBlanc et al. 2007). But, feasible and realistic fouling control solutions will only be successful when they are developed with local farming practices and constraints in mind. For example, the oyster farming enterprise that collaborated with this research typically operates with two workers, one of which is the owner. These farmers work seven days a week, year-round. Because more labor is hard to afford and time is always limiting, a successful management solution to control fouling communities would be one that is low cost, low time investment, and ideally can be easily incorporated into other maintenance or routines already in place. One suggested solution is to monitor fouling communities, and when the population of a fouling species is observed, to immediately target that population (i.e., racks) for maintenance and cleaning to try to remove the biomass of that species before it becomes sexually mature. Although this would likely be labor intensive, because there is low propagule pressure from external sources to the bay, the local reduction of fouling species could ultimately control populations of nonindigenous species. Although eradication is unlikely, populations could be reduced so that deleterious impacts are undetectable.

[FIGURE 5 OMITTED]

[FIGURE 6 OMITTED]

The oyster farmers of San Quintin Bay are continuously concerned with fouling communities, because of the direct impact on labor costs, as well as their belief that the fouling communities might be harming the growth of their crops. This research successfully documents the species composition and cover of the current fouling communities of the bay, specifically the dominant ascidians. Further, this research establishes a baseline knowledge of the species composition of the fouling communities, which will more easily enable the detection, and possible early eradication, of future invaders. Future research is needed to determine effective and feasible fouling control methods. Also, the physiological impact of fouling community cover on oyster growth needs to be investigated. Finally, the economic impact to the oyster farmers needs to be quantified to compare the perceived cost of reduced oyster growth to the actual cost of increased labor.

ACKNOWLEDGMENTS

This article is dedicated to Juan Guerrero and Ana Salazar. This study could not have been possible without their everyday assistance and support. (Este articulo se 1o dedicamos a Juan Guerrero y Ana Salazar, que sin su ayuda este estudio nunca hubiera sido possible.) Miriam Poumian, Susan Williams, Jay Stachowicz and Ted Grosholz also provided invaluable help at all stages of this research. This research was funded by UCMEXUS Research Grant, as well as a National Science Foundation Predoctoral Fellowship. Work in Mexico was conducted under CONAPESCA Permit #260104-613-03.

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LAURA F. RODRIGUEZ (1) * AND SILVIA E. IBARRA-OBANDO (2)

(1) Section of Evolution and Ecology, University of California, Davis, California 95616; (2) Centro de Investigacion Cientifica y de Educacion Superior de Ensenada, CICESE, Km. 107 Carretera Tijuana-Ensenada, Apdo. Postal 360, Ensenada, B.C. Mexico 22860

* Corresponding author. E-mail: [e-mail]

TABLE 1.
List of ascidian species in the fouling
communities of San Quintin Bay.

Native ascidians:
  Aplidium californicum
  Botrylloides diegensis
  Distaplia occidentales
Non-indigenous ascidians:
  Ascidia zara
  Botrylloides perspicuum
  Botrylloides violaceus
  Botryllus schlosseri
  Ciona sp.
  Didemnum sp A
  Microcosmus squamiger
  POI yandrocarpa zorritensis
  Stylea plicata
  Symplegma reptans

TABLE 2.
ANOVA analysis of percent cover of different fouling
taxa groups by months submerged (referring to Figure 3).

Source             DF      SS     F Ratio   Prob > F

Months Submerged    4    0.2744   83.3476   < 0.0001
Taxa Group          2    0.0576   35.0308   < 0.0001
Months Submerged
  * Taxa Group      8    0.0227   3.4533     0.0010
Error              180   0.1481   0.0008