Appendix A:Estimated ci, Museum collections and the geographical survey (Figure 1)

Estimated ci:

Dumbauld et al.’s (2011) estimate of Orthione prevalence, ci,for10-38 mm carapace length, CL, Upogebiaas[ci = e (0.9023CL-0.0135CL^2-13.5884)/(1+ e (0.9023CL-0.0135CL^2-13.5884))].


Figure 1.Carapace length frequencies of: 82 Upogebia pugettensis collected from western Canadian and US estuaries between 1918 and 1976 (solid line); the estimated 36.9 effective hosts in the population (equation 4, broken line) and; the 95% Orthione griffenisdetection limit when ρ = 0.03 (equation 3, thin solid line).

Museum collections

We estimated Orthione sample detection probabilitiesfrom museum collections, based on assumptions that Allee threshold densities occurred among all North American populations previous to the 1980s. The sample included 32 Upogebia in the California Academy of Sciences (CAS) (carapace lengths [CL] ranging between 16 to 39 mm) among 1 U. pugettensis (CL 32 mm) in the Santa Barbara Museum of Natural History (SBNH) and 49 U. pugettensis from the Los Angeles County Museum of Natural History LACMNH Upogebia (CL 7-35 mm) (Appendix A, Figure 1). Orthione were not found among 8 U. pugettensis from San Francisco collected in 1859, a single specimen with no date or collector that was almost certainly collected before the 1950s or among 4 other lots of U. pugettensis from other pre-1950s sites north of San Francisco in the collections of the Harvard Museum of Comparative Zoology (MCZ) (Ardis Johnston, personal communication).

The geographical survey (Figure 1):

Previously known or reported Upogebia beds from Mexico to Canada (e.g., Bird 1982, Schmitt 1921, MacGinitie 1930, 1935, Ricketts, Calvin and Hedgpeth 1962, Stenzel et al. 1976, Thompson 1972, Swinbanks and Murray 1981, Swinbanks and Lauternaur 1987) were sampled directly in June and early July 2008 and January through March 2009 or by correspondence with other researchers since 2005.

Orthione griffenis was sampled directly in Grays Harbor, Washington (6/19/2008 – 19 shrimp, < 8 m-2); Willapa Bay, Washington (6/20/2008 - 31 shrimp, < 13 m-2, respectively); upper and lower Tillamook Bay, Oregon (7/6/2008 – 52 shrimp, 43 m-2 and 13 shrimp, < 5 m-2, respectively); upper and lower Yaquina Bay, Oregon (6/23/2008 – 222 shrimp, 185 m-2, and 6/24/2008 – 346 shrimp, 288 m-2, respectively); Coos Bay, Oregon (6/10/2008 – 28 shrimp, 17 m-2) and; Morro Bay, California (6/12/2008 – 28 shrimp, 17 m-2). Upogebia were collected from Coos Bay and Morro Bay Upogebia beds using 20 and 10 small cores, respectively.

British Columbia

The first records of Orthione in British Columbia are prior to 2005 in the Strait of Georgia, at Stanley Park, Vancouver Harbor (Lamb and Hanby, 2005, p. 280, as Ione sp.) and 2006 on the outer west coast of Vancouver Island, near Bamfield, at Ross Inlet in Barkley Sound (Williams and An, 2009, p. 117).

Vancouver Ferry terminal - Francis Choi and Trampus Goodman (University of British Columbia, Vancouver, British Columbia, personal communication), collected a single female U. pugettensis infested by a male - female O. griffenis pair, which they photographed. This single shrimp was collected on 7 September 2009 out of 28 - 15 cm diameter by 60 cm deep core samples plus 24 - 40 cm diameter by 60 cm deep core samples collected over the previous transect D of Swinbanks and Luternauer (1987, p. 324) near the border of an eelgrass bed (49o 01' 35.72" N, 123o 06' 10.14" W). Swinbanks and Luternauer (1987) found 10 burrow openings m-2 at this site in July 1977, an approximate density of 5 m-2 compared to the 0.28 m-2 density found by Choi and Goodman.

Bamfield, Vancouver Island - “Orthione are established in Bamfield Inlet (48o 48' 47.94" N, 125o 09' 25.93" W) and Grappler Inlets (48o 50’ 03.66” N; 125o 06’ 40.24” W) of Vancouver Island, BC, infesting more than 90% of the Upogebia this summer. These populations were at low densities (< 5 m-2) and consisted primarily of very large individuals, symptomatic of extended recruitment failures.” (Greg Jensen, personal communication, Fall 2008).

Washington

The first records of Orthione in Washington are 1988 in Willapa Bay (Dumbauld et al., 2011, and herein) and 1995 in southern Puget Sound, as detailed below.

Puget Sound - Upogebia was an oyster pest in many areas of Puget Sound, Grays Harbor and Willapa Bay (Stevens 1928, 1929, Posey et al. 1991, Dumbauld et al. 1996, 2001) where it was rare or absent by 2008 (Dumbauld, personal observations). Infested U. pugettensis of Freeland Town Beach and Crescent Harbor, Whidbey Island and Camano Island, Washington (48o 13’ 24.57” N; 122o 43’ 04.62” W) were first discovered on 12 July 2003 (Mary Jo Adams, personal communication). A population located in southern Puget Sound near the mouth of the Nisqually River (47o 06’ 13.33” N; 122o 43’ 57.83” W) was highly infested with Orthione in 2006 (50% prevalence, Dumbauld, personal observations). Burrowing shrimp populations declined sufficiently in some areas of Samish Bay in the late 1980s or early 1990s, to allow oyster culture operations where they had previously not been possible (Dumbauld via Bill Dewey, personal observation).A photograph of U. pugettensis posted in Telnack and Phipps (2005) was taken by Jennifer Telnack in 1995 as part of an independent study project from Eld Inlet beach, southern Puget Sound, (47°05'14" 122°58'29") on the Evergreen State College campus (Erik V. Thuesen, personal communication, February 2010). Dr. Thuesen continued: “I have caught them there many times, and have seen them with a parasitic isopod(s). A couple of years ago, I had some students doing a project on N. californiensis and its commensal copepod Clausidium vancouverense. I just double checked with one of them (Freya Goetz), and they didn't find a single specimen of U. pugettensis on the beach when they were surveying.”

Grays Harbor - Severe U. pugettensis population declines occurred in Grays Harbor where several locations that had abundant mud shrimp populations in the early 1990’s (Steve Ferraro, Kristine Feldman, and Dumbauld, unpublished data) were revisited in 2006 and had either no mud shrimp present (North Bay - 46o 58’ 56.42” N; 124o 06’ 44.15” W) or much reduced populations that were highly infested by Orthione (53% prevalence, South Bay - 46o 53’ 36.41” N; 124o 03’ 40.15” W) . Both Grays Harbor and Willapa Bay populations were at extreme low densities in 2009 (Dumbauld et al. 2011).

Willapa Bay–Previous to 1998, Upogebia abundant, widespread and significant oyster pests in the northern sections of Willapa Bay (Dumbauld et al. 2001). A population at Cedar River, Willapa Bay, Washington (46o 43’ 20.74” N; 123o 54’ 27.51” W) became extinct, between 2001 and 2002, following an exponential increase in Orthione prevalence that began in 1998 (Table 1). Mud shrimp have disappeared from many other locations in Willapa Bay and the only known Upogebia population remaining, at Goose Point (46o 37’ 35.57” N; 123o 57’ 36.73” W) is at low and declining densities and remained intensely infested with Orthione through summer of 2009 (Dumbauld et al. 2011).

Oregon

The first records of Orthione in Oregon are anecdotal accounts from Yaquina and Coos Bays between 1986 and 1988, as detailed below; 1997 in Coos Bay (below), 1999 (Yaquina Bay, Markham, 2004), and 2001 in Tillamook Bay (below).

Tillamook Bay - A dense Upogebia population identified in central western Tillamook Bay (>100 m-2), (45o 31’ 16.39” N; 123o 56’ 30.07” W) (Hancock et al. 1979) remains. However, another large population of eastern Tillamook Bay (45o 32’ 25.32” N; 123o 54’ 18.00” W) declined from 75 m-2 to less than 10 m-2 between 2007 and 2008 (Dumbauld et al. 2011). Thirty-five Upogebia specimens ranging between 3 - 4 inches in length (~25 -33 mm carapace lengths), shipped as live bait from a Tillamook Bay bait dealer and received on 25 June 2001 were 100% infested with Orthione (J. T. Carlton, personal communication).

Netarts Bay - Stout (1976) and Hancock et al. (1979) reported large “dense” U. pugettensis populations in central and eastern Netarts Bay in 1975 and 1977, respectively. A “dense” population adjacent to the road on the east shore (45o 24’ 52.80” N; 123o 56’ 04.33” W) noted by Stout (1976), and in 1986 (Chapman, personal observations) was sampled by Janssen and John Levin in October 2006. They found 24 infested Upogebia among the 56 sampled and 15 of the 19 females were infested. No shrimp were found at this site on 2 August 2008 (Chapman, personal observations). Other low density Upogebia populations persisted in the central area of Netarts Bay (45o 24’ 21.61” N; 123o 57’ 04.93” W) in summer of 2008 (Anthony D’Andrea, personal communication) and in the south bay in summer 2011 (Dumbauld, personal observation).

Siletz Bay - Upogebia pugettensis at greater than 100 m-2 occurred in an area covering less than 4,000 m2 in Siletz Bay adjacent to highway 101 (45o 55’ 31.18” N; 124o 00’ 53.70” W) in July 2007 that were noticeably less abundant in July 2008 and too rare to quantify in summer 2011 (Chapman, personal observation).

Yaquina Bay - Dense Upogebia beds cover extensive areas of Yaquina Bay as of 2009, but remain intensely infested. The major Idaho Flat Upogebia population (44o 37’ 06.09” N; 124o 02’ 27.09” W) monitored since 2005 (Smith et al. 2008) through 2009 (Dumbauld et al. 2011) has significantly declined since the 2002 survey by DeWitt et al. (2004).

Alsea Bay - The largest Upogebia population of Alsea Bay, Oregon (44o 26’ 43.61” N; 124o 03’ 25.92” W) were intensely infested in July 2007 and July 2008 (Chapman, personal observations) but remained at relatively high densities in 2009 (Chapman, personal observations).

Coos Bay - Upogebia were not found in the east or west intertidal mudflats of Coos Bay on 30 October 2006, 20 July 2007, 29 May 2008 or 10 June 2008 (Chapman and Dumbauld, personal observations). Three low density (< 1 - 17 m-2) populations were located on 10 June 2008 (Chapman, personal observations), including a minor population in a rocky beach to the southeast of the power station on the northwest shore of South Slough (< 1 m-2, 43o 21’ 10.80” N; 124o 18’ 54.20” W) and two other populations approximately 2 km south of the Charleston Bridge in South Slough (17 m-2 [above], 43o 19’ 52.00” N; 124o 19’ 36.66” W) and (< 1 m-2, 43o 21’ 10.80” N; 124o 18’ 54.20” W).

California

The first records of Orthione in California are 1992 in Morro Bay (see Introduction), 2000 in Bodega Harbor (below), and 2003 in Carpinteria (Williams and An, 2009, p. 118).

Humboldt Bay - Few U. pugettensis burrow openings (<1 m2) were detected in a survey of the northern Arcata Bay portion of Humboldt Bay, California on 29 August 2007 (Dumbauld, personal observations). Most burrows were attributed to Neotrypaea gigas (several of which were taken in yabby gun samples), but one parasitized Upogebia was collected from the low intertidal fringe along the main channel southeast of Bird Island (40o 49’ 33.86” N; 124o 09’ 26.00” W).Neotrypaea californiensis were common along the seaward side of the South Bay but the survey did not include Upogebia in this area or the central Humboldt Bay and we have not found references to their historical abundances in this bay.

Bodega Harbor - Dense Upogebia beds occurred historically on the intertidal mudflats of the northwest side of Bodega Harbor, California in the 1970s Campbell Cove, 38o 18' 41.71" N, 123o 03' 25.24" W, (Greg Jensen personal communication) and also on the same mudflats, 38o 18’ 44.97” N; 123o 03’ 32.77” W,(Mastache 1971, Thompson 1972, Ronan 1975, Standing et al. 1975, Chapman, personal observations). Upogebia were not found in three low tide transect surveys of these same northwest flats on 4 and 5 November 2007 or in two transects of the southern flats on 5 November 2007 or on 10 January 2009 (Chapman, personal observations). Greg Jensen (July 2007) wrote “Upogebia were uncommon in Bodega Harbor in 2000 and intensely infested with Orthione.” Bruno Pernet, (personal observations) found a few specimens, all infested from the mudflat adjacent to the Bodega Marine Lab entrance, 38o 18’ 46.33” N; 123o 03’ 38.73” W, in June 2009. We classified this remaining population as “collapsed” (Figure 1) but this apparently nonreproductive population is likely to be “extinct”.

Tomales Bay - Upogebia was found in stomachs of brown smoothhound sharks, Mustelus henlei, captured near Hog Island and Indian Beach, Tomales Bay, California in 1992 (Haeseker and Cech 1993). Lockington (1878) noted "This species [Upogebia] is exceedingly abundant in San Francisco and Tomales Bays, and frequently attains a length of six inches [approximately 49 mm CL!] and even more” and that "almost every specimen collected in Tomales Bay, in the month of May, bore upon its abdominal feet either the curious Isopod Phyllodurus abdominalis (Stimpson, op. cit. p. 71), or a small bivalve mollusk, Pythina [=Neaeromya] rugifera". Lockington (1878, p. 300) continues: “In only one case, out of over a hundred specimens dug up in Tomales Bay, were the mollusk [Neaeromya] and the Isopod [Phyllodurus] found in company upon the same Gebia (=Upogebia)” and “On specimens collected July 4 I did not find the bivalve, and the Phyllodurus was less common in May”. Lockington thus examined more than 100 and very likely hundredsof Tomales Bay Upogebia noting the frequencies of the two known parasitic isopods of the day but not branchial infestations that could have been Orthione. Lockington (1878) did not report an exact locality in Tomales Bay Upogebia but presumably it was near to his Preston Point locality for Neotrypaea californiensis at the north side of the mouth of Walker Creek or at Sand Point, 4 km to the north (Ricketts, Calvin, and Hedgpeth 1962). Lockington (1878) continues "While most of the smaller individuals are accompanied by a pair of P. abdominalis, the larger specimens were free from this crustacean", and "In San Francisco Bay ..... Phyllodurus is sufficiently common". MacGinitie (1935) collected Phyllodurus infested Upogebia from Tomales Bay in August 1930, presumably, from the same areas.

Ricketts, Calvin, and Hedgpeth (1962, pp. 300, 316) include Upogebia on a map made by the “Pitelka & Paulson Survey” of Sand Point mudflat, adjacent to Dillon Beach, Tomales Bay where extensive Upogebia beds occurred in the 1940s (~ 38o 13’ 51.32” N; 122o 57’ 31.56” W). The map apparently was not published elsewhere. Thompson (1972, p. 15) referred to this area as “White Gulch” where she studied Upogebia burrows that, presumably, were part of a large population. Only a cuticle and a single pre-reproductive sized live Upogebia were collected from this site and surrounding areas in the course of an extensive search made on 10 January 2009 (Chapman, personal observations). Since an existing reproductive Tomales Bay population is thus unlikely, we assume this population is statistically extinct.

Bolinas Lagoon - Upogebia was an important prey of long billed curlews in Bolinas Lagoon, California in the 1970s (Stenzel et al. 1976, and personal communication) and specimens from Pickleweed Island (37o 54’ 50.47” N; 122o 41’ 02.25” W) are in the California Academy of Sciences collections. No Upogebia were found during a detailed search of Bolinas Lagoon on 13 June 2008 (Chapman, personal observations) that included the Pickleweed Island area in particular.

San Francisco Bay - Before 1878, Upogebia was “exceedingly abundant” in San Francisco Bay, including Oakland Inner Harbor, and Hunter's Point, South San Francisco, “on rock strewn beaches”, “where they average 2 to 3 inches in length” (Lockington 1878). Three Upogebia were collected in the course of the 1911 Albatross survey from Tiburon and Sausalito (Schmitt 1921). Reproductive sized U. pugettensis in the CAS collections from San Francisco Bay include a 34 mm CL male and 31 mm CL female from the rocky intertidal of Belvedere Peninsula Point (37o 51’ 43.70” N; 122o 27’ 30.72” W) collected by J. Sutton, D. Lindberg and M. Kellogg 12 June 1975 and by Chet Chaffee et al. 14 April 1976. Many Neotrypaea gigas populations were found in searches of the Sausalito, Richardson Bay, Belvedere Peninsula and Tiburon intertidal shores in November 2006 and June 2008 but no Upogebia were found (Chapman, personal observations). Upogebia larvae collected from central and north San Francisco Bay between 1980 and 1985 (Kathy Hieb, personal communication), were as abundant as presently dominant decapod crustaceans of the bay, including Palaemon macrodactylus, Cancer spp and Neotrypaea spp. We are unaware of zooplankton sampling since 1985 that could reveal whether Upogebia larvae still occur there. However, an unidentified subtidal species of Upogebia has just been discovered in the bay in 2011 (Michael McGowan, personal communication) that could be the source of these larvae rather than possibly overlooked populations of U. pugettensis.

Elkhorn Slough - Upogebia was abundant in the 1920s (MacGinitie 1930) and in the 1930s at stations 1, 4, 5 and 6 (MacGinitie 1935, MacGinitie and MacGinitie 1949) (~37o 51’ 44” N; 122o 27’ 31” W). MacGinitie (1935), remarking on the abundant Phyllodurus Lockington (1878) found in Tomales Bay, noted that only three pairs were found in Elkhorn slough on “medium sized” individuals among populations of predominantly large Upogebia. Upogebia pugettensis were listed as a resident species in 1998 (De Vogelaere et al. 1998) and in the Elkhorn Slough National Estuarine Research Reserve final management plan of 2007-2011 (Anonymous, 2007). However, Upogebia were not found in Elkhorn Slough despite extensive searches in December 2006 and 5 November 2007 (Chapman, personal observations). Kirsten Wasson, Elkhorn SloughNational Estuarine Research Reserve, wrote in October 2008 that the Elkhorn Upogebia population could be locally extinct or close to it and that she had last seen a Upogebia "about 10 years" previously.

Morro Bay - The Upogebia bedlocated and sampled in May 2008 (35o 20’ 50.06” N; 120o50’ 58.14” W)was at less than 20 m-2 and consisted almost entirely of one year old U. pugettensis (< 25 mm CL). Individuals of this population grew approximately 6 mm to reproductive size by January 2009 and distributions of these beds and another bed to the east (35o 20’ 42.08” N; 120o50’ 39.38” W) expanded but then contracted again by May 2010. Orthione were found in all three sampling periods (Chapman, personal observations).

Carpinteria Slough - Ryan Hechinger (personal communication) found Orthione in Upogebia macginitieorum collected from the Carpinteria Salt Marsh, California (34o 23’ 53.96” N; 119o 32’ 13.22” W) but the status of that population remains unclear.

Baja California, Mexico

Campos et al. (2009) report Phyllodurus abdominalis in Todos los Santos Bay from U. macginitieorum and Progebiophilus bruscai in Tortugas Bay from U. macginitieorum but did not include records of O. griffenis. Ernesto Campos in correspondence, on 25 July 2008, reported Orthione griffenisina few reproductive sized U. macginitieorum collected in a preliminary survey of Punta Banda, Todos los Santos Bay, Ensenada 31o 40’- 31o 56’N, 116o 36’- 116o 56’W and in a much larger sample of shrimp collected later Campos et al. (2010).

Appendix A References

Anonymous (2007) Elkhorn Slough National Estuarine Research Reserve Final Management Plan 2007-2011, 338 pp.

Bird EM (1982) Population dynamics of thalassinidean shrimps and community effects through sediment modification. University of Maryland, PhD Dissertation, 151 pp.

Campos E, de Campos AR, Manriquez I (2009) Intertidal thalassinidean shrimps (Thalassinidea, Calianassidae and Upogebiidae) of the west coast off Baja California, Mexico: Annotated checklist, key for identification, symbionts. Crustaceana 82:1249-1263

Campos E, Ruíz Campos G, Delgadillo-Hinojosa J and Rodríguez Almaraz GA (2010) Especies exóticas y criptogénicas de Baja California: densidad y distribución del mejillón rayado Geukensiademissa Dillwyn, 1817 y del isópodo bopírido Orthione griffenis Markham, 2004. XVI Congr Nat Oceanog Ensenada, B.C. Mexico, 9-12 Nov, p. 59

De Vogelaere A, Holte J, Silberstein M, Jacobi M (1998) A Species List for Elkhorn Slough and Adjacent Uplands. Report to the Monterey Bay National Marine Sanctuary

DeWitt, TH., D’Andrea AF, Brown CA, Griffen BD and Eldridge PM 2004. Impact of burrowing shrimp populations on nitrogen and water quality in western North American temperate estuaries, pp. 107-118 In A Tamaki (ed.) Ecology of large biotrubators in tidal flats and shallow sublittoral sediments – from individual behavior to their role as ecosystem engineers 1-2 November 2003 Proc Nagasaki university, Nagasaki, Japan, Ministry of Education, Culture, Sports, Science and Technology, Nagasaki, University, Japan.

Dumbauld BR, Brooks KM and Posey MH (2001) Response of an estuarine benthic community to application of the pesticide carbaryl and cultivation of pacific oysters (Crassostrea gigas) in Willapa Bay, Mar Pollut Bull 42:826-844