VI.
Nonnative Species

A.
BACKGROUND

The introduction of nonnative species can result in dramatic environmental and economic impacts (Parker et al., 1999; Ruiz et al., 1999). The committee defines nonnative species as those “… that have been transported by human activities beyond their native ranges” (Wonham, 2003). Commonly employed synonyms are exotic or introduced; the definition explicitly excludes natural range extensions. The term invasive is sometimes used as a synonym for nonnative, but it can also carry the implication that the species is especially aggressive in its ability to spread or proliferate in the new environment. In this report, we use invasive in this latter context. Some introductions may go unnoticed, while others may have either negative or positive environmental or economic impacts. Most shellfish mariculture in the United States is based on nonnative species (Goldburg et al., 2001), including the Pacific oyster (originally imported from Japan), which is grown in Drakes Estero and nearby Tomales Bay in California, as well as many other locations worldwide . When examining the potential introduction of nonnative species via mariculture practices, it is important to distinguish between ongoing and historical practices. Oysters are now supplied to DBOC as eyed larvae or spat on shell or cultchless (single) seed that have been certified free of known pathogens and hitchhiking species (Carolyn Friedman, personal observation; Kevin Lunny, personal communication). Clams are supplied as 3–15 mm juveniles and are also certified free of known pathogens and hitchhiking species. It is in this context that we examine the potential of ongoing cul-



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VI. Nonnative Species A. BACKGROUND The introduction of nonnative species can result in dramatic environ- mental and economic impacts (Parker et al., 1999; Ruiz et al., 1999). The committee defines nonnative species as those “. . . that have been trans- ported by human activities beyond their native ranges” (Wonham, 2003). Commonly employed synonyms are exotic or introduced; the definition explicitly excludes natural range extensions. The term invasive is some - times used as a synonym for nonnative, but it can also carry the impli- cation that the species is especially aggressive in its ability to spread or proliferate in the new environment. In this report, we use invasive in this latter context. Some introductions may go unnoticed, while others may have either negative or positive environmental or economic impacts. Most shellfish mariculture in the United States is based on nonnative species (Goldburg et al., 2001), including the Pacific oyster (originally imported from Japan), which is grown in Drakes Estero and nearby Tomales Bay in California, as well as many other locations worldwide . When examining the potential introduction of nonnative species via mariculture practices, it is important to distinguish between ongoing and historical practices. Oysters are now supplied to DBOC as eyed larvae or spat on shell or cultchless (single) seed that have been certified free of known patho- gens and hitchhiking species (Carolyn Friedman, personal observation; Kevin Lunny, personal communication). Clams are supplied as 3–15 mm juveniles and are also certified free of known pathogens and hitchhiking species. It is in this context that we examine the potential of ongoing cul - 0

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 NONNATIVE SPECIES ture of the nonnative Pacific oyster in Drakes Estero as a vector of exotic species. Historical importation of the juvenile Pacific oysters on cultch (large shells) has resulted in the introduction of other species such as the Manila clam (V. philippinarum; Quayle, 1941), now another farmed bivalve, and several pests and parasites into various west coast estuaries (Chew, 1979). For example, the Japanese oyster drill, Ocinebrellus inornatus, was intro- duced to the United States in shipments of Pacific oysters. Nonnative spe- cies have been shown to bring a small proportion of parasites from their native environment to their transplanted location (Mitchell and Power, 2003; Torchin et al., 2003). When these parasites encounter new hosts that lack resistance, they may become pathogenic and cause epidemic disease. Many of the devastating, emerging infectious diseases are attributable to exotic pathogens (Harvell et al., 1999; Daszak et al., 2001). The Pacific oyster has been cultured in Drakes Estero since the 1930s. The following issues require closer examination before the potential of these nonnative oysters to become naturalized in the estero can be identified: • Do the Pacific oysters spawn naturally in Drakes Estero? The exclu- sive use of triploid stock could reduce but would not eliminate successful reproduction and the production of viable, dispersing larvae (NRC, 2004). In addition, unknown numbers of diploid Pacific oysters from previous bottom culture operations may exist loose on the estero’s bottom, a legacy from past on-bottom culture practices. • Is sufficient natural hard substrate available in the estero for oyster establishment in the absence of oyster racks and shells of the cultured oysters? There appears to be limited natural hard substrate within the estero, present mostly at Bull Point, but it is possible that there is enough to support a small population. • Oyster larvae spend 10–30 days or more in the plankton, duration being largely dependent on ambient temperature conditions (Strathmann, 1987). Given the high flushing rate in the mariculture lease areas in Drakes Estero, it is uncertain whether larvae would be retained in the estero in sufficient numbers to sustain a viable adult population. Whether the nonnative oysters would persist or go locally extinct in the absence of DBOC requires answers to these questions. Equally, if the cul - tured oysters spawn successfully, could they serve as a source population, supplying larvae that disperse to other suitable habitats both within and beyond the spatial limits of the estero? The failure of C. gigas to naturalize in Drakes Estero in the past might be considered an unreliable indicator of future naturalization potential given that C. gigas only recently has

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 SHELLFISH MARICULTURE IN DRAKES ESTERO become established in the Wadden Sea, potentially in response to a warm- ing climate, even though the species had been used in mariculture there since the 1960s (Diederich, et al., 2005). Notwithstanding the situation in the Wadden Sea, the combination of factors such as shellfish culture locations within the Estero, hydrography of the system (short residence time), and the lack of suitable natural habitat for settlement (as opposed to habitat associated with oyster culture) might mitigate against the suc - cessful establishment of the Pacific oysters in Drakes Estero. The nonnative Manila clam, V. philippinarum, is also cultivated in Drakes Estero. DBOC currently raises about 1 million individuals (NPS, 2007c) in bags on an acre of intertidal flat, at a density of about 250 indi - viduals per m2. The Manila clam, V. philippinarum was introduced in the mid-1930s and has become naturalized in some estuaries along the Pacific coast. Culture of clams in bags reduces some of the risk of naturalization compared to the method of culturing clams in beds because bags of clams can be readily recovered whereas some of the loose clams in beds could persist for years in a reproductively mature status. Even with bags, there is some risk of release because bags may break and clams may spawn within the bags. If the Manila clam successfully reproduces and estab- lishes populations in Drakes Estero, it may compete with native infaunal suspension-feeding bivalves, but is less likely to compete with Macoma clams which are surface deposit feeders. Any culture bags used to contain Manila clams would provide additional solid surfaces for epibionts (spe - cies that attach to other living organisms). Oyster mariculture provides solid surfaces in the form of the shells of oysters and the structures, such as wooden racks and plastic mesh bags, used in the culture operations. Hard surfaces are attractive to and necessary for the successful settlement of epibionts such as sponges, bryozoans, barnacles, and tunicates. A nonnative compound tunicate, Didemnum vexillum, (Lambert, 2009; Stefaniak et al., 2009) (also referred to in the literature as Didemnum species A or Didemnum sp.) has established a worldwide distribution. It is now a very evident epibiont covering a substantial fraction (up to about half, judging from the committee’s obser- vations made during its September 2008 visit) of subtidal surface space on shell surfaces of living Pacific oysters and on associated oyster-rearing gear in Drakes Estero and is also common in nearby Tomales and Bodega Bays. It is reported to have colonized the limited natural solid mud and sandstone substrates and rocks at Bull Point in Drakes Estero (Dixon, 2007; NPS, 2007c, 2007d). Finally, three more nonnative epibiotic species, the bryozoans Schizoporella unicornis and Watersipora subtorquata and the sponge Halichondria bowerbanki, have been recorded on oyster culturing gear in Drakes Estero (Elliott-Fisk et al., 2005).

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 NONNATIVE SPECIES B. WHAT IS THE BODY OF SCIENTIFIC STUDIES ON THE IMPACT OF THE OYSTER FARM ON DRAKES ESTERO? While numerous publications identify the extent to which nonnative species have invaded suitable marine habitats in California (Carlton, 1979, 1985; Carlton et al., 1990; Cohen and Carlton, 1998; Foss et al., 2007; Hhttp://www.dfg.ca.gov/ospr/about/science/misp.html), only one peer-reviewed publication (Byers, 1999) specifically addressed non - natives in Drakes Estero. Byers examined the effect of the introduced mud snail, Batillaria attramentaria, on the native mud snail, Cerithidea cali- fornica, and found an interaction that could be detrimental to the native species. The nonnative mud snail is present in high intertidal salt pannes in Schooner Bay but “. . . remains very restricted” (Byers, 1999) in distri- bution for unknown reasons. In the study on infaunal invertebrates by Harbin-Ireland (2004), no nonnative invertebrate species were identified in unconsolidated sediment adjacent to the oyster racks in Drakes Estero. Unfortunately, one cannot conclude that nonnative infaunal invertebrates are absent from or even rare in Drakes Estero because of the limited spa - tial and temporal sampling and low degree of taxonomic resolution—of the taxa collected, fewer than 30% were identified to the species level. Little research has been conducted within Drakes Estero on nonnative organisms, whether introduced as a result of importations of the Pacific oyster, or by some other mechanism. For example, although several stud- ies surveyed California embayments for presence of the Japanese oys - ter drill, Ocinebrellus inornatus, the published literature does not include Drakes Estero among the sampling sites. Thus, there are no published reports indicating presence of the Japanese oyster drill in Drakes Estero (e.g., Carlton, 1992). The owners of DBOC, Kevin and Nancy Lunny, also indicated that they and their workers have not seen oyster drills in the estero (Kevin and Nancy Lunny, committee tour of DBOC on 9.5.2008). Additionally, all importations to Drakes Estero of C. gigas on cultch were examined for the Japanese oyster drill by the California Department of Fish and Game at the point of delivery prior to issuance of a Planting Certificate. In the early 1990s, health examinations were conducted on seed and adult oysters (both with a sample size of 60) from Matsushima Bay, Japan, that were destined for importation into Drakes Estero. Follow- ing the observation of a haplosporidian parasite in the oysters, additional samples were collected from Japan and from several areas in Drakes Estero (e.g., Home Bay, Berries Bar). The latter samples were collected for several years (1990–1993) for histological examination and, later, molecu - lar analyses (Friedman et al., 1991; Friedman, 1996; Burreson et al., 2000). In the early 2000s, a single sample of Pacific oyster seed from Drakes Estero was examined for the presence of an oyster herpes virus (see

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 SHELLFISH MARICULTURE IN DRAKES ESTERO below). The oyster herpes virus has been observed in many coastal areas globally where Pacific oysters are cultured or native, including Tomales Bay and Drakes Estero, California, which are the only two known loca - tions in the United States where this virus has been documented (Hine et al., 1992; Nicolas et al., 1992; Friedman et al., 2005; Kimberly Reece, unpublished data). C. WHAT EFFECTS CAN BE DIRECTLY DEMONSTRATED BY RESEARCH CONDUCTED IN DRAKES ESTERO ITSELF? As noted above, prior owners of the oyster farm (Johnson Oyster Company) imported seed on cultch directly from Japan for many years until the early 1990s. Microscopic and molecular examination of oysters revealed the presence of the pathogen, Haplosporidium nelsoni, which may have been introduced into Drakes Estero with Pacific oyster importations from Matsushima Bay, Japan (Friedman et al., 1991; Burreson et al., 2000). Haplosporidian infections were observed in adult and seed Pacific oys- ters destined for importation into Drakes Estero from Matsushima Bay, Japan, in 1989 and 1990 (Friedman et al., 1991). Although importations from Japan ceased, one to three percent of the Pacific oysters sampled from Drakes Estero between 1990 and 1993 had mild systemic or localized infections with haplosporidia, indicating that the parasite had become established in Drakes Estero (Friedman, 1996). No haplosporidia were observed in oysters from Tomales and Humboldt Bays in California. These protists appear to have been established at very low levels in domestic stocks of Pacific oysters reared in Drakes Estero, California, during the period of study in the early 1990s. A sampling of oysters from Drakes Estero in 2006 suggests that a low level (<1%) of H. nelsoni infection per- sists (J. Moore, CDFG, personal communication 4.6.09). There is currently a Memorandum of Understanding between DBOC and the California of Fish and Game that states that all oysters from Drakes Estero shall go to terminal markets and not be planted in any other waters of the state or be held in tanks that drain into waters of the state (T. Moore, CDFG, personal communication 4.7.09). Currently, DBOC imports eyed larvae from two U.S. West Coast hatcheries (Whiskey Creek Shellfish Hatchery in Tillamook, Oregon, and Coast Oyster Company in Quilcene, Washington) that participate in a High Health Program (see Appendix E). As directed by the California Department of Fish and Game, all importations require annual health examinations in which at least 60 individuals of both larvae and adults from each facility are examined (Jim Moore, personal communication).

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 NONNATIVE SPECIES D. WHAT EFFECTS CAN REASONABLY BE INFERRED FROM RESEARCH CONDUCTED IN SIMILAR ECOSYSTEMS? Oyster Parasites Introductions are often the primary cause of diseases that drive for- merly common species to low levels (Lafferty and Gerber, 2002). For example, the introduction of Haplosporidium nelsoni, which may have been introduced with importations of infected Pacific oysters from Matsushima Bay, Japan, where this disease agent is endemic, resulted in catastrophic losses of the native eastern oyster along the mid-Atlantic coast (Friedman et al., 1991; Burreson et al., 2000; Burreson and Ford, 2004). Unlike the eastern oyster, Pacific oysters, which appear to have co-evolved some level of resistance to H. nelsoni, do not experience epidemic losses when infected with this parasite. DBOC currently imports High Health eyed larvae of the Pacific oyster (i.e., from one of two West Coast hatcheries that are tested for diseases and pathogens annually; K. Lunny, personal communication) and sells their products directly to a terminal market. Thus, the potential introduction of disease is limited to those that infect larvae and those that go undetected in annual examinations. A disease agent, the ostreid herpes virus (OsHV), which causes catastrophic losses of both larval and seed oysters (Renault et al., 1995; Burge et al., 2006, 2007), has been observed in Tomales Bay (Burge et al., 2005; Friedman et al., 2005). The presence of OsHV nucleic acid has been detected in Drakes Estero oysters by polymerase chain reaction (PCR) analysis (Burge and Friedman, unpublished). This patho- gen was lacking from all other U.S. regions examined, including juvenile oysters produced by the two hatcheries that provide larvae to DBOC (Friedman et al., 2005). Despite the PCR evidence of OsHV in Drakes Estero oysters, no associated oyster losses have been reported, whereas significant losses have occurred in nearby Tomales Bay (Burge et al., 2006, 2007). The origin of this virus is unknown, and there is no evidence of its introduction with regionally imported oysters (Friedman et al., 2005). Nonnative Invertebrates Affiliated with Oysters Understanding the threat posed by the invasive tunicate D. vexillum requires data on how it reproduces, its capacity to spread spatially and how it interacts with other benthic fauna and flora resident in Drakes Estero. Although it cannot grow on the sandy and muddy unconsol- idated sediments that predominate in Drakes Estero, D. vexillum has recently been reported colonizing eelgrass blades at presently low lev-

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 SHELLFISH MARICULTURE IN DRAKES ESTERO els in Tomales Bay (Susan Williams, personal communication; Benjamin Becker, personal communication). Its rapid growth and competitive over- topping abilities make it an ecological threat to many native and nonna- tive invertebrate taxa (Osman and Whitlatch, 2007; Mercer et al., 2009), as well as a nuisance potentially interfering with oyster cultivation and production activities. D. vexillum can reattach if fragmented (Bullard et al., 2007), thereby expanding asexually the presence and dispersal poten- tial of the species. Commercial cleaning of fouled oysters and associated materials used to grow the shellfish, as now practiced by DBOC, could promote asexual spread of the species. Sexual reproduction in didemnid tunicates produces a dispersing larva spending “. . . a few minutes or several hours. . . .” in the plankton (Strathmann, 1987), a short time that would severely limit larval dispersal. The biological requirements of D. vexillum suggest that it could neither flourish nor persist in the absence of the hard surfaces provided by oysters and oyster racks. Carman et al. (2009) found that shellfish and marine plants such as eelgrass were more likely to be colonized by tunicates when in close proximity to hard sub - strates, such as docks and shellfish aquaculture gear. The recent observa - tions of eelgrass blades colonized by D. vexillum in Tomales Bay should drive further detailed research. In summary, movement of oysters has resulted in the introduction of nonnative species including disease agents with varying impacts. Histori- cal importations on cultch (wild-caught juvenile oysters on large oyster shells) from Japan are associated with the introduction of several nonna - tive species. Current practices of DBOC, in which they import larvae, min- imize the risk for introduction of diseases and eliminate risk of external hitchhikers, like oyster drills, as long as the company continues to import larvae from local hatcheries that participate in a High Health Program. Both Whiskey Creek Shellfish Hatchery and Coast Oyster Company, cur- rent sources for DBOC, participate in a High Health Program (R. Elston, personal communication). Given the relatively high level of control, for larvae and young seed, coupled with annual health examinations, the risk of introducing unwanted exotic species is low, although the protections against nonnative introductions currently in place are not mandated.