The Olympia Oyster Ostrea lurida: Recent Advances in Natural History, Ecology, and Restoration Author(s): Catharine Pritchard, Alan Shanks, Rose Rimler, Mark Oates and Steven Rumrill Source: Journal of Shellfish Research, 34(2):259-271. Published By: National Shellfisheries Association DOI: http://dx.doi.org/10.2983/035.034.0207 URL: http://www.bioone.org/doi/full/10.2983/035.034.0207

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THE OLYMPIA OYSTER OSTREA LURIDA: RECENT ADVANCES IN NATURAL HISTORY, ECOLOGY, AND RESTORATION

CATHARINE PRITCHARD,1,2* ALAN SHANKS,1 ROSE RIMLER,1 MARK OATES1 AND STEVEN RUMRILL1,3 1University of Oregon, Oregon Institute of Marine Biology, 63466 Boat Basin Road, Charleston, OR 97420; 2Oregon Department of Fish and Wildlife, 2040 SE Marine Science Drive, Newport, OR 97465; 3Penn State University, Department of Ecosystem Sciences, University Park, PA 16802

ABSTRACT This article reviews recent literature on the biology of Ostrea lurida, emphasizing information that has arisen subsequent to BakerÕs review in 1995. The review highlights recent work that contributes to improvements in restoration efforts. Included are sections on phylogeny, reproductive biology, shell morphology, harvesting, associations with other organisms, threats to recovering populations, ocean acidification, and larval supply, settlement and recruitment.

KEY WORDS: Olympia oyster, Ostrea lurida, native oyster, oyster reef restoration

The Olympia oyster Ostrea lurida (Carpenter, 1864), is the One of the most important services bivalves provide is filter only native oyster occurring along the western coast of the feeding. They sequester toxins such as pesticides, polychlori- United States with a historical distribution from Baja Califor- nated biphenyls (PCBs), heavy metals, and even coliform nia to Sitka, AK (Dall 1914, Coen et al. 2000). The current bacteria from agricultural waste during filter feeding (Alzieu range of O. lurida is estimated to be up to 40% smaller than its 1998, Aune et al. 1998, Scott et al. 1998, Nice et al. 2000, historic range, with the southern limit now near Bahia San Dumbauld et al. 2001). They can provide long-term storage of Quintin, Baja California, Mexico and the northern limit near pollutants by their incorporation into shell or pseudofeces, Queen Charlotte Island, British Columbia (Gillespie 2009). which become buried in the substrate. As filter feeders, they also Additionally, the health of O. lurida populations along the facilitate nutrient cycling between the pelagic and benthic majority of the Pacific Northwest have been classified as either environments and improve water quality (Newell 2004). Very poor (90%–99% lost) or functionally extinct (>99% lost), with few current populations still occur at historic abundances, and the exception of healthy populations in British Columbia (Beck little empirical information exists on how communities de- et al. 2011). Mainly confined to estuaries and sheltered waters, pendent on oyster beds have changed. However, the hypothet- O. lurida (Cook et al. 2000) is found both intertidally and in ical benefits provided by these oysters are clear. If ecosystem shallow, subtidal, euryhaline waters. It has been reported as health in Pacific Northwest estuaries are a goal, restoration of deep as 71 m (Hertlein 1959), and appears to be more tolerant of healthy Ostrea lurida populations may be one tool to help full strength seawater than of freshwater (Gibson 1974). For achieve this goal. a comprehensive compilation of O. lurida populations, see Baker (1995). PHYLOGENY As with other bivalves capable of producing dense aggrega- tions, healthy populations of Ostrea lurida could likely contrib- Until recently, some considered Ostrea lurida to be one ute considerably to the health of the ecosystem in which they species whose distribution extended from Alaska to Central live. They form reefs that provide habitat and help prevent America, whereas others separated O. lurida from its southern shoreline erosion, are important in food webs, and promote sister species, Ostrea conchaphila, which occurs as far south as biodiversity. They also provide environmental heterogeneity Panama (Polson et al. 2009). The characteristics of the shell and thus refuge for many invertebrates and larval fish (Burrell shape of O. lurida led, at one time, to the distinction of three 1986, Baker 1995, Posey et al. 1998, Breitburg et al. 2000, Coen different forms of the species: f. rufoides, f. expansa, and f. & Luckenbach 2000, Lenihan et al. 2001). Little historic laticaudata, which may have been instrumental in splitting the information, however, is available on the faunal communities species into two distinct species, O. lurida and O. conchaphila supported by healthy O. lurida reefs, and even less is known (Arakawa 1990). In 1985, however, O. lurida and O. conchaphila about reef depth, density of reefs, and where they occurred were merged based on morphology (Harry 1985), but recent naturally in both subtidal and intertidal environments. In genetic work indicates that the two species are indeed separate experimental manipulations, Crassostrea virginica has been members of Ostrea (Polson et al. 2009). The approximate point used more frequently to understand their importance in eco- of separation is Baja, CA; O. lurida occurs north, whereas system functioning. Coen and Luckenbach (2000) provide O. conchaphila occurs south. a comprehensive review in Section 4, Ecology of Oyster Reefs. Within Ostrea lurida, as it is now recognized, there appear to It is likely that on the West Coast, O. lurida may have be isolated populations along the Pacific Northwest. Five historically provided these same ecosystem services. genetically distinct metapopulations (Vancouver Island, Puget Sound, Willapa/Coos Bay, Yaquina Bay, and California) were recently identified, and genetic and geographic distances were *Corresponding author. E-mail: [email protected] related in most cases (Stick 2011). However, it was unclear if the DOI: 10.2983/035.034.0207 divergence in the current genetic structure of the populations

259 260 PRITCHARD ET AL. was naturally or anthropogenically induced, with the exception sampled contained eggs, whereas most other oysters sampled of the Willapa Bay and Coos Bay population. (O. lurida is appeared to be developing ripe gonads (Dinnel et al. 2009). In suspected to have been moved manually from Willapa Bay to June, 1 in 18 sampled oysters had larvae in the mantle cavity, Coos Bay.) As adaptations to local conditions may have and other oysters were in various stages of gamete development. contributed to this genetic divergence, it may be important to In August, however, no oysters (n ¼ 12) had larvae or eggs, and understand how the genetic structure of seed oysters transferred most appeared to have decreased gonad sizes, suggesting the from one location to another during restoration efforts in- termination of the reproductive season. These data suggest the fluences their success in restoration efforts (Stick 2011). reproductive period may occur during a short (;2–3 mo) Characterizing the genetic structure of local oyster popula- window during summer in some locations. tions is possible due to the sequencing of microsatellite regions. Whereas the Ostrea lurida genome in its entirety has not been REPRODUCTIVE CYCLE sequenced, the CO1 gene region has been successfully amplified, and O. lurida-specific primers and probes for qPCR have been The gonad follicles lie within connective tissue below the produced (Wight et al. 2009). epithelium, and can cover the entire body tissue (Coe 1932). Within approximately 1 y after settlement, Ostrea lurida REPRODUCTIVE BIOLOGY becomes reproductively mature and gonads begin to appear within about 8 wk during periods of warm water (Coe 1932). As reported by Coe (1931b), Ostrea lurida is a protandrous, During this period of preliminary gonad formation, there is sequential hermaphrodite, viviparous, and larviparous. Gam- little sexual differentiation (Coe 1931b). After 12–16 wk, the etes from both sexes are commonly found simultaneously in the gonads begin to differentiate, and both oogonia and spermata- gonad follicles (Coe 1931b, Oates 2013). However, oysters of gonia are present. The spermatagonia develop more quickly this genus are only known to spawn the gametes of one sex at than oogonia, resulting in a protandrous oyster (Coe 1931b). If a time, which is characteristic of sequential hermaphroditism. water temperatures are sufficient, spermatogenesis occurs, and There is also some conjecture that this species (and perhaps spermatozoa may be ripe at about 5 mo of age (Coe 1931b). genus) occasionally deviates from the protandrous life history; Sperm develop in aggregates or sperm balls, each with 250– oogonia and spermatogonia appear to compete for the starting 2,000 sperm (Coe 1931b); the flagellum of each individual sperm role in newly matured oysters, with some evidence that females in the sperm ball faces outward, and the adhesive holding the occasionally develop first (Coe 1931b, Coe 1932). See Orton sperm heads together dissolves once in contact with the (1927, 1933) and Orton and Amirthalingam (1931) for re- seawater, allowing sperm to begin swimming independently productive studies conducted with a congener, Ostrea edulis. (Coe 1932). The sperm balls are characteristic of the genus For the majority of the year, Ostrea lurida can remain Ostrea,asCrassostrea oysters do not develop this ultrastruc- reproductive if temperatures persist above those required for ture. It is thought that sperm ball formation prevents self- reproduction (Coe 1931b). The critical threshold for reproduc- fertilization by sequestering spermatozoa from developing tion in southern California (32° 52.0#N 117° 15.4#W) is about oocytes. Free-spawning oysters that do not exhibit gamete 16°C (Hopkins 1937), whereas it is reported to be closer to 13°C retention of both sexes (such as Crassostrea virginica) do not in the more northern range of the distribution of O. lurida in aggregate their sperm (Coe 1931a). It may also serve to deliver British Columbia (Stafford 1913). Preliminary data in the Coos higher concentrations of sperm to nearby females who capture Bay estuary, OR, indicate the critical temperature may be the spawned aggregates before they fully disaggregate. If and somewhere between those two values, at approximately 14.5– how current sparse O. lurida populations may be limited by 16°C (Garcia-Peteiro unpublished, Oates 2013). diffuse sperm delivery remains a topic for future research. Spawning may begin as early as April, and the reproductive The peak of the male phase of O. lurida is characterized by season may continue through October or November (Coe aggregations of spermatozoa, followed by the release of sperm 1931b). In a summer, Ostrea lurida may have either one or balls. Within the same individual, alongside mature male two spawning peaks (Hopkins 1937, Bonnot 1938, Carson gametes, female oogonia also develop (Coe 1931b). After 2010), although years with an apparent reproductive failure approximately 6 mo, the oocytes are ripe, and fertilization have been observed several times. For example, in 2010, larval may take place when mature oocytes are discharged from the densities up to 50 m–3 were observed in plankton samples from gonad and transported internally to the incurrent chamber of the Coos Bay estuary, but larvae were absent in 2011 (Garcia- the female oyster. Spermatozoa are pulled into the gills of the Peteiro unpublished). Larvae were again found in 2012 (Pritchard female-stage adults, and enter the mantle cavity where they et al. in preparation), likely indicating a reproductive failure in fertilize the eggs. Larvae develop in the mantle cavity or on the 2011, rather than a large-scale mortality event of adult pop- labial palps and gills (Coe 1931a, Hopkins 1936, 1937). The ulations. In Tomales Bay, CA, 603more recruits were found at brooded larvae are released through paired genital pores, one site in 2008 than 2009, also likely due to larval supply located ventrally to the adductor muscle. Whereas embryos limitations (Deck 2011). are growing within a brooding oyster, spermatogenesis con- Although oysters may not be actively spawning or brooding, tinues in the gonad amongst remnant oocytes, and reaches its all stages of sexual reproduction can be found within a single peak again after the embryos are released (Coe 1931b). population year-round (Coe 1931b, Oates 2013), and many Oysters that undergo three successive spawning events in one stages of male or female gamete development (see Reproductive season (spermatogenesis, ovigenisis, and spermatogenesis) may Cycle, below) may be found within a population at a single time exhibit decreased meat condition where their flesh becomes (Coe 1931a, Hopkins 1936, Oates 2013). For instance, in May translucent (as opposed to white, when oyster growers and 2006 at a restoration site in Fidaldgo Bay, WA, 1 in 10 oysters consumers consider the oyster to be in good condition). During RECENT ADVANCES ON THE BIOLOGY OF OSTREA LURIDA 261 this decline in condition, the oyster takes time to replenish and after a period ranging from a few days to a few weeks, they nutrient and energy stores. Upon recuperation, an individual develop an eyespot and are considered pediveligers (Zacherl may resume its reproductive cycle, ready to produce another 2005). Pediveligers are estimated to be competent to settle at round of eggs or sperm (Stafford 1913, Coe 1931b). This cycle approximately 300 mm (Loosanoff et al. 1966). Once suitable may continue throughout the remainder of the oysterÕs life, substrate is found, the oyster will cement itself to the substrate given that water temperatures remain sufficiently high. When and undergo metamorphosis to the juvenile stage (Galtsoff temperatures fall below the critical temperature, growth and 1964). mass gain may continue, but reproduction will halt, and resume The planktonic larval duration of Ostrea lurida is estimated only when temperatures rise again (Coe 1931b). A predeter- to range from 7 days to 8 wk (reviewed in Baker 1995). Imai mined number of sexual phases throughout the year are not et al. (1954) estimated it to be 11–16 days, whereas Hopkins apparent, as the length of each cycle is dependent on both oyster (1937) estimated the larval duration to be at least 30 days. Baker and environmental conditions (Coe 1932). Approximately 1.5 (1995) and Carson (2010) estimate larvae may spend from 1 to generations each year are the normal output per individual 8 wk in the water column before settling. Couch and Hassler oyster in southern California, with development of the second (1989) estimate 2 wk, Breese (1953) estimates 8 wk and finally generation of male- or female-phase development held in stasis Wight et al. (2009) estimate 22 days (summarized in Table 1). throughout low temperatures in winter (Coe 1932). This These discrepancies are areas that could benefit from future estimate supplements evidence of two spawning peaks during research, especially when considering that larvae may be the reproductive season which are often observed, where larvae estuarine dependent, and likely need to be retained within an appear rapidly after water temperatures rise, and the second estuary for their entire larval duration to successfully settle larval peak appears later in the season, after the individual (Pritchard et al. in preparation). oyster has gone through another male and female stage (Coe Settlement generally occurs in the summer and fall in 1932). Washington and Oregon. In Puget Sound, WA, settlers were Females carry an average of 250,000–300,000 larvae per observed between June and October and settlement peaked brood (Hopkins 1937). Unlike free-spawning oysters, the larvae multiple times each summer (Hopkins 1937). The settlement of Ostrea lurida complete much of their development in the period in Coos Bay, OR, has been observed from July to brood chamber of the egg-bearing oyster. Although larval December, with a peak in settlement occurring in July, growth likely depends to some degree on environmental factors, August, or October, depending on the year (Sawyer 2011, according to Hopkins (1937) working in California, the larva Rimler 2014). In Tomales Bay, CA, settlement occurred spends 2 days as a zygote, Day 1 as a blastula, and Day 2 as between August and November and peaked in September of a gastrula. On Day 3, the zygote becomes a trochophore, and on 2008 and in August of 2009 (Deck 2011). In La Jolla, CA, an Day 4, the trochophore becomes a D-stage larva, so named anomalous open coast population of Ostrea lurida settled because of the shape of the prodissoconch, or initial shell. from April to November (Coe 1932). In the Upper Newport During a subsequent 10–12 days, the larva maintains its shape, Bay in Southern California, settlement occurred from May to but grows in size, and is released as a D-stage veliger between November and peaked in June; in Aqua Hedionda Lagoon, 163 and 187 mm in diameter (Coe 1931b, Hopkins 1937, Zacherl a slightly more southern estuary, settlement occurred from et al. 2009). After its release, the veliger shell begins to thicken, June to February, again with a peak in June (Seale & Zacherl especially near the umbo—resulting in a characteristic shape for 2009). Natural recruitment was observed from December to the older larva of this species (Zacherl et al. 2009). These February in 2006 and 2007 in San Francisco Bay (Grosholz ‘‘umbo-stage’’ larvae propel themselves with a ciliated velum, et al. 2008).

TABLE 1. Growth rates of Ostrea lurida.

Maximum Growth duration Growth rate Source size (mm) (days) Season Location (mm/day)

Davis (1949) 35 70 0.5 37 0.53 Coe and Allen (1937) 50 210 0.24 Korringa (1976) 35 1,277 0.03 Grosholz et al. (2008) San Francisco Bay, CA 0.03–0.10 Deck (2011) Summer 1 Tomales Bay, CA 0.09–0.16 Summer 2 0.04–0.07 Kimbro et al. (2009a) Summer Tomales Bay, CA 0.03–0.3 Rimler (2014) Summer Coos Bay, OR 0.14 Trimble et al. (2009) Late summer/early fall Willapa Bay, WA 0.37 Trimble et al. (2009) Winter Willapa Bay, WA 0.01 Trimble et al. (2009) Spring, early summer Willapa Bay, WA 0.08

Maximum size and growth duration and were converted into growth rate (mm/day) when reported as days, months or years (Davis 1949, Coe & Allen 1937, Korringa 1976). Remaining values were reported as mm/day (Grosholz et al. 2008, Kimbro et al. 2009a, Trimble et al. 2009, Deck 2011, Rimler 2014). Empty cells indicate data were not reported. 262 PRITCHARD ET AL.

SHELL MORPHOLOGY temperature tolerance. For example, in San Francisco Bay, the monthly average temperatures for intertidal O. lurida popula- Shells of Ostrea lurida are made of a variety of crystalline tions were between 18.5 and 27.3°C (Carson 2010). High forms of calcium carbonate simultaneously: a mixture of calcite, temperatures, however, may also result in mortality. For aragonite, and vaterite, each of which is able to substitute example, Trimble et al. (2009) observed very high losses of a variety of elements for Ca in the shellÕs crystal structure outplanted oysters, and suggested high temperatures in the (Campana 1999). As a larval shell grows, elements with similar summer could have been responsible. properties to Ca (such as Sr, Ba, Pb) can replace Ca in the Although considered an estuarine species that presumably calcium carbonate matrix (Campana 1999) depending on also requires a tolerance to a wide array of salinities, Ostrea salinity, temperature, and element concentration (Zacherl lurida does not appear to do well at extremely low salinities. et al. 2009). Higher concentrations of these elements relative Oysters may do well at salinities above 25, although they can to Ca are seen in younger life stages. Shell elemental uptake tolerate brief exposure to lower salinities (Korringa 1976, Peter- during earlier life-stages is a potential tool for researchers Contesse & Peabody 2005). For instance, O. lurida kept at wishing to identify a larvaÕs natal site through elemental a salinity of 15 for 5 wk experienced 83% survival, and oysters spectroscopy (Zacherl et al. 2009, Carson 2010). Changing survived salinities of 5 or lower for 2–3 wk before suffering growth rates and changes in the crystalline form of the shell 100% mortality (Gibson 1974). are mechanisms for varying rates of elemental uptake, and earlier shells may be composed of aragonite (Zacherl et al. HARVESTING 2009). The subsequent crystalline structures, approximately at the age of settlement, are calcite (Zacherl et al. 2009). Through Little information is available on historic (baseline) sizes of spectroscopy of shell material, researchers have determined populations of Ostrea lurida throughout its entire range. There source and sink populations in San Diego County (Carson are currently healthy populations on Nootka Island, British 2010). Columbia, with densities surpassing 1100 individuals m–2 (Beck The adult shell of Ostrea lurida is small relative to members et al. 2009), but these densities may be uncharacteristically high. of Crassostrea, and both hinges are serrated. The right valve is Others report historical densities around 116 individuals m–2 flat, whereas the left is approximately concave (Couch & (zu Ermgassen et al. 2012). Regardless, historically, populations Hassler 1989, Arakawa 1990). The shell lacks a periostracum, of O. lurida were sufficient to support both tribal subsistence but the inner shell ranges from white to purple (Allen 1977), and and commercial harvesting. Large shell middens indicate the the exterior of the shell may be striped purplish, brown, or importance of the oysters to tribes (Steele 1957, Barrett 1963, yellow (Hertlein 1959). By the presence of chomata, small Elsasser & Heizer 1966, Baker 1995, Groth & Rumrill 2009). bumps on the inside of the hinge (a characteristic of the Ostrea For instance, one particular midden found near San Francisco, genus), O. lurida can also be distinguished from small Crassos- CA, was at least 107 m in diameter and 13.7 m tall and trea gigas although chomata in older specimens may be contained only O. lurida shells (Elsasser & Heizer 1966). obscured by a build of up of nacre (Light 2007, Carlton, Settlers of the American West also considered this oyster Williams College, 2013, personal communication). See Baker a delicacy. In the 1850s, one plate of Ostrea lurida on the half (1995) for a more complete description of anatomy and shell cost approximately $20 (about $400 in 2005 currency: characteristic shell morphologies. Peter-Contesse & Peabody 2005), and O. lurida was said to be Descriptions of maximum shell size and shell growth of a favorite of Mark Twain (Beahrs 2012). Commercial takes Ostrea lurida vary. Hertlein (1959) reports a maximum shell were once high—over 7 million liters year–1 were reported in length of approximately 7.5 cm, whereas Buhle and Ruesink Washington in the 1870s (Cook et al. 2000), but unsustainable (2009) report 6 cm, Arakawa (1990) 5–8 cm, and Peter-Contesse extraction depleted the species early in the 1900s throughout its and Peabody (2005) report a maximum shell length of 10 cm. range. Declines continued with the removal of adults, decreas- Growth rates are variable (Table 1), and may be related to ing the reproductive output of populations and removing the a latitudinal gradient driven by temperature or food availabil- preferred substrate (adult shells) used for larval settlement ity, although enough data to conclusively support this hypoth- (Sayce 1976, Cook et al. 2000). Commercial oyster harvesters esis are lacking. The range of growth rates of O. lurida taken in realized O. lurida was being overexploited as early as 1855, and the field is 0.01–0.53 mm per day (Trimble et al. 2009, Dinnel new regulations for harvest were set; namely, no oysters could et al. 2009, Rimler 2014). be harvested during the main reproductive season, July– Environmental parameters such as temperature and salinity August, in the Washington area (Steele 1957). Washington may not only affect this oysterÕs growth and maximum size, but eventually established oyster reserves in 1897, but populations also distributional limitations. For instance, populations may were already devastated, and no significant increases in experience 100% mortality in the intertidal or shallow subtidal population growth were observed despite the harvest ban. during cold weather, as they cannot survive freezing tempera- One potential reason for limited recovery may have been the tures, even if not inundated or covered with ice (Davis 1955, fishing techniques used for oyster harvest, which included hand- Peter-Contesse & Peabody 2005). This mortality may not be due picking, dredging, and ‘‘tongs.’’ The methodologies resulted in to feeding inhibition, as dead oysters often have adequate food all size classes of oysters being removed. Those below the legal reserves (Davis 1955). When cultivated for commercial harvest limit were thrown back into the water but left unattached, likely in the late 1800s and early 1900s, dykes were built to maintain to be buried in the sediment (Coen & Luckenbach 2000). a water level of 15–30 cm across the growing grounds to reduce Between 1924 and 1926, approximately 1.5 million liters of the risk of freezing (Hopkins 1936). Despite this sensiti- O. lurida were extracted for nontribal consumption in Wash- vity to freezing temperatures, Ostrea lurida maintains a wide ington, but the catch decreased to approximately 106,000 L by RECENT ADVANCES ON THE BIOLOGY OF OSTREA LURIDA 263

1955 (Steele 1957). In Washington in the 1930s to 1950s, coastal introduction of C. gigas may have carried this protist ‘‘hitch- degradation and water quality problems, notably sulfur waste hiker,’’ and it may also have played a role in the demise of O. liquor produced by pulp mills, further prevented their recovery lurida in British Columbia during the 1940s (Bower et al. 1997). (Gunter & McKee 1960, Cook et al. 2000). Between 1991 and The San Francisco Bay populations of Ostrea lurida were not 1996, only about 1,900 L were commercially harvested (Cook found to host Microsytos mackini, although a haplosporidian- et al. 2000). Once natural populations were depleted, farmers like plasmodium that was found could be related to M. mackini began cultivating O. lurida with dyke systems (see Steele 1957 (Friedman et al. 2005). A hemic neoplasia was also found in for details). the San Francisco Bay populations; the source of the hemic neoplasia, and its impact on O. lurida, remains unknown ASSOCIATION WITH OTHER ORGANISMS (Friedman et al. 2005) (but see review on this disease in oysters by Elston et al. 1992). The first occurrences of the haplospori- The movement of oysters for aquaculture is a notorious dian parasite in O. lurida were described in Yaquina Bay and vector for introduced pest species. In fact, it is considered the Alsea Bay, OR, in 1972 at low occurrences (5% at both sites second highest cause of nonnative marine species introductions through May, 1973) (Mix & Sprague 1974). Atypical cells after transport in ballast water (National Research Council characteristic of infections with this parasite were seen in most 2004, Molnar et al. 2008). Introduced parasites, protistans, organs and tissues, but no inflammation or degeneration was diseases, and macrofauna including bivalves, crabs, and oyster observed (Mix 1975). Samples of O. lurida were collected from drills have been associated with the transport of Ostrea lurida. the Coos Bay estuary, OR, in 2008 to 2009 and inspected for the Likely owing to the current low density of most populations of presence of protistan parasites. All samples were subsequently O. lurida, these introductions, however, have received little found to be uninfected (Rumrill, personal observation). Despite notice in recent literature. In the future, it will be essential for the number of diseases and parasites known to affect O. lurida, coastal resource managers to identify and manage infections little work has been done on the demographic consequences and/or infestations of these introductions to promote future of large-scale infections. This information could prove to be healthy populations of O. lurida. crucial for managing future restoration efforts, and the absence A number of parasites have been found in Ostrea lurida, of infection is considered to be a prerequisite to some future most likely introduced with other bivalves brought in for restoration efforts, including those in the Coos Bay estuary, aquaculture. A parasitic copepod, Mytilicola orientalis, affects OR. Baker (1995) provides additional information on parasitic both Crassostrea virginica and O. lurida. It appears to have been organisms that affect O. lurida. introduced from Japan with oyster seed, and there is currently Introduced bivalves have also proven harmful to Ostrea no known treatment or prevention. Symptoms of infected lurida, although indirectly. When the O. lurida decline began, oysters range from undetectable (Bradley & Seibert 1978) to Crassostrea virginica was imported to supplement the commer- poor growth and condition, extreme damage to gut tissue, and cial oyster industry (Sayce 1976). Later, Crassostrea gigas was in some cases, mortality (Sinderman 1974). In the San Francisco introduced (Sayce 1976), and the continued decline of O. lurida Bay area, M. orientalis has been reported in O. lurida popula- has been attributed, in part, to the aquaculture of C. gigas tions but these populations appeared to have no negative (McKernan et al. 1949). Indirect effects, direct competition, or symptoms from the copepod (Friedman et al. 2005). A ‘‘red both could be contributing to this decline in the presence of worm’’ that lives in its anus was then introduced by M. C. gigas. For instance, in the absence of predatory oyster drills orientalis, and oysters found with this worm are usually in poor (see below), an initial increase in O. lurida survival was observed condition (Sinderman 1974, Peters 1993). Flagellated proto- when C. gigas was introduced, possibly because of direct zoan parasites (Hexamita spp.) can be pathogens at low facilitation and shared predation risk (Buhle & Ruesink temperatures (Stein et al. 1959), and the parasitic flatworm 2009). This trend, however, was followed by a decline in Pseudostylochus ostreaophagus has also been introduced, caus- O. lurida survival and mean relative growth rate as the density ing declines in body condition for infected oysters (Peters 1993). of C. gigas beds increased, perhaps because of competition Additionally, an ectoparasitic gastropod, Odostomia spp., has (Buhle & Ruesink 2009). been found on O. lurida, but to date, has not been shown to Another indirect effect possibly contributing to the decline cause negative effects on populations (Strong 1928). of Ostrea lurida within Crassostrea gigas beds includes O. lurida Although not yet demonstrated to cause widespread mor- larval settlement onto C. gigas shells. O. lurida is likely to settle tality in current natural populations, Ostrea lurida is susceptible on shell, and often settles among the aquacultures of C. gigas to infection by a small protistan (Microsytos mackini), recently that, however, grows twice as quickly as O. lurida. If spat of present in commercial beds of Crassostrea gigas in British both oysters occur in the same place (within 5 cm of each other), Columbia, Canada (Bower et al. 1997). In fact, O. lurida was C. gigas could be expected to outcompete or overgrow O. lurida almost twice as susceptible to infection by Mikrocytos mackini within a single year (Trimble et al. 2009). Furthermore, owing to as C. gigas (present in 96% of O. lurida versus 48% of C. gigas) a lack of hard substrate, naturally produced O. lurida larvae are (Bower et al. 1997). In the laboratory, M. mackini infection settling on C. gigas shells (located mainly above mean low low caused 89% of O. lurida (then known as Ostrea conchaphila)to water [MLLW]), which are located higher in the intertidal than become moribund, as opposed to just 17% of C. gigas (Bower where O. lurida settle under natural conditions (Trimble et al. et al. 1997). Field-collected O. lurida were also infected, 2009). This change in settlement height could impact mortality demonstrating M. mackini is already present in wild popula- through thermal stress or desiccation, as well as removal of the tions, although it may not yet be problematic on a population O. lurida recruits during harvesting of C. gigas. In Coos Bay, scale (Bower et al. 1997). It also appears that M. mackini was OR, commercial C. gigas growers routinely find juvenile found in Washington in May 2002 (Friedman et al. 2005). The O. lurida on shells of C. gigas adults, and visual inspections of 264 PRITCHARD ET AL.

C. gigas shells indicate ;5% incidence of O. lurida settlement it is likely a competitor of drills, rather than a predator of drills on C. gigas shells (Rumrill, personal observation). The native (Grason & Miner 2012). Importantly, feeding rates on drills by oysters are removed and discarded from C. gigas before sale C. productus in the field may be lower than those observed in the (Groth, OR Department of Fish and Wildlife 2013, personal laboratory because increased habitat heterogeneity would communication). For these reasons, there is speculation that facilitate the escape of drills (Grason & Miner 2012). C. gigas shells are sinks for naturally occurring O. lurida larvae, Invasive crabs (Carcinus maenas) and drills (Urosalpinx but more work needs to be done in the future. cinerea) have also been deemed culprits in disrupting trait- With the introductions of Crassostrea virginica and Crassostrea and density-mediated trophic cascades usually occupied by gigas also came a number of predatory gastropods. The Eastern native crabs and whelks, resulting in increased mortality of drill (Urosalpinx cinerea) was introduced with C. virginica Ostrea lurida. Patterns of oyster mortality in Tomales Bay, CA, (Carlton 1979), whereas the Japanese drill (Ocebrina inornata) have been positively related to U. cinerea abundance, rather was introduced from Japan with C. gigas (Dall 1926). Both drill than abiotic conditions such as thermal stress or desiccation species lack a planktonic larval stage, and introduction is (Kimbro et al. 2009b). These altered food webs and trophic primarily through the anthropogenic transfer of infected oys- cascades could have large impacts on restoration sites where ters (Grason & Miner 2012). Both species of introduced drills drills and Cancer productus are both present, the predation have the potential to increase predation pressure on Ostrea pressure possibly being too great to allow recovery. lurida populations. A number of species may also indirectly compromise Ostrea Through evidence based on feeding trials, it appears that both lurida populations. As O. lurida is a sessile, benthic filter-feeder, Urosalpinx cinerea and Ocebrina inornata prefer Crassostrea sediment resuspension from resident fauna, such as bioturbat- gigas over Ostrea lurida when similarly sized individuals are ing thalassinidean shrimp, can be fatal. For example, Neo- offered, but prefer small individuals over large individuals of trypaea californiensis and Upogebia pugettensis destabilize and either species (Buhle & Ruesink 2009). As adult C. gigas are resuspend sediment when making burrows (Swinbanks & larger than adult O. lurida, predation pressure on O. lurida is Luternauer 1987). The destabilized sediment may no longer likely greater in locations with both species present. In Willapa support the oysters, at which point they begin to sink into the Bay, WA, 4.0% of mortality of O. lurida could be due to mud, preventing water flow needed for feeding and respiration. predation by oyster drills, and up to 32% of O. lurida were Furthermore, gills and ciliary tracts can become clogged drilled (Buhle & Ruesink 2009). with sediment, causing slower growth and higher mortality Historically, Ocebrina inornata has had an especially large (Feldman et al. 2000). Thus, shrimp populations are yet another impact on juvenile oysters. Because of difficulties in eradication variable managers should be taken into account when selecting once a population became infected, some oyster growers restoration sites. abandoned beds of Crassostrea gigas on the West Coast with Large blooms of the diatom Melosira borreri may pose persistent and abundant populations of the drill (Buhle & another threat to Ostrea lurida. During the 1950s, sulfur liquor Ruesink 2009). In addition, O. inornata has caused high pollution from pulp mills was problematic, notably in Puget mortality of Ostrea lurida in Puget Sound (Chapman & Banner Sound, where these diatoms ‘‘bloomed’’ all year long—the dead 1949), and numerous other works suggest O. inornata feeds diatomsaccumulatedupto15cmindykeswhereO. lurida preferentially not on C. gigas, but on O. lurida, Mytilus edulis, was grown, causing local extinction (Steele 1957). The sulfur and Tapes japonica in Puget Sound, WA (reviewed in Carlton waste liquor caused a continuous decline of O. lurida in the 1979). Among these, Ostrea lurida is also preyed upon by several 1950s (Hopkins 1935, McKernan et al. 1949, Steele 1957), native organisms, including sea stars, diving ducks (scaups and partially owing to its facilitation of M. borreri growth. scoters; Galtsoff 1930, Cook et al. 2000), crabs (Cancer Despite the historic impact on O. lurida, no recent work was productus; Couch & Hassler 1989), bat rays (Matthiessen found for this review to indicate if this diatom is still 1970), and native whelks. ecologically important. In laboratory experiments, trophic cascades involving both As filter feeders, one would also suspect fouling organisms, native and nonnative predators have been examined for their many of which are also filter feeders, and conspecifics to affect influence on the recovery of Ostrea lurida populations. For growth and survival. Indeed, the presence of competitors instance, Grason and Miner (2012) examined the feeding (typical fouling organisms such as bryozoans and tunicates) preferences of a native generalist crab (Cancer productus)on can decrease average Ostrea lurida recruit size by up to ;50% both oysters (O. lurida and Crassostrea gigas) and nonnative (Deck 2011). Interestingly, these competition effects appear drills (Ocebrina inornata and Urosalpinx cinerea) that may serve only to influence early-stage recruits; there was no apparent as intermediate predators, feeding only on oysters. Results from effect of competition on juvenile (mean size 15 mm) or adult feeding trials suggested that C. productus does not exhibit growth rate or survival (Deck 2011). Competition effects may a feeding preference between juveniles of O. lurida and C. gigas. also be at play in San Francisco Bay, where recruit abundance When, however, offered a choice of two species of nonnative decreased in the presence of competitors (Deck 2011). In out- oyster drill adults and juvenile C. gigas, C. productus consumed planted oysters on tiles in Fidalgo Bay, WA, fouling organisms six times more juvenile oysters than either species of drill. As (ascidians, hydroids, sponges) and conspecific competitors de- O. lurida and C. gigas were consumed equally, these results pressed the maximum length of O. lurida by 2%–35%, and indicate recovering O. lurida populations could be experiencing decreased survival from 15%–7% (Trimble et al. 2009). Fur- much stronger predation pressure, via invasive drills, than they thermore, removing fouling organisms (e.g., barnacles, ascid- did historically. Despite the classification of C. productus as ians) from tiles resulted in oysters twice as likely to survive as a generalist predator, it is likely not releasing O. lurida from those with fouling organisms left in place (Trimble et al. 2009). increased predation pressure from the introduced oyster drills; In addition, the largest five oysters on each tile were those RECENT ADVANCES ON THE BIOLOGY OF OSTREA LURIDA 265 farthest separated from the nearest neighbor, further suggesting Like many marine species, Ostrea lurida seems to have intraspecific competition could affect growth and subse- source and sink populations. Using shell elemental spectros- quent success, including reproductive condition and fecundity copy in San Diego County, CA, for instance, San Diego Bay (Trimble et al. 2009). Whereas settlement of O. lurida may be was found to contribute 45.0% of recruits to surrounding bays, gregarious—encouraged by the presence of other larvae or followed by two North County lagoons (35.4%) and Mission other settled consepecifics—little work (see Bayne 1969) has Bay (19.6%) (Carson 2010). Although Mission Bay supplied been done to identify or understand this behavior, or to about 20% of the larvae in the area, it received approximately understand its connection to intraspecific competition. 80% of larvae from San Diego Bay and the North County lagoons. At larger scales, population connectivity between LARVAL SUPPLY, SETTLEMENT, AND RECRUITMENT estuaries separated by 75 km in California has been observed, and California populations may be more strongly or frequently To understand population dynamics of multiphasic organ- connected than northern populations in Oregon, Washington, isms such as Ostrea lurida, all stages of its lifecycle need to be and British Columbia (Carson 2010). Dispersal that occurs investigated, including larval supply, settlement/recruitment between these populations is likely heavily influenced by and adult survivorship (Porri et al. 2008). Current adult O. hydrodynamic regimes and pelagic larval duration. lurida populations are far below historic numbers (Beck et al. The larval contribution of a population is important from 2011, zu Ermgassen et al. 2012). Despite bans on harvesting and a management perspective. For example, when designing widespread restoration efforts, some population sizes remain a marine reserve, it may be desirable to include both source perplexingly low. One potential limitation could be larval and sink populations. Sink populations (as in Mission Bay, CA) supply—either because few larvae are being produced, or receive high larval input relative to their output, and could because few larvae are surviving and settling successfully. In accumulate a healthy oyster bed relatively quickly, subse- the latter scenario, the retention of larvae within estuaries quently helping to restore habitat health and function. In should be considered, as it can greatly influence recruitment addition, if larvae are supplied to the sink population from patterns (Graham & Largier 1997, Sponaugle et al. 2002). a variety of local source populations, genetic diversity increases, In the Coos Bay estuary, OR, larval abundance and re- making the populations more genetically heterogeneous and cruitment of Ostrea lurida is high in the mid to upper-bay, but perhaps robust over time. Including source populations (e.g., low in the more marine reaches of the bay (Garcia-Peteiro San Diego Bay and the North County lagoons) in marine unpublished, Pritchard et al. in preparation). During the dry reserves is also important to promote larval supply to nearby season in the Coos Bay estuary, the water mass in the upper bay populations. is characterized by long residence times, but in the lower bay, Do Ostrea lurida larvae have behavioral mechanisms allow- short residence times prevail. Thus, it is feasible that larvae ing them to be retained close to their natal population, resulting produced in the upper bay are retained within the bay for their in short dispersal distances? Should restoration managers be pelagic larval duration, and may settle successfully, whereas cautious about expecting restored populations to seed distant larvae transported to, or produced in the lower bay are swept populations (e.g., outside a particular estuary)? Is there more out of the bay before settlement, resulting in larval wastage. support for StickÕs work (2011) that long-range dispersal is Likewise, in Tomales Bay, CA, recruitment along an estuarine a rare occurrence? These questions could benefit from future gradient was strongly influenced by the water residence time research. within the estuary, and recruitment to intertidal and subtidal Restoration efforts are currently being implemented habitats was positively correlated with residence time (Kimbro throughout the entire range of Ostrea lurida, at both small 2008, Deck 2011). These patterns demonstrate that small-scale scales (individual landowners; Rumrill personal observation), variation in larval supply can be important within a single bay. and large scales (13% of Willapa Bay) (Trimble et al. 2009). In the future, expanding channels and bays through dredging These efforts most commonly consist of artificially spreading may decrease the portion of the bays with long residence times, hard substrate (such as adult shell), and releasing hatchery- increasing the likelihood of larval wastage of already estab- reared ‘‘seed’’ (i.e., late-stage larval oysters capable of settling), lished O. lurida populations (Pritchard et al. in preparation). with the hopes that these seed will settle, survive, reproduce, and Most evidence to date suggests larval dispersal distances in contribute to future natural populations. Very little work has, Ostrea lurida may be low. For example, at a restoration site in however, addressed factors contributing to successful settle- Fidalgo Bay, WA, the highest densities of recruits were found ment, survival, and growth by the early life-history stages of closest to the restoration site, with abundance decreasing with O. lurida in the field, which could obviously help improve the distance away from the site, suggesting that larvae were from success of future similar projects. For example, in 2002, the the nearby site (Dinnel et al. 2011). In Coos Bay, OR, larvae are Skagit County Marine Resources Committee began restoration found at low concentrations offshore compared with concen- efforts in South Fidalgo Bay (Dinnel et al. 2009). Fidalgo Bay trations within the bay (;3m–3 versus ;50 m–3, respectively) was thought to lack the hard substrate necessary to allow (Garcia-Peteiro unpublished) which suggests that large-scale, natural, successful recruitment of O. lurida. Shell of Crassostrea long-distance connectivity is rare near the Coos Bay estuary. gigas was used under a railroad bridge to provide this hard The five genetically distinct regions presented by Stick (2011) substrate. Shell bags were placed out in June 2003, and from also support this hypothesis. Although it is possible that rogue 2002 to 2006, survival was consistently high, about 90%, but larvae may disperse among the five regions, the apparent genetic dropped to 39% by 2009. Thus, although the conditions at this distinctions of oysters among these five regions suggest that site were satisfactory for the early-stage oysters between 2002 population connectivity is low enough for genetic differences to and 2006, some unknown factor led to higher mortality between accumulate. 2006 and 2009 (Dinnel et al. 2011). In terms of recruitment, 266 PRITCHARD ET AL. young of the year were not detected until June 2005, and then because of the muted daily ranges in salinity. Perhaps either the only in very low numbers. No young of the year were found in larvae were not finding the two more riverward sites suitable for 2006, suggesting that spawning and/or successful recruitment settlement, or they were not surviving the 2 wk period between did not occur in 2005. Moderate numbers of recruits were found collections due to stress from environmental parameters such as in 2007, suggesting 2006 was a mildly successful reproductive temperature, salinity, or desiccation, or alternatively, preda- year. No recruits were found again until 2010, when moderate tion. Examining larval supply and settlement or recruitment recruitment (2.7 juveniles/cultch shell) was again observed simultaneously allows researchers and managers to better un- (Dinnel et al. 2011). No recruits, however, were found on shell derstand population dynamics; namely, whether populations bags in locations other than south Fidalgo Bay (Cape Sante have limited recovery due to a lack of larvae, inadequate Head, Guemes Channel, or east MarchÕs Point). These patterns settlement surfaces, or postsettlement mortality. of irregular successful recruitment further support the idea that As Ostrea lurida exhibits both a planktonic larval stage and populations of O. lurida may be subject to reproductive and/or a benthic, filter-feeding adult stage, the importance of settling in recruitment failure in some years. An alternative explanation is an area with sufficient water movement cannot be overstated. that the oysters were not surviving the winter. Despite frequent Water provides a continuously renewed source of food and poor recruitment, initially low densities of oysters recorded in oxygen, helps regulate thermal and water quality parameters in 2003 in Fidalgo Bay (45 ind. m–2), were up to 130 m–2 by June which larvae and adults live, and once reproductive, water 2011 (Dinnel et al. 2011). The Samish Tribe tried another disperses sperm and delivers it to females. Larval dispersal to restoration site at Weaverling Spit, Fidalgo Bay in 2003. By other populations also cannot occur without water movement 2006, however, no live oysters, were found. It was suggested (Bertness et al. 1991, Leonard et al. 1998). Conversely, very high that restoration efforts failed at this site because it did not have flows can prevent larval attachment and settlement by whisking standing water at extreme low tides (Dinnel et al. 2009). In Coos larvae away before they have an opportunity to attach solidly to Bay, OR, 100% mortality occurred among very small (2–7 mm) the settlement surface (Connell 1985, Pawlik & Butman 1993, oysters over the winter, and mortality was roughly 50% among Qian et al. 2000, Larsson & Jonsson 2006). There likely exists the larger group (17.5–27.5 mm) (Rimler 2014). In addition to some balance between high and low flow, which allows for size, location within the estuary and time of year also successful larval attachment and sufficient oxygen and food contributed to variations in mortality rates. Future research delivery. should focus on the mechanisms (larval supply, settlement, Because of their dependence on water flow, tidal height of and recruitment) limiting temporal consistency in population a settlement location may also play a role in the growth and recovery. survival of Ostrea lurida. For instance, growth rates up to 81% It is essential to understand the abiotic factors that could higher have been documented subtidally than intertidally (Deck either render a site successful and thus promote self-sustaining 2011). Because there were no clear differences between oyster populations, or lead to failure. Newly settled oysters and adults growth along the estuarine gradient subtidally, perhaps in- are vulnerable to thermal stress, desiccation, food shortage, tertidal oysters are limited by feeding time and food concentra- predation, and competition. Thermal stress caused by extreme tion, as they would likely be more exposed to riverine input than heat or cold affects metabolic and reproductive perfor- to phytoplankton-rich seawater (Deck 2011, Kimbro et al. mance, growth, and mortality within invertebrate populations 2009a). In other field studies, tidal elevation had no effect on (Bertness et al. 1999, Leonard et al. 1999, Leonard 2000, Pineda growth, but did have a large influence on survival (Trimble et al. et al. 2009). Thermal stress is minimized when the surrounding 2009). Oysters 0.3 m above MLLW had <5% survival, whereas water acts as a buffer from large shifts in temperature and oysters on tiles that were continuously submerged had survival minimizes risk of desiccation. Seed (settlers) also appear to of 20%. Settlers of O. lurida were more than twice as likely to become somewhat acclimated to the physical environment into settle on cultch placed 0.3 m below MLLW than 0.3 m above, which they settle. For instance, seed transported from one and juvenile oysters experienced over 50% mortality after air location to another after settlement may only grow if the second exposure (2%–10% of the time) (Trimble et al. 2009). location had the same temperature, salinity and ‘‘mineral In Elkhorn Slough, CA, adults and juveniles of Ostrea lurida content’’ as the first location (Steele 1957). were absent all at 13 sites with minimal (maximum 1–15 cm) Specific settlement cues used by larvae of Ostrea lurida, tidal exchanges (Wasson 2010). These areas could be more which could strongly contribute to variations in recruitment, heavily influenced by pollution, hypoxia, and low salinities than remain unknown, although the presence of hard substrate, areas with more tidal mixing. Juvenile survival, however, was conspecifics, and biofilms all may contribute. Another possibil- up to 90% in areas with muted tidal ranges (defined as ity is that larvae are sensitive to environmental parameters such a maximum range between 15 and 100 cm) but an average of as temperature and salinity, which could strongly influence their only 65% survival at sites with full tidal ranges (250 cm). Higher survival. For example, within the Coos Bay estuary, larvae are survival at sites with muted tidal ranges may be due to decreased supplied to two sites (Catching and Coalbank Sloughs) that, sedimentation, and suggests that these areas might be successful due to their proximity to the outflow of the Coos River, are restoration sites, provided that tidal flushing is substantial subject to large fluctuations in temperature and salinity on both enough to prevent water quality problems (Wasson 2010). daily (tidal) and seasonal scales. Recruitment data collected Few studies, however, have been conducted to understand approximately every 2 wk at these sites revealed recruitment how flow regime directly affects settlement, growth, and was near zero despite sufficient larval supply (Pritchard et al. in survival in O. lurida. preparation). Seaward of these two sites approximately 4 km, Flow may also directly influence sedimentation rates, and the larval supply, however, is slightly higher (in Downtown may be a significant component that drives settlement prefer- Coos Bay), but recruitment is dramatically higher, possibly ences (Wasson 2010). Increased sedimentation rates caused by RECENT ADVANCES ON THE BIOLOGY OF OSTREA LURIDA 267 hydraulic mining may have caused Ostrea lurida to disappear high densities (Wasson 2010). Conversely, sites with oysters from Bolinas Lagoon and Morro Bay, CA (Barrett 1963). absent or found in low densities were loosely clustered in the Likewise, the disappearance of the oyster from Coos Bay, nMDS plot, indicating a high level of variability in these water OR, may have been due to a tsunami or large fire followed by quality parameters where oysters were scarce. These data heavy rains, which caused heavy sedimentation that smothered highlight the need for more information on the influence of O. lurida populations (Groth & Rumrill 2009). Interestingly, in water quality parameters and characteristics in limiting the Elkhorn Slough, CA, neither juvenile size nor density was natural recovery or future restoration of O. lurida populations. significantly different between sites of high versus low sedimen- On the basis of StickÕs (2011) work indicating distinct genetic tation, although mortality was significantly higher (P ¼ 0.03) in populations, there is a need to explore the interactions between of areas of high versus low sedimentation (85% versus 66%, life-stages, genotype and tolerances to water quality parameters. respectively) (Wasson 2010). One last parameter that has been examined with Ostrea Population declines of Ostrea lurida to the point of func- lurida is water pH. Having a shell composed primarily of tional extinction have been observed over their entire distribu- calcium, bivalves may be particularly sensitive to future ocean tion (Kirby 2004, Beck et al. 2011). The dearth of hard substrate acidification. Hettinger et al. (2012) investigated the effects of providing settling sites may also be an important factor ocean acidification on larval and juvenile growth in O. lurida. hindering the recovery of O. lurida (Groth & Rumrill 2009, Larvae were reared in treatments of 700 (control), 800, or 1100 see Brumbaugh & Coen 2009 for a full review). In addition, O. ppm CO2, corresponding to pH values of approximately 8.0, lurida also shows a preference for settling on natural hard 7.9, and 7.8, respectively. These CO2 concentrations were substrates such as rocks, shells, and gravel in shallower mud, chosen to fall within the ranges of current conditions in Tomales but not deep mud, where these substrates are absent or are likely Bay (between 200 and up to 1500 ppm CO2 during severe to sink over time (Groth & Rumrill 2009, Wasson 2010). conditions). The mean summer condition of 700 ppm CO2 was Without sufficient hard substrate (rip-rap, shells, pilings, etc.) chosen as a control, whereas 800 and 1100 ppm CO2 were settling larvae may be forced to settle on driftwood, mud, or chosen to simulate future mean conditions based on available debris, which could be washed away, buried in settling sedi- projections. After 9 days, larvae reared in a pH of 7.8 had 15% ment, or resuspended and deposited in unsuitable environmen- slower shell growth relative to larvae reared in control condi- tal conditions. Monitoring natural recruitment and survival on tions (pH 8.0). Furthermore, larvae reared in pH 7.8 had 7% unenhanced (mud, debris) and enhanced (e.g., with shell bags or smaller shells area at settlement relative to control larvae. rip-rap) areas would help illuminate the importance of hard Lastly, 7 days after settlement, juveniles reared in pH 7.8 had substrate in promoting recovery (Polson & Zacherl 2009). 41% slower shell growth compared with control juveniles. In Coos Bay, OR, settlement has been observed on old Depending on the conditions to which they were exposed as marine batteries, logging cables, and a submerged shopping cart larvae, this study concluded that persistent carryover effects and motorcycle (Groth & Rumrill 2009). Recruits may also influence juvenile shell growth rates. In a restoration context, prefer hard and shell habitat to bare sediment, which in turn, therefore, this study suggests that site selection for restoration may be preferred to eelgrass habitats (Zostrea marina) (Trimble efforts should consider annual fluctuations in pH. et al. 2009). These recruitment patterns among substrate types Even within a small area, some habitats are more suitable could, however, have been an effect of survival rather than than others. For example, 1153 more spat were found on the settlement preference. Among 32 sites observed in Elkhorn under-side of horizontal surfaces (settlement plates) compared Slough, CA, 25 sites were characterized as mudflats, and seven with the upper, and 33 more on the underside of horizontal were characterized as mudflats enhanced with anthropogenic surfaces compared with vertical surfaces (Hopkins 1935). This hard substrate. At any sites characterized as mudflats, Ostrea is likely due to the swimming orientation of a larva, with the lurida was not present and was only present at five of the seven velum pointed upward (Hopkins 1935). Other hypotheses sites where hard substrate was available (Wasson 2010). If suggest settling on the underside of shell, plates, or rocks, settlement substrate is lacking, larvae may cope through one of prevents the animal from being smothered by sediment (Cole & two choices: (1) settle in a suboptimal area (for instance, on soft Knight-Jones 1939, Michener & Kenny 1991). The oysterÕs substrate, where they are likely to encounter heavy sedimenta- preferential attachment is also not a negative phototrophic tion and mortality); or (2) continue their pelagic larval stage, behavior, but the larvae may be negatively geotactic: a possible which may result in mortality because of predation or larval evolutionary adaptation to reduce exposure to direct sunlight wastage (Rumrill 1990, Morgan 1995). Therefore, it is essential and decrease thermal stress to the future recruit (Hopkins 1935). for restoration sites to have sufficient settlement substrate. Working with settlement plates submerged for 3 mo, however, In naturally occurring populations, the influence of envi- Hopkins (1935) recognized that these recruitment data might ronmental parameters in addition to the availability of settle- reflect survivorship and not settling preference. ment substrate on Ostrea lurida population size and health has With little information regarding the locations of historical been infrequently examined. In Elkhorn Slough, CA, popula- populations within estuaries, coupled with the slow recovery tions of O. lurida were absent or at very low densities at of present populations, it remains unknown under what locations with large ranges in water quality parameters, in- conditions Ostrea lurida are most successful during different cluding temperature, salinity, turbidity, dissolved oxygen, and life history stages. It has been suggested that the earliest life fluorescence, whereas sites with smaller ranges in these param- stages in marine invertebrates are most sensitive to physiolog- eters tended to have larger populations (Wasson 2010). High- ical stress (Bayne et al. 1976), but there is currently little density oyster sites were also very closely clustered within information on the tolerances of larvae of O. lurida to a water quality nMDS plot, indicating a high level of similarity temperature and salinity, or how variations in these para- in these water quality parameters where oysters are found in meters might influence growth, settlement, or mortality. 268 PRITCHARD ET AL.

Although it is relatively straightforward to observe adult water quality parameters like salinity and temperature to which mortality and growth, understanding the physiological toler- adults have adapted, genetically or phenotypically. ances of the early life stages (larvae, settlers) of this oyster in the field is limited by their small size and planktonic habitat. CONCLUSIONS Understanding these tolerances may provide information to managers, who can evaluate potential restoration sites based Regarding restoration efforts, location within the estuary on their ability to promote high larval growth, settlement, and appears to be an important factor influencing the success of survival. attempts to reestablish populations of Ostrea lurida. First, water in the area needs to have residence times facilitating local OTHER THREATS TO RECOVERING POPULATIONS retention of larvae of O. lurida. Second, restoration locations should occur midbay (not too far seaward or riverward). This is Declining populations of Ostrea lurida have also been due to where high larval supply (Garcia-Peteiro unpublished, Pritchard land use changes (Clasen et al. 2010), sewage contamination 2013), and recruitment (Kimbro 2008, Deck 2011, Rimler 2014) (Galtsoff 1929), and long-term effects of sulfur liquor emissions have been observed. These midbay sites also appear to have from pulp mills in the early 1900s, which was shown to have longer retention times than sites located close to the mouth of negative effects on both reproduction and health (Hopkins et al. the bay, yet they are far enough away from fresh water that the 1935, Odlaug 1949). Logging, mining, and high boat traffic large ranges in environmental parameters observed closer to the could also be compromising bay water quality and thus, oyster head of the bay are less extreme. At the head of the bay, ranges habitats. Pollution from gasoline and motor oil are of concern, in environmental parameters are generally high because of the especially in areas of high boat traffic such as the Coos Bay proximity to the river, and recruitment is low at these sites estuary, OR, where shipping and commercial and recreational (Wasson 2010, Rimler 2014) despite ample larval supply, in fishing are prevalent activities. It has been estimated that there is some cases (Pritchard 2013). Third, in the northern part of their approximately a 10% loss of outboard fuel for each boat on the range, hard substrata should be available in the low intertidal or waterways (Clark et al. 1974). Although oysters may be able to high subtidal to allow the water to buffer and protect oysters tolerate brief exposure to motor oil and gasoline by closing their from desiccation and freezing temperatures. Fourth, tidal shell, up to 14% population mortality results after 10 days at flushing must be sufficient to allow for food resources and even dilute concentrations (Clark et al. 1974). Other sources of oxygen delivery. Lastly, summer temperatures at restoration anthropogenic disturbance, including sedimentation caused by sites must reach critical reproductive temperatures; this will topsoil runoff in areas of logging and mining, could cause facilitate spawning and increase the probability that popula- clogging of gills and respiratory tracts in bays with low water tions will become self-sustaining. If restoration efforts were movement and tidal flushing (Trimble et al. 2009). Dredging initiated at sites where the minimum temperature never rose may also affect populations by changing hydrodynamics of above the minimum threshold for spawning, the site would be bays, influencing dispersal (Pritchard et al. in preparation) and completely dependent on management-supplied spat.

LITERATURE CITED Allen, R. K. 1977. Common intertidal invertebrates of southern Beck, M. W., R. D. Brumbaugh, L. Airoldi, A. Carranza, L. D. Coen, California. Palo Alto, CA: Peek Publications. 316 pp. C. Crawford, O. Defeo, G. J. Edgar, B. Hancock, M. C. Kay, H. S. Alzieu, C. 1998. Tributyltin: case study of a chronic contaminant in the Lenihan, M. W. Luckenbach, C. L. Toropova, G. Zhang & X. Guo. coastal environment. Ocean Coast. Manage. 40:23–36. 2011. Oyster reefs at risk and recommendations for conservation, Arakawa, K. Y. 1990. Commercially important species of oysters in the restoration, and management. Bioscience 61:107–116. world. Mar. Freshwat. Behav. Physiol. 17:1–13. Bertness, M. D., S. D. Gaines, D. Bermudez & E. Sanford. 1991. Aune, T., H. Ramstad, B. Heidenreich, T. Landsverk, T. Waaler, E. Extreme spatial variation in the growth and reproductive output of Egaas & K. Julshamn. 1998. Zinc accumulation in oysters giving the acorn barnacle Semibalanus balanoides. Mar. Ecol. Prog. Ser. mouse deaths in paralytic shellfish poisoning bioassay. J. Shellfish 75:91–100. Res. 17:1243–1246. Bertness, M. D., G. H. Leonard, J. M. Levine & J. F. Bruno. 1999. Baker, P. 1995. Review of ecology and fishery of the Olympia oyster, Climate-driven interactions among rocky intertidal organisms Ostrea lurida with annotated bibliography. J. Shellfish Res. 14:501– caught between a rock and a hot place. Oecologia 120:446–450. 518. Bonnot, P. 1938. Report of the California oyster industry for 1937. Barrett, E. M. 1963. The California oyster industry, vol. 123. Sacra- Calif. Fish Game 24:191–195. mento, CA: California Department of Fish and Game. Bower, S. M., D. Hervio & G. R. Meyer. 1997. Infectivity of Bayne, B. L. 1969. The gregarious behaviour of the larvae of Ostrea Mikrocytos mackini, the causative agent of Denman Island disease edulis L. at settlement. J. Mar. Biol. Ass. U.K. 49:327–356. in Pacific oysters Crassostrea gigas, to various species of oysters. Bayne, B. L., C. J. Bayne, T. C. Carefoot & R. J. Thompson. 1976. Dis. Aquat. Org. 29:111–116. Physiological ecology of Mytilus californianus Conrad. Metabolism Bradley, W. & A. E. Seibert. 1978. Infection of Ostrea lurida and and energy balance. Oecologia 22:211–228. Mytilus edulis by the parasititc copepod Mytilicola orientalis in San Beahrs A. 2012. The decades-long comeback of Mark TwainÕs favorite Francisco Bay, California. Veliger 2:131–134. food. Smithsonian Magazine, June 2012. Breese, W. P. 1953. Rearing of the native Pacific Coast oyster larvae, Beck, M. W., R. D. Brumbaugh, L. Airoldi, A. Carranza, L. D. Coen, Ostrea lurida Carp., under controlled laboratory conditions. PhD C.Crawford,O.Defeo,G.J.Edgar,B.Hancock,M.Kay, diss., Oregon State University, Corvallis, OR. H. Lenihan, M. W. Luckenback, C. L. Toropova & G. Zhang. 2009. Breitburg, D. L., L. D. Coen, M. W. Luckenbach, R. Mann, M. Posey & Shellfish reefs at risk: a global analysis of problems and solutions. J. A. Wesson. 2000. Oyster reef restoration: convergence of harvest Arlington, VA: The Nature Conservancy. and conservation strategies. J. Shellfish Res. 19:371–377. RECENT ADVANCES ON THE BIOLOGY OF OSTREA LURIDA 269

Brumbaugh, R. D. & L. D. Coen. 2009. Contemporary approaches for Deck, A. 2011. Effects of interspecific competition and coastal ocean- small-scale oyster reef restoration to address substrate versus re- ography on population dynamics of the Olympia oyster, Ostrea cruitment limitation: a review and comments relevant for the lurida, along estuarine gradients. PhD thesis., University of Cal- Olympia oyster, Ostrea lurida Carpenter 1864. J. Shellfish Res. ifornia, Davis, CA. 28:147–161. Dinnel, P., I. Dolph, D. Elder, C. Woodward & T. Woodard. 2011. Buhle, E. R. & J. L. Ruesink. 2009. Impacts of invasive oyster drills on Restoration of the Native oyster in Fidalgo Bay, Washington–year Olympia oyster (Ostrea lurida Carpenter 1864) recovery in Willapa nine report. Mount Vernon, WA: Skagit County Marine Resource Bay, Washington, United States. J. Shellfish Res. 28:87–96. Committee. Burrell, V. G. 1986. Species profiles: life histories and environmental Dinnel, P. A., B. Peabody & T. Peter-Contesse. 2009. Rebuilding requirements of coastal fishes and invertebrates (South Atlantic): Olympia oysters, Ostrea lurida Carpenter 1864, in Fidalgo Bay, American oyster. U.S. Fish Wildl. Serv. Biological Report 82 Washington. J. Shellfish Res. 28:79–85. (11.57), U.S. Army Corps of Engineers TR EL-82-4. 17 pp. Dumbauld, B. R., K. M. Brooks & M. H. Posey. 2001. Response of an Campana, S. E. 1999. Chemistry and composition of fish otoliths: estuarine benthic community to application of the pesticide carbaryl pathways, mechanisms and applications. Mar. Ecol. Prog. Ser. and cultivation of Pacific oysters (Crassostrea gigas) in Willapa Bay, 188:263–297. Washington. Mar. Pollut. Bull. 42:826–844. Carlton, J. T. 1979. History, biogeography, and ecology of the in- Elsasser, A. B. & R. F. Heizer. 1966. Excavation of two northwestern troduced marine and estuarine invertebrates of the Pacific Coast of California coastal sites. University of California Archaeological North America. PhD diss., Davis, CA: University of California. 904 Survey. Berkeley, CA: University of California. pp. Elston, R. A., J. D. Moore & K. M. Brooks. 1992. Disseminated Carson, H. S. 2010. Population connectivity of the Olympia oyster in neoplasia of bivalve molluscs. Rev. Aquat. Sci. 6:405–466. southern California. Limnol. Oceanogr. 55:134–148. Feldman,K.L.,D.A.Armstrong,B.R.Dumbauld,T.H.DeWitt& Chapman, W. M. & A. H. Banner. 1949. Contributions to the life D. C. Doty. 2000. Oysters, crabs and burrowing shrimp: review history of the Japanese oyster drill, Tritonalia japonica, with notes of an environmental conflict over aquatic resources and pesticide on other enemies of the Olympia oyster, Ostrea lurida. Washington use in Washington State’s (USA) coastal estuaries. Estuaries Dept. Fish. Biol. Rep. 49:168–200. 23:141–176. Clark, R. C., Jr., J. S. Finley & G. G. Gibson. 1974. Acute effects of Friedman, C. S., H. M. Brown, T. W. Ewing, F. J. Griffin & G. N. outboard motor effluent on two marine shellfish. Environ. Sci. Cherr. 2005. Pilot study of the Olympia oyster Ostrea conchaphila in Technol. 8:1009–1014. the San Francisco Bay estuary: description and distribution of Clasen, J. L., J. K. Llopiz, C. E. H. Kissman, D. Marshalonis & D. L. diseases. Dis. Aquat. Organ. 65:1–8. Pascual. 2010. The vulnerability of ecosystem trophic dynamics to Galtsoff, P. S. 1929. Oyster industry of the Pacific coast of the United anthropogenically induced environmental change: a comparative States. Appendix VIII to Report of the U.S. Commissioner of approach. In: Eco-DAS VIII Symposium Proceedings. pp. 45–64. Fisheries for 1929. Bur. Fish. Doc. 1066:367–400. Coe, W. R. 1931a. Spermatogenisis in the California Oyster (Ostrea Galtsoff, P. S. 1930. The role of chemical stimulation in the spawning lurida). Biol. Bull. 61:309–315. reactions of Ostrea virginica and Ostrea gigas. Proc. Natl. Acad. Sci. Coe, W. R. 1931b. Sexual rhythm in the California Oyster (Ostrea USA 16:555–559. lurida). Science 74:247–249. Galtsoff, P. S. 1964. The American oyster Crassostrea virginica Gmelin. Coe, W. R. 1932. Development of the gonads and the sequence of the Fish. Bull. 64:1–480. sexual phases in the California oyster (Ostrea lurida). San Diego, Gibson, G. G. 1974. Oyster mortality study summary report 1966-1972. CA: Scripps Institution of Oceanography. Newport, OR: Fish Commission of Oregon Management and Coe, W. R. & W. E. Allen, 1937. Growth of sedentary marine organisms Research Division, U.S. Department of Commerce National Ma- on experimental blocks and plates for nine successive years. Bulletin rine Fisheries Service. of the Scripps Institute of Oceanography, University of California, Gillespie, G. 2009. Status of the Olympia oyster, Ostrea lurida Technical Series 4:101–136. Carpenter 1864 in British Columbia, Canada. J. Shellfish Res. 28:59–68. Coen, L. D. & M. W. Luckenbach. 2000. Developing success criteria Grason, E. W. & B. G. Miner. 2012. Preference alters consumptive and goals for evaluating oyster reef restoration: ecological function effects of predators: top-down effects of a native crab on a system of or resource exploitation? Ecol. Eng. 15:323–343. native and introduced prey. PLoS ONE 7:e51322. Cole, H. A. & E. W. Knight-Jones. 1939. Some observations and Groth, S. & S. Rumrill. 2009. History of Olympia oysters (Ostrea lurida experiments on the setting behaviour of larvae of Ostrea edulis. Carpenter 1864) in Oregon estuaries, and a description of recovering Conseil Permanent International pour lÕExploration de la Mer 14:86– populations in Coos Bay. J. Shellfish Res. 28:51–58. 105. Graham, W. M. & J. L. Largier. 1997. Upwelling shadows as nearshore Connell, J. H. 1985. The consequences of variation in initial settlement retention sites: the example of northern Monterey Bay. Cont. Shelf vs. post-settlement mortality in rocky intertidal communities. J. Res. 17:509–532. Exp. Mar. Biol. Ecol. 93:11–45. Grosholz, E. D., J. Moore, C. Zabin, S. Attoe & R. Obernolte. 2008. Cook, E. A., J. A. Shaffer, B. Dumbauld & A. B. Kauffman. 2000. A Planning for Native oyster restoration in San Francisco Bay. Final plan for rebuilding stocks of Olympia oysters (Ostreola concha- Report to California Coastal Conservancy Agreement # 05-134. phila, Carpenter 1857) in Washington State. J. Shellfish Res. Gunter, G. & J. McKee. 1960. On oyster and sulfite waste liquor. A 19:109–412. special report to the Washington State Pollution Control Commis- Couch, D. & T. J. Hassler. 1989. Species Profiles. Life histories and sion, Olympia, Washington. 93 pp. environmental requirements of coastal fishes and invertebrates Harry, H. 1985. Synopsis of the supraspecific classification of living (Pacific Northwest). Olympia Oyster. U.S. Fish Wildl. Serv. Biol. oysters (Bivalvia: Gryphaeidae and Ostreidae). Veliger 28:121–158. Rep. 82(11.124). U.S. Army Corps of Engineers, TR EL-82-4. Hertlein, L. G. 1959. Notes on California oysters. Veliger 2:5–10. 8pp. Hettinger, A., E. Sanford, T. M. Hill, A. D. Russell, K. N. S. Sato, J. Dall, W. H. 1914. Notes on west American oysters. Nautilus 28:1–3. Hoey, M. Forsch, H. N. Page & B. Gaylord. 2012. Persistent carry- Davis, H. C. 1949. On cultivation of the larvae Ostrea lurida. Anat. Rec. over effects of planktonic exposure to ocean acidification in the 105:111. Olympia oyster. Ecology 93:2758–2768. Davis, H. C. 1955. Mortality of Olympia oysters at low temperatures. Hopkins, A. E. 1935. Attachment of larvae of the Olympia oyster, Biol. Bull. 109:404–406. Ostrea lurida, to plane surfaces. Ecology 16:82–87. 270 PRITCHARD ET AL.

Hopkins, A. E. 1936. Ecological observations on spawning and early Molnar, J. L., R. I. Gamboa, C. Revenga & M. D. Spalding. 2008. larval development in the Olympia oyster (Ostrea lurida). Ecology Assessing the global threat of invasive species to marine biodiversity. 17:551–566. Front. Ecol. Environ. 6:485–492. Hopkins, A. E. 1937. Experimental observations on spawning, larval Morgan, S. G. 1995. Life and death in the plankton: larval mortality and development, and setting in the Olympia oyster, Ostrea lurida. adaptation. In: L. McEdward, editor. Ecology of Marine Inverte- Bulletin of the Bureau of Fisheries 68:437–502. brate Larvae. Boca Raton, FL: CRC Press. pp. 279–321. Hopkins, A. E., P. S. Galtsoff & H. C. McMillin. 1935. Effects of pulp Newell, R. I. E. 2004. Ecosystem influences of natural and cultivated mill pollution on oysters. Bull. U.S. Bur. Fish. 47:125–162. populations of suspension-feeding bivalve molluscs: a review. J. Imai, T., S. Sakai, H. Okada & T. Yoshida. 1954. Breeding of the Shellfish Res. 23:51–62. Olympia oyster in tanks and culture experiments in Japanese waters. Nice, H. E., M. C. Thorndyke, D. Morritt, S. Steele & M. Crane. Tohoku J. Agric. Res. 2000. Development of Crassostrea gigaslarvaeisaffectedby4- Kimbro, D. L. 2008. Evolutionary history, predation, and coastal nonylphenol. Mar. Pollut. Bull. 40:491–496. upwelling interactively influence native oyster habitat in Tomales National Research Council. 2004. Non-native oyster in the Chesapeake Bay, California. PhD diss., University of California, Davis, CA. Bay. National Academy Press. Kimbro, D. L., J. Largier & E. D. Grosholz. 2009a. Coastal Oates, M. 2013. Observations of gonad structure and gametogenic oceanographic processes influence the growth and size of a key timing in a recovering population of Ostrea lurida (Carpenter 1864). estuarine species, the Olympia oyster. Limnol. Oceanogr. PhD thesis, Eugene, OR: University of Oregon. 54:1425–1437. Odlaug TO. 1949. Effects of stabilized and unstabilized waste sulphite Kimbro, D. L., E. D. Grosholz, A. J. Baukus, N. J. Nesbitt, N. M. liquor on the Olympia oyster, Ostrea lurida. T. Am. Microsc. Soc. Travis, S. Attoe & C. Coleman-Hulbert. 2009b. Invasive species 68:163–182. cause large-scale loss of native California oyster habitat by disrupt- Orton, J. H. 1927. Observation and experiments on sex-change in the ing trophic cascades. Oecologia 160:563–575. European oyster (O. edulis): Part I. The change from female to male. Kirby, M. X. 2004. Fishing down the coast: historical expansion and J. Mar. Biol. Ass. U.K. 14:967–1045. collapse of oyster fisheries along continental margins. Proc. Natl. Orton, J. H. & C. Amirthalingam. 1931. Observations and experiments Acad. Sci. USA 101:13096–13099. on sex-change in the European oyster (O. edulis). Part II. On the Korringa, P. 1976. Farming the flat oysters of the genus Ostrea. A gonad of egg-spawning individuals. J. Mar. Biol. Ass. U.K. 17:315– multidisciplinary treatise. Amsterdam, The Netherlands: Elsevier. 324. 238 pp. Orton, J. H. 1933. Observation and experiments on sex-change in the Larsson, A. I. & P. R. Jonsson. 2006. Barnacle larvae actively select flow European oyster (O. edulis). Part III. On the fate of unspawned ova. environments supporting post-settlement growth and survival. Part IV. J. Mar. Biol. Ass. U.K. 19:1–54. Ecology 87:1960–1966. Pawlik, J. R. & C. A. Butman. 1993. Settlement of a marine tube worm Lenihan, H. S., C. H. Peterson, J. E. Byers, J. H. Grabowski, G. W. as a function of current velocity: interacting effects of hydrodynam- Thayer & D. R. Colby. 2001. Cascading of habitat degradation: ics and behavior. Limnol. Oceangr. 38:1730–1740. oyster reefs invaded by refugee fishes escaping stress. Ecol. Appl. Peter-Contesse, T. & B. Peabody. 2005. Reestablishing Olympia oyster 11:764–782. populations in Puget Sound, Washington. Washington Sea Grant Leonard, G. H. 2000. Latitudinal variation in species interactions: a test Program. pp. 1–8. in the New England rocky intertidal zone. Ecology 81:1015–1030. Peters, R. 1993. Past and current conditions of marine resources. Big Leonard, G. H., P. J. Ewanchuk & M. D. Bertness. 1999. How Quilcene Watershed Analysis. U.S. Forest Service, Olympic Region, recruitment, intraspecific interactions, and predation control species Olympia, WA. borders in a tidal estuary. Oecologia 118:492–502. Pineda, J., N. B. Reyns & V. R. Starczak. 2009. Complexity and Leonard, G. H., J. M. Levine, P. R. Schmidt & M. D. Bertness. 1998. simplification in understanding recruitment in benthic populations. Flow-driven variation in intertidal community structure in a Maine Popul. Ecol. 51:17–32. estuary. Ecology 79:1395–1411. Polson, M. P. & D. C. Zacherl. 2009. Geographic distribution and Light, S. F. 2007. The Light and Smith manual: intertidal invertebrates intertidal population status for the Olympia oyster, Ostrea lurida from central California to Oregon. Oakland, CA: University of Carpenter 1864, from Alaska to Baja. J. Shellfish Res. 28:69–77. California Press. Polson,M.P.,W.E.Hewson,D.J.Eernisse,P.K.Baker&D.C. Loosanoff, V. L., H. C. Davis & P. E. Chanley. 1966. Dimensions and Zacherl. 2009. You say conchaphila,Isaylurida: molecular shapes of larvae of some marine bivalve mollusks. Malacologia evidence for restricting the Olympia oyster (Ostrea lurida Carpen- 4:351–435. ter 1864) to temperate western North America. J. Shellfish Res. Matthiessen GC. 1970. A review of the oyster culture and the oyster 28:11–21. industry in North America. Woods Hole Oceanography Institute. Porri, F., T. Jordaan & C. D. McQuaid. 2008. Does cannibalism of Contribution No. 2528. larvae by adults affect settlement and connectivity of mussel McKernan, D. L., V. Tartar & R. Tollefson. 1949. An investigation of populations? Estuar. Coast. Shelf Sci. 79:687–693. the decline of the native oyster industry of the state of Washington, Posey, M. H., T. D. Alphin, T. K. Frazer & S. B. Blitch. 1998. Oyster with special reference to the effects of sulfite pulp mill waste on the beds as essential habitat for decapods and fish. J. Shellfish Res. Olympia oyster (Ostrea lurida). Washington Department of Fisher- 17:1311. ies Biological Report. Gig Harbor, WA: Washington Department of Pritchard, C. 2013. Distribution of larval bivalves in the Coos Bay Fisheries. 115 pp. estuary, Oregon. PhD thesis, Eugene, OR: University of Oregon. Michener, W. K. & P. D. Kenny. 1991. Spatial and temporal patterns of Qian, P. Y., D. Rittschof & B. Sreedhar. 2000. Macrofouling in Crassostrea virginica (Gmelin) recruitment: relationship to scale and unidirectional flow: miniature pipes as experimental models for substratum. J. Exp. Mar. Biol. Ecol. 154:97–121. studying the interaction of flow and surface characteristics on the Mix, M. C. 1975. Proliferative characteristics of atypical cells in native attachment of barnacle, bryozoan and polychaete larvae. Mar. Ecol. oysters (Ostrea lurida) from Yaquina Bay, Oregon. J. Invertebr. Prog. Ser. 207:109–121. Pathol. 26:289–298. Rimler, R. N. 2014. Larval supply, settlement, and post-settlement Mix, M. C. & V. Sprague. 1974. Occurrence of a haplosporidian in performance as determinants of the spatial distribution of Olympia native oysters (Ostrea lurida) from Yaquina bay and Alsea bay, oysters (Ostrea lurida) in Coos Bay, OR. PhD thesis, Eugene, OR: Oregon. J. Invertebr. Pathol. 23:252–254. University of Oregon. RECENT ADVANCES ON THE BIOLOGY OF OSTREA LURIDA 271

Rumrill, S. S. 1990. Natural mortality of marine invertebrate larvae. Strong, A. M. 1928. Notes on microscopic shells from Newport Bay, Ophelia 32:163–198. California. Nautilus 24:1–4. Sawyer, K. 2011. Settlement preference and the timing of settlement of Swinbanks, D. D. & J. L. Luternauer. 1987. Burrow distribution of the Olympia oyster, Ostrea lurida, in Coos Bay Oregon. PhD thesis, thalassinidean shrimp on a Fraster Delta tidal flat, British Colum- Eugene, OR: University of Oregon. bia. J. Paleontol. 61:315–332. Sayce, C. S. 1976. The oyster industry of Willapa Bay. In: R. D. Trimble, A. C., J. L. Ruesink & B. R. Dumbauld. 2009. Factors Andrews III, editor. Proceedings of the symposium on terrestrial preventing the recovery of a historically overexploited shellfish and aquatic ecological studies of the northwest. Cheney, WA: species, Ostrea lurida Carpenter 1864. J. Shellfish Res. 28:97–106. Eastern Washington State College Press. pp. 347–356. Troost, K. 2010. Causes and effects of a highly successful marine Scott, G. I., L. Webster, B. Thompson, W. Ellenberg, P. Comar & G. P. invasion: case-study of the introduced Pacific oyster Crassostrea Richards. 1998. The impacts of urbanization on shellfish harvesting gigas in continental NW European estuaries. J. Sea Res. 64:145–165. waters: development of techniques to identify coliform pollution Wasson, K. 2010. Informing Olympia oyster restoration: evaluation of sources. J. Shellfish Res. 17:1312–1313. factors that limit populations in a California estuary. Wetlands Seale, E. M. & D. C. Zacherl. 2009. Seasonal settlement of Olympia 30:449–459. oyster larvae, Ostrea lurida Carpenter 1864 and its relationship to Wight, N. A., J. Suzuki, B. Vadopalas & C. S. Friedman. 2009. seawater temperature in two southern California estuaries. J. Development and optimization of quantitative PCR assays to aid Shellfish Res. 28:113–120. Ostrea lurida Carpenter 1864 restoration efforts. J. Shellfish Res. Sinderman, C. J. 1974. Disease diagnosis and control in Northern 28:33–41. American marine aquaculture. New York, NY: Elsevier Scientific Zacherl, D. C. 2005. Spatial and temporal variation in statolith and Publishing Company. protoconch trace elements as natural tags to track larval dispersal. Sponaugle, S., R. K. Cowen, A. Shanks, S. G. Morgan, J. M. Leis, J. Pineda, G. W. Boehlert, M. J. Kingsford, K. C. Lindeman & Mar. Ecol. Prog. Ser. 290:145–163. C. Grimes. 2002. Predicting self-recruitment in marine populations: Zacherl, D. C., S. G. Morgan, S. E. Swearer & R. R. Warner. 2009. A biophysical correlates and mechanisms. Bull. Mar. Sci. 70:341–375. shell of its former self: can Ostrea lurida Carpenter 1864 larval shells Stafford, J. 1913. The Canadian oyster. Canada: Commission of reveal information about a recruit’s birth location? J. Shellfish Res. Conservation. pp. 1–159. 28:23–32. Steele, E. N. 1957. The Olympia oyster. Elma, WA: Fulco Publications. zu Ermgassen, P. S. E., M. D. Spalding, B. Blake, L. D. Coen, Stein, J. E., J. G. Denison & J. G. Mackin. 1959. Hexamita sp. and an B. Dumbauld, S. Geiger, J. H. Grabowski, R. Grizzle, M. Luckenbach, infectious disease in the commercial oyster Ostrea lurida. Proc. Natl. K. McGraw, W. Rodney, J. L. Ruesink, S. P. Powers & Shellfish. Assoc. 50:67–81. R. Brumbaugh. 2012. Historical ecology with real numbers: past and Stick, D. A. 2011 Identification of optimal broodstock for Pacific North- present extent and biomass of an imperilled estuarine habitat. Proc. west oysters. PhD dissertation. Corvallis, OR: Oregon State University. R. Soc. B. 279:3393–3400.