THE VELIGER © CMS, Inc., 1999 The Veliger 42(1):17-20 (January 4, 1999)

Pea Crab, Pinna theres ostreum Say, 1817, in the Eastern Oyster, Crassostrea virginica (Gmelin, 1791): Prevalence and Apparent Adverse Effects on Oyster Gonad Development

FRANCIS X. O'BEIRN* VIMS-Eastern Shore Laboratory, P.O. Box 350, Wachapreague, Virginia 23480, USA

AND RANDAL L. WALKER University of Georgia, Marine Extension Service, Shellfish Aquaculture Laboratory, 20 Ocean Science Circle, Savannah, Georgia 31411-1011, USA

Abstract. Incidence of pea crab, Pinnotheres ostreun1 Say 1817, infestation in the eastern oyster, Crassostrea vir­ ginica (Gn1elin, 1791), was recorded and related to oyster ga1netogenic activity over 18 months. Sampling occun·ed at t\VO tidal heights (high intertidal HI and lo\v intertidal LI) at t\VO sites (House Creek, HC and Skida\vay Rive1~ SR) in Wassaw Sound, Georgia. Overall, incidence rates were 3% HC LI, 1 % HC HI, 8% SR LI, and 4% SR HI. At both tidal heights at HC, no differences \Vere observed in gonad area between those oysters \Vith and without pea crabs. At SR (where overall incidences \Vere higher), oysters \Vithout pea crabs had significantly higher gonad area values than those oysters with pea crabs present. These results suggest that at higher incidences of pea crab infestation, oyster reproductive capabilities could be impacted, and support the claim that the pea crab/oyster relationship is a parasitic one.

INTRODUCTION tologically. Pea crab presence and absence \Vas recorded in the oysters and these data were then related to the The brachyuran pea crab, Pinnotheres ostrezon Say, 1817, gonad condition of the oysters throughout the san1pling has been observed in a nutnber of bivalve species, e.g., period. Mytilus edulis Linnaeus, 1758, Geukensia denlissa (Dill­ \Vyn, 1817), Anonzia sirnplex d'Orbigny, 1842, and Pecten sp. (Williams, 1984). Ho\vever, it is pri111arily a parasite SITE DESCRIPTION AND METHODS (formerly considered a conunensal) of the eastern oyster, The two sites chosen for this investigation are sho\vn in Crassostrea virginica (Gmelin, 1791). This pea crab is Figure 1. House Creek (HC), a shallow sheltered creek, found predominantly in the western Atlantic from Mas­ is located on the northern end of Wass aw Sound, Georgia. sachusetts, United States, to Santa Catarina in Brazil This site is characterized by relatively high salinities (> (\Villiams, 1984). The prevalence of the pea crab in oys­ 25 %0) and is sheltered from wave action. The Skida\vay ters along the eastern seaboard of the United States has River (SR) site, under the Skida\vay Institute of Ocean­ generally been high, \Vith prevalences of up to 100% in ography dock on the north end of Skida\vay Island, has some subtidal oyster populations in the Chesapeake Bay 1nore variable salinities and is exposed to higher wave (Galtsoff, 1964). Ho\vever, records of pea crab occu1rence action from passing boats than the House Creek site. in the southeastern United States and especially coastal 'l\vo tidal heights \Vere chosen for this study. The low­ Georgia are scant. Linton (1968) stated that the occur­ intertidal (LI) area \Vas that area in and around the mean rence of pea crabs in subtidal oysters in coastal Georgia low \Yater n1ark. The high-intertidal (HI) area \Vas des­ was 100%. Ho\vever, the vast majority of Georgia oysters ignated as the area above the region designated by the occur intertidally (Hanis, 1980). Parks (1968) reported tidal level at approximately 3 hours after mean lo\v \Vater. that there were substantially higher proportions of pea In coastal Georgia, the majority of oysters occur bet\veen crabs in oysters found subtidally than in those found in­ these t\vo intertidal boundaries. tertidally. In the present study, oysters \Vere satnpled over Sampling commenced in June 1993 and continued on a pe1iod of l 1h years, and the gonads were exan1ined his- a bi\veekly basis until the end of September 1993, when inonthly sampling took place. Monthly sampling contin­ *Corresponding author: Telephone: (757)787-5837, fax: ued until January 1994. Biweekly san1pling reco1nmenced (757)787-5831, c-n1ail: [email protected] in April 1994 through September 1994. Page 18 The Veliger, Vol. 42, No. 1

Table 1 Percent of oysters, Crassostrea virginica, according to presence or absence of pea crabs, Pinnotheres ostreu111. Also given (in parentheses) is the absolute number of oysters in each category.

PEA. CRAB Present Absent HOUSE CREEK HIGH INTERTIDAL 1%(4) 99% (394) LO"\V INTERTIDAL 3% (13) 97% (380) SI<:IDA,VAY RIVEll HIGH INTERTIDAL 4% (16) 96% (380) LO"\V INTERTIDAL 8% (33) 92% (364)

of oysters sa1npled throughout the study contained pea Figure 1 crabs (Table 1). The lowest proportion of pea crabs \\las \Vassa\\' Sound, Georgia \Vith the t\VO sainpling sites indicated: at the House Creek high intertidal site \Vhere 1% of the (l) House Creek and (2) Skida\vay River near the Skida\vay In­ oysters contained pea crabs (Table 1). \Vithin the sa1u­ stitute of Oceanography (SkIO). pling periods, the highest incidence of pea crabs in oys­ ters \Vas found in the Skida\vay Lo\V Intertidal oysters in At each san1pling period, 20 (n = 20) adult oysters April, 1995 where 21 % (4 of 19) of the oysters contained were taken fro1n each tidal height at each site. Upon pea crabs. No oysters \Vere found containing more than shucking, the tissue \Vas examined and the presence or one pea crab. absence of pea crabs were recorded. A transverse tissue There were no significant differences in gonad area be­ section (5 mm) was dissected from each shucked oyster t\veen those oysters with pea crabs and those without, at and \Vas processed for histological exa1nination and qual­ both tidal heights at House Creek (HI P ~ 0.4152 and LI itative and quantitative analysis of the gonad tissue ac­ P ~ 0.8366; Table 2). cording to the 1nethods outlined in O'Beirn et al. (1996). The high intertidal oysters at Skidaway River had sig­ The quantitative para1nctcr used in this study \Vas gonad nificantly higher (P = 0.0085) gonad area in oysters \Vith­ area which accounted for that proportion, in a standard out pea crabs, than those with pea crabs (Table 2). The viewing area of a histological section of the oyster's tis­ low intertidal oysters also had significantly higher gonad sue, occupied by gonad. area values (P = 0.0117) in oysters \Vhere pea crabs \Vere absent than those \Vith pea crabs present (Table 2). Statistical Analysis Single factor repeated measures analysis \Vas ca1Tied out on the data whereby all of the independent variables (oyster height, gonad area) \vere grouped into t\vo cate­ Table 2 gories-pea crabs present or pea crabs absent. '1\vo de­ Percent gonad area of oysters, Crassostrea virginica, ac­ pendent variables _were examined in the analysis-of-vari­ cording to presence or absence of pea crabs, Pinuotheres ance (ANOVA): pea crab presence/absence and sampling ostreu111. Also given are the p-values of repeated nlea- periods. No interaction term \Vas detennined. The varia­ sures analysis using ANOVA. tions fron1 the grand n1ean due to pea crabs and sa1npling periods \Vill have been accounted for \Vith ren1aining de­ PEA CRAB ·' viations being the source of error. All proportional data Present Absent p-value \Vas arcsine square-root transformed prior to analysis. An arbitrary value of (o: = 0.05) \Vas chosen as the signifi­ HOUSE CREEK cance level for each ANOVA. HIGH INTERTIDAL 38.4% 55.4% 0.4152 LOW INTERTIDAL 54.5% 56.8% 0.8366 RESULTS SKIDAWAY RIVER HIGH INTERTIDAL 38.4% 56.9% 0.0085 The highest recorded proportion of pea crabs in oysters LOW INTERTIDAL 42.0% 52.5% 0.0117 was at the Skidaway River 1ow intertidal site, \Vhere 8% F. X. O'Beirn & R. L. Walker, 1999 Page 19

DISCUSSION relationship bet\veen presence or absence of pea crabs in Mytilus edulis and salinity. The nutuber of pea crabs found in oysters in our study is The presence of pea crabs \Vithin the mantle cavity of substantially lo\ver that those reported previously for oys­ bivalves has been determined to have an adverse effect ters in coastal Georgia. Not surprisingly, in our study, on the host 1nollusk. Physical damage to the gilJs, palps, oysters located near the low-tide n1ark had higher nu1n­ and gonads of the bivalves has been recorded by a variety bers of pea crabs than those located higher in the inter­ of authors (Stauber, 1945; McDermott, 1962; Dix, 1973; tidal zone. A sintllar phenomenon \Vas rcpo1ted by Beach Jones, 1977). The presence of pea crabs, Pinnotheres n1a­ (1969) in North Carolina. Ho\vcver, the maxitnun1 pro­ culatus Say, 1818, \Vas deemed responsible for adversely portions at any one intertidal height and site of 8% \Vas iinpacting filtration and oxygen consu1nption rates in My­ substantially lo\ver than that of 100% in subtidal oysters tilus edulis (Bicrbau1n & Shum\vay, 1988), as \Veil as as reported previously by Linton (1968). Parks (1968) did having an apparent negative impact on gro\vth rates in record higher instances of pea crabs in subtidal oysters nutrient-poor environments (Bierbau1n & Ferson, 1986). than inte1tidal oysters. Ho\vever, the values in Park's Tablada & Lopez-Gappa (1995) demonstrated that Myti­ (1968) study \Vere in terms of nu1nber of pea crabs ob­ lus edulis individuals harboring n1ature fe1nale pea crabs, tained from a specific nu1nber of oysters necessary to give Tu1nidotheres (Pinnotheres) nzaculatus (Say), were sig­ one pint of oyster n1eat. The nun1ber of oysters differed nificantly sn1aller and had lo\ver dry weights than those considerably between the sites (tidal heights). Therefore, mussels \Vithout pea crabs. Bay scallops, Argopecten ir­ comparison of Park's (1968) data to those obtained in this radians concentricus (Say, 1822), containing adult feinale study can only be cursory. The disparity bet\veen the re­ pea crabs tended to \Veigh less and were smaller than sults of Linton (1968) and this study can be accounted those scallops without pea crabs in Bogue Sound, North for by the differences in sa1npling location (subtidal ver­ Carolina (Krnczynski, 1972). Havert (1958) determined sus intertidal, respectively). Ho\veve1~ given that the ma­ that oysters, Crassostrea virginica, containing pea crabs, jority of oysters in coastal Georgia are located intertidal1y Pinnotheres ostreun1, had significantly lo\ver dry 111eat (Harris, 1980), the propo11ions reported herein are per­ weight and condition indices than oysters \Vithout pea haps n1ore reflective of pea crab incidence in oysters in crabs. Kruczynski (1972) noted that in the presence of the region. large female pea crabs, the host bivalves tended to have In Dela\vare Bay, Flower & McDermott (1952) noted reduced gan1etogenic output, \Vhich \Vas attributed to that the proportion of oysters containing pea crabs \Vas physical pressure on the gonads. higher as they sainpled fro1n the upper reaches of the bay At both sites in our study, oysters with pea crabs pre­ toward the ocean, which was conco1nitant with an in­ sent had lo\ver gonad area values overall than oysters \Vithout the pea crabs (Table 2). At the House Creek site, crease in salinity. Such a pattern \Vas not observed in this no significant difference in gonad area \Vas determined study. In fact, it appears that the higher incidences of pea between those oysters with or \Vithout pea crabs. \Ve at­ crabs \Vere found at the Skidaway River site, \Vhich tra­ tribute tltls to insufficient numbers of infested oysters ob­ ditionally has lo\ver salinities (O'Beirn et al., 1995, 1996; tained fro1n this site. The differences at the Skida\vay Spiuck et al., 1995). The reason for this apparent reversal River site \Vere statistically significant, at both tidal in prevalence is unclear, but it n1ight be related to the heights. In a parallel study (O'Bcirn, unpublished stud­ exact location of the House Creek sampling site. All oys­ ies), oysters in the high intertidal zone tended to have ters \Vere removed fro1n a small sheltered tidal creek, higher quantitative gametogenic para1neters than oysters which is subject to high temperature fluctuations on a lo\ver down, suggesting that the high intertidal zone \Vas daily basis. O'Beirn et al. (1995) reported an 8°C water less stressful to the oyster than previously hypothesized temperature change at this site in the space of 8 hours in (O'Beirn, unpublished studies). In this study, this appar­ 1991. Also, because of the shallo\v nature of the creek, ent negative itnpact of pea crabs on oyster gonad quantity it is subject to higher salinity fluctuations caused by fresh­ was not confined to these supposedly more stressful en­ water iunoff fron1 the marsh, originating from stonns viron1nents as was the case with Mytilus edulis infested which are frequent in the sum1ner n1onths in coastal Geor­ with Pinuotlleres n1aculatus (Bierbaum & Ferson, 1986). gia. Pea crab developn1ent is inhibited by salinities less The observation in this study that the presence of pea than 15%0 (Beach, 1969). Assuming the salinities \Vill crabs corresponded \Vith lower gonad area 1neasurements drop below 1530, such factors ntlght inhibit free-s\vin1- in oysters \vould question the classification of pea crabs ming invasive stages from surviving and hence infesting as a conunensal of oysters. Haines ct al. (1994) proposed oysters, at this particular site. A 1nore comprehensive in­ that the relationship bet\veen female pea crabs and their vestigation of pea crab incidences along a salinity gra­ molluscan hosts be classified as hue parasitism, as the dient in the Wassa\v Sound, Georgia area would need to female is rarely found free-living outside of the host. The be carried out to confirm that our findings \Vere not ano1n­ results of the findings herein go further to suggest that alous. It must be noted that Kruczynski (1974) found no the pea crabs negatively i1npact the fitness of oysters. The Page 20 The Veliger, Vol. 42, No. 1 significance of these results in terms of pea crab influence HAVEN, D.S. 1958. Effects of pea crabs, Pinnotlteres ostreu111, on oyster reproduction, 1nust be tempered by the fact that on oysters, Crassostrea virginica. Proceedings of the Na­ the infestation rates observed were lo\v. Consequently, tional Shellfisheries Association 49:77-86. ]ONES, J. B. 1977. Natural history of the pea crab in \Vellington the impact on the oyster populations in Georgia would Harbour, Ne\V Zealand. Ne\V Zealand Journal of Marine and appear to be minimal. Ho\vever, given the high rates of Freslnvater Research 11 :667-676. pea crab infestation in oysters reported elsewhere, the ap­ KRUCZYNSKI, \V. L. 1972. The effect of the pea crab, Pinnotheres parent negative impact may be extensive and could have 111aculatus Say, on growth of the bay scallop, Argopecten more far-reaching implications. irradians concentricus (Say). Chesapeake Science 13:218- 220. KRuczYNSKT, \\'. L. 1974. Relationship between depth and oc­ ACKNOWLEDGMENTS currence of pea crabs, Pinnotheres 111aculatus, in blue 1nus­ sels, A1ytilus edulis, in the vicinity of \Voods Hole Massa­ The authors \Vish to thank Michelle L. Jansen who helped chusetts. Chesapeake Science 15:167-169. \Vith the histological samples. This \York was supported LINTON, T. L. 1968. Feasibility of raft culturing oysters in Geor­ by the University of Georgia Marine Extension Service gia. Pp. 69-73 in T. L. Linton (ed.), Proceedings of the Oys­ and the Georgia Sea Grant College Progran1 under grant ter Culture \Vorkshop, July 11-13, 1967. University of Geor­ number NA 84AA-D-00072. gia and Georgia Game and Fisheries Con1mission, Marine Fisheries Division, Contribution Series Nu1nber 6. h1cDERMOIT, J. J, 1962. The incidence and host-parasite rela­ LITERATURE CITED tions of pinnotherid crabs (Decapoda, Pinnotheridae). Pro­ ceedings of the First National Coastal Shallow \Yater Re­ BEACH, N. \V. 1969. The oyster crab, Pinnotheres ostreu111 Say, search Conference. 1961:162-164. in the vicinity of Beaufort North Carolina. Crustaceana 17: O'BEIRN, R X., P. B. HEFFERNAN & R. L. \VALK.ER. 1995. Pre­ 87-199. litninary recruitinent studies of the eastern oyster, Crassos­ BIERBAUM, R. M. & s. FERSON. 1986. Do sy1nbiotic pea crabs trea virginica, and their potential applications in coastal decrease growth rates in n1ussels? Biological Bulletin 170: Georgia. Aquaculture 136:231-342. 51-61. O'BEIRN, R X., P. B. HEfl'ERNAN, R. L. \VAT.KER & M. L. JANSEN. BIERBA1Thf, R. M. & s. E. SHUM\VAY. 1988. Filtration and oxygen 1996. 'Young of the year' oyster, C'rassostrea virginica, re­ consu1nption in 1nussels, Mytilus edulis, \Vith and \Vithout production in coastal Georgia. Estuaries 19:651-658. pea crabs, Pinnotheres tnaculatus. Estuaries 11 :264-271. PARKS, P. 1968. A con1parison of chemical co1nposition of oys­ DIX, T. G. 1973. Mantle changes in the pearl oyster Pinctada ters (Crassostrea i•irginica) from different ecological habi­ 111axi111a induced by the pea crab Pinnotheres villosulus. The tats. Pp. 147-173 in T. L. Linton (ed.), Proceedings of the Veliger 15:330-331. Oyster Culture \Vorkshop, July 11-13, 1967. University of FLOWER, R B. & J. J. McDERMOIT. 1952. Observations on the Georgia and Georgia Game and Fisheries Com111ission, Ma­ occurrence of the oyster crab, Pinnotheres ostreu111, as re­ rine Fisheries Division, Contribution Series Nu1nber 6. lated to oyster dainage in Dela\vare Bay. Proceedings of the SPRUCK, C.R., R. L. \VALKER, M. L. S\\'EENEY & D. H. HURLEY. 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Survey of the Intertidal and Subtidal Oyster lantic. Journal of Shellfish Research. 14:417-423. Resources of the Georgia Coast. Georgia Depa11n1ent of Nat­ \VILLTAMS, A. B. 1984. Shriinps, Lobsters and Crabs of the At­ ural Resources, Coastal Resources Division (Project No. 2- lantic Coast of the Eastern United States, Maine to Florida. 234-R), Bn1ns,vick, Georgia. 44 pp. S1nithsonian Institution Press: \Vashington D.C. 550 pp.

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