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Aquatic Invasions (2009) Volume 4, Issue 1: 105-110 This is an Open Access article; doi: 10.3391/ai. 2009.4.1.11 © 2009 The Author(s). Journal compilation © 2009 REABIC

Special issue “Proceedings of the 2nd International Invasive Sea Squirt Conference” (October 2-4, 2007, Prince Edward Island, ) Andrea Locke and Mary Carman (Guest Editors) Research article

Lobsters and as potential vectors for tunicate dispersal in the southern Gulf of St. Lawrence, Canada

Renée Y. Bernier, Andrea Locke* and John Mark Hanson and Canada, Gulf Fisheries Centre, P.O. Box 5030, Moncton, NB, E1C 9B6 Canada * Corresponding author E-mail: [email protected]

Received 20 February 2008; accepted for special issue 5 June 2008; accepted in revised form 22 December 2008; published online 16 January 2009

Abstract

Following anecdotal reports of tunicates on the of rock ( irroratus) and American (Homarus americanus), we evaluated the role of these and northern lady crab ocellatus as natural vectors for the spread of invasive tunicates in the southern Gulf of St. Lawrence. Several hundred adult specimens of crabs and lobster from two tunicate- infested estuaries and Northumberland Strait were examined for epibionts. Small patches of Botrylloides violaceus were found on rock crabs examined from Savage Harbour and a small colony of Botryllus schlosseri was found on one lobster from St. Peters Bay. Lobster and lady crab collected in Northumberland Strait had no attached colonial tunicates but small sea grapes (Molgula sp.) were found attached on the underside of 5.5% of the rock crab and on 2.5% of lobster collected in Northumberland Strait in August 2006. Lobster and rock crab clearly represent a vector for the spread of invasive tunicates regionally and wherever living are shipped globally.

Key words: invasive tunicates, epibiont dispersal, natural transport vectors

Introduction towards natural vectors of spread. There are, however, anecdotal reports of tunicates occurring Since about 1998, the viability of the bivalve on shells of crabs and caught in industry in eastern Canada, and commercial fisheries in these waters. To confirm particularly in Prince Edward Island (PEI, Figure the possibility that large crustaceans can 1), has been challenged by the colonization and transport invasive tunicates on their carapaces, spread of several non-indigenous tunicate we collected and examined adult specimens of species: the clubbed tunicate (Styela clava crab and lobster collected from two tunicate Herdman, 1882), first detected in 1997; the infested estuaries (St. Peters Bay and Savage golden star tunicate (Botryllus schlosseri (Pallas, Harbour, PEI) and the Northumberland Strait to 1766)) in 2001; the violet tunicate (Botrylloides determine the presence/absence of invasive violaceus (Oka, 1927)) in 2002; and the vase tunicate (Ciona intestinalis (Linnaeus, 1767)) in tunicates and other epibionts. The potential host 2004 (Locke et al. 2007, Ramsay et al. 2008). species examined were The rapid spread of these non-indigenous (Homarus americanus H. Milne-Edwards, 1837), tunicates along the PEI coast has prompted Atlantic rock crab ( Say, 1817), several investigations into the vectors facilitating and northern lady crab ( their dispersal. Much of the emphasis has been (Herbst, 1799). Lobster and rock crab were on processes related to the bivalve aquaculture expected to occur in all three study areas, but industry, recreational boating, and commercial northern lady crab were expected to be found boating for wide-range dispersal (e.g., papers in only in Northumberland Strait (Voutier and this issue). Scant attention has been directed Hanson 2008).

105 R.Y. Bernier et al.

Methods stage of all lobsters was estimated by means of a shell durometer, and the second pleopods were During November 2005, artificial structures in clipped and preserved in 95% ethanol for St. Peters Bay and Savage Harbour (Figure 1) subsequent analysis in the laboratory (after exhibited moderate to high infestations of golden Comeau and Savoie 2001). star (Botryllus schlosseri) and violet Crab and lobster from Northumberland Strait (Botrylloides violaceus) tunicates. Rock crab and (Figure 1) were also inspected for tunicates and American lobster were collected on 3-4 other epibionts during a bottom trawl survey on November by means of lobster traps baited with 4-5 August 2006 (survey details in Voutier and . Ten traps were set in each bay (5 traps Hanson 2008). At the time of the survey, B. in each of the inner and outer halves of the bays) violaceus was highly abundant and B. schlosseri for 24 hours. Each captured was was in low abundance off Borden (PEI). B. measured ( length CL in mm for lobster; violaceus was found at Cape Tormentine (NB) carapace width CW in mm for crabs), sex approximately a month later. When epibionts determined, the presence or absence of tunicates were detected, the crab or lobster was taken to and other epibionts determined, and the percent the laboratory for detailed examination and coverage of epibionts estimated. The molting identification of the epibiont.

Figure 1. Map of southern Gulf of St. Lawrence, Canada, showing locations sampled in November 2005 (Savage Harbour and St. Peters Bay), Northumberland Strait (yellow dot) sampled in August 2006 and other place names mentioned in the text.

106 Lobsters and crabs as potential vectors for tunicate dispersal

Small sea grapes (Molgula sp., Figure 3) were Results discovered either in clusters or individually on 5.4% of rock crab from St. Peters Bay and on No invasive tunicates were found on any of the 5.5% of those from Savage Harbour. These 112 rock crab from St. Peters Bay. Small patches Molgula sp. ranged in size from 0.8-10 mm in of Botrylloides violaceus (from 2-9 mm in dia- width and 0.5-12 mm in length. Other epibionts meter; Figure 2) were found on the carapaces of (e.g., Anomia simplex d’Orbigny, 1847, 5 of 275 rock crabs from Savage Harbour. How- Crepidula fornicata (Linnaeus, 1758), Crepidula ever, the most common rock crab epibionts were plana Say, 1822, and various sponges and green, red and brown algae, which were found on bryozoans) occurred on 6.3% and 4.7% of rock 58% and 64% of rock crab examined from St. crab from Savage Harbour and St. Peters Bay, Peters Bay and Savage Harbour, respectively. respectively.

Figure 4. Colony of Botryllus schlosseri (14 mm in Figure 2. Newly settled Botrylloides violaceus on dorsal diameter) on large (92 mm carapace length) female surface of a commercial-size (>105 mm in carapace width) American lobster (Homarus americanus) from St. Peters rock crab Cancer irroratus collected from Savage Harbour, Bay, Canada. The orange organism to the right of the circled Canada (Photo: N. MacNair). tunicate colony is a sponge (Photo: A. Nadeau).

Figure 3. Patch of ten Molgula sp. clustered together on Figure 5. Molgula citrina (4 mm in width X 4 mm in ventral surface of Cancer irroratus from St. Peters Bay, length) on male American lobster (Homarus americanus) Canada (Photo: A. Nadeau). from Northumberland Strait, Canada (Photo: A. Nadeau).

107 R.Y. Bernier et al.

The six lobster collected from Savage Harbour The extent to which large crustaceans serve as were free of epibionts. In contrast, eight of 66 vectors of spread of invasive tunicates (or any lobster collected from St. Peters Bay had bryo- other invasive species group) will depend on the zoans on them, and a colony (14 mm in dia- distance traveled and the frequency of migration meter) of Botryllus schlosseri was found on the between estuarine and coastal habitats. mid-ventral surface of one large female lobster Unfortunately, relatively little is known about (92 mm CL, Figure 4), which was in intermolt the migrations of commercial decapods in the stage C4 as described by Comeau and Savoie estuarine and coastal waters of the southern Gulf (2001). of St. Lawrence. Lobster travel seasonally as On 4-5 August 2006, 199 lobster and 126 lady much as 86 km each way in Northumberland crab from Northumberland Strait were examined. Strait (Bowlby et al. 2007) and to a maximum of Unfortunately, no rock crab were caught. Non- 24 km off the northern shore of Prince Edward indigenous tunicates were not found on any Island (Comeau and Savoie 2002). Preliminary lobster or lady crab; however, 2.5% of lobster data from an acoustic tagging study conducted in had Molgula sp. attached on their ventral the Montague/Brudenell (PEI) estuarine system surface, typically between pereopods 2 and 4. suggest that rock crab move seasonally from at Most Molgula could not be identified to species, least 7 km into the estuary to locations in coastal but the native Molgula citrina Alder and waters outside of the estuary; however, the Hancock, 1848 was identified on one of the large potential for movement between estuaries was (144 mm CL) male lobster (Figure 5). not investigated (L. Comeau, Fisheries and Oceans Canada, unpublished data). Given these extensive movements, and the large populations Discussion involved, further study of the importance of crab and lobster as vectors of regional spread of Even though invasive tunicates were found on a invasive tunicates appears warranted. relatively low proportion of the rock crab and Invasive tunicates may only be able to spread lobster from Savage Harbour, St. Peters Bay, and to non-infected areas on large crustaceans if they Northumberland Strait, these crustaceans are can remain attached for extended periods. clearly susceptible to colonization by non- Several defensive mechanisms (including indigenous and native epibionts. Moreover, this substratum wettability, production of chemical represents a significant potential vector for repellants/toxins and mechanical sloughing, spread of invasive tunicates because there are grooming and abrasion) have been suggested to many millions of adult crab and lobster in the diminish the colonization success of epibionts southern Gulf of St. Lawrence where thousands (Wahl 1997). However, surface wettability was of tonnes are landed each year (Department of not found to be an efficient antifouling defense Fisheries and Oceans Canada 2002, 2007). mechanism for crustaceans in general (Becker et The composition of the fouling community al. 2000) and neither was mechanical grooming appeared to differ between crustaceans captured for brachyuran crabs (Bauer 1989). Behavioral in estuarine versus more open coastal waters. patterns such as sediment burrowing, hiding in Algae were by far the most common epibionts of amongst hard substrates, and emersion from rock crab in estuarine waters of Savage Harbour water (especially for intertidal species) seem to and St. Peters Bay. In contrast, lady crab and be more efficient defenses against epibiont lobster from Northumberland Strait had very few colonization (Becker and Wahl 1996). Indeed, algal epibionts; however, Molgula sp. was there were remarkably few epibionts on the present on crustaceans from both estuarine and northern lady crab examined in this study, and coastal habitats, occurring on 5.5% of rock crab this is a crab that spends much of its time buried in estuaries and on 2.5% of lobster from deep in sand (Barshaw and Able 1990; Northumberland Strait. The limited information Sponaugle and Lawton 1990). Finally, molting on the fouling community of the snow crab and molt frequency are the most obvious means ( opilio (Fabricius, 1788)) that for crustaceans to rid their of occur in the deeper offshore waters of the epibionts. southern Gulf of St. Lawrence suggests Molting by crabs and lobsters clearly would bryozoans (94.5%) and polychaetes (68.8%) affect the success of epibiont colonization and were the most common epibionts, and no the frequency of molting almost certainly affects tunicates were observed (Savoie et al. 2007). the rate and extent of spread of epibionts.

108 Lobsters and crabs as potential vectors for tunicate dispersal

Although molting might delay the dispersal of References tunicates by these crustaceans, it would most likely not eliminate dispersal since invasive Abelló P, Villanueva R, Gili JM (1990) Epibiosis in deep- tunicates may be able to survive and proliferate sea crab populations and behavioral characteristics of the host. Journal of Marine Biological Association 70: on the discarded , assuming the 687-697, doi:10.1017/S0025315400058975 exoskeleton is not immediately consumed by a Barshaw DE, Able KW (1990) Deep burial as a refuge for lobster or crab, as often occurs. Some studies lady crabs Ovalipes ocellatus: comparisons with blue suggest that crustaceans with longer inter-molt crabs sapidus. Marine Ecology Progress Series 66: 75-79, doi:10.3354/meps066075 duration (i.e. older individuals or ovigerous Bauer RT (1989) Decapod crustacean grooming: Functional females) host more epibionts than those with morphology, adaptive value, and phylogenetic shorter inter-molt periods (Abelló et al. 1990, significance. In: Felgenhauer BE, Watling L, Thistle Gili et al. 1993, Shields 1992). Consequently, AB (eds) Functional morphology of feeding and grooming in Crustacea, Crustacean Issues 6, Schran FR because molting frequency decreases with age, and Balkema AA (eds), Rotterdam, Brookfield, pp 49- the larger and older lobster and rock crab might 73 represent more of a threat for tunicate dispersal Becker K, Wahl M (1996) Behaviour patterns as natural than younger individuals that molt at least antifouling mechanisms of tropical marine crabs. Journal of Experimental Marine Biology and Ecology annually. 203: 245-258, doi:10.1016/0022-0981(96)02575-0 Our results indicate that lobster and rock crab Becker K, Hormchong T, Wahl M (2000) Relevance of should be considered as likely vectors for crustacean carapace wettability for fouling. regional transport and spread of tunicates within Hydrobiologia 426: 193-201, doi:10.1023/A:100391 8512565 the southern Gulf of St. Lawrence. Since our Bowlby HD, Hanson JM, Hutchings JA (2007) Resident and study was not focused in areas where Ciona dispersal behavior among individuals within a intestinalis and Styela clava are abundant, we do population of American lobster Homarus americanus. Marine Ecological Progress Series 331: 207-218, not have any indication that these solitary doi:10.3354/meps331207 invasive species can be transported by means of Comeau M, Savoie F (2001) Growth increment and molt epibiosis on crab or lobster. Although Styela frequency of the American lobster (Homarus clava has been reported to occur on the carapace americanus) in the southwestern Gulf of St. Lawrence. Journal of Crustacean Biology 21: 923-936, doi:10.1651 of rock crab (Thompson and MacNair 2004), it /0278-0372(2001)021[0923:GIAMFO]2.0.CO;2 remains to be determined if this is a common Comeau M, Savoie F (2002) Movement of American lobster occurrence. Lastly, living lobster are extensively (Homarus americanus) in the southwestern Gulf of St. Lawrence. Bulletin 100: 181-192 shipped between processing plants and holding Department of Fisheries and Oceans (2002) Southern Gulf pens in Atlantic Canada and all parts of the USA. of St. Lawrence rock crab (Lobster areas 23, Thus, they may represent a hitherto poorly 24, 25, 26A and 26B). Canadian Science Advisory documented means of spread of hitchhiking alien Secretariat Stock Status Report C3-04: 1-7 Department of Fisheries and Oceans (2007) Framework and marine species between marine waters. Given the assessment for lobster (Homarus americanus) in the long distances that live lobster are shipped southern Gulf of Saint Lawrence areas (indeed, worldwide), a thorough investigation 23, 24, 25, 26A and 26B. Canadian Science Advisory into the identity, prevalence, and invasion Secretariat Science Advisory Report 2007/35: 1-12 Gili J-M, Abelló P, Villanueva R (1993) Epibionts and potential of the epibiont community on lobster intermoult duration in the crab piperitus. would appear warranted. Marine Ecology Progress Series 98: 107-113, doi:10.33 54/meps098107 Locke A, Hanson JM, Ellis KM, Thompson J, Rochette R Acknowledgements (2007) Invasion of the southern Gulf of St. Lawrence by the clubbed tunicate (Styela clava Herdman): Potential mechanisms for invasions of Prince Edward The authors wish to thank Ken Campbell from the Prince Island estuaries. Journal of Experimental Marine Edward Island Fishermen’s Association for logistical Biology and Ecology 342: 69-77, doi:10.1016/j.jembe. assistance and his collaboration with local fishers from 2006.10.016 Savage Harbour and St. Peters Bay for sample collection Ramsay A, Davidson J, Landry T, Arsenault T (2008) and Marc Lanteigne (Fisheries and Oceans Canada) for Process of invasiveness among exotic tunicates in providing additional funding to complete field sampling. We Prince Edward Island, Canada. Biological Invasions also wish to thank the crew of the Fisheries and Oceans 10: 1311-1316, doi:10.1007/s10530-007-9205-y Canada research vessel “Opilio” for their assistance with Savoie L, Miron G, Biron M (2007) Fouling community of sampling in the Northumberland Strait. Thanks to A. the snow crab in Atlantic Canada. Nadeau, S. Bosman and S. Richardson for technical Journal of Crustacean Biology 27: 30-36, doi:10.1651/S- assistance in the field and/or laboratory, to B. Comeau and 2722.1 R. Doucette for lobster laboratory analysis, and to N. MacNair for use of his photograph.

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Shields JD (1992) Parasites and symbionts of the crab Voutier JL, Hanson JM (2008) Abundance, distribution, and pelagicus from Moreton Bay, eastern feeding of lady crab in the southern Gulf of St. Australia. Journal of Crustacean Biology 12: 94-100, Lawrence. Aquatic Ecology 42: 43-60, doi:10.1007/s10 doi:10.2307/1548723 452-007-9078-2 Sponaugle S, Lawton P (1990) Portunid crab on Wahl M (1997) Living attached: Aufwuchs, fouling, juvenile hard clams: effect of substrate type and prey epibiosis. In: Nagabhushanam R, Thompson M-F (eds) density. Marine Ecology Progress Series 67: 43-53, Fouling Organisms of the Indian . Biology and doi:10.3354/meps067043 control technology. Balkema Publishers, Rotterdam, Thompson R, MacNair N (2004) An overview of the The Netherlands, pp 31-83 clubbed tunicate (Styela clava) in Prince Edward Island. PEI Department of Agriculture, Fisheries, Aquaculture and Forestry Technical Report 234

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