Management and Risk Assessment of Sabellid Polychaete Infestations In

Home , Calliostoma, Calliostoma annulatum, Haliotis rufescens, Kelletia kelletii

Management and Risk Assessment of Sabellid University of California, Santa Barbara R/A-97 Polychaete Infestations in Abalone Mariculture 1995–97 Facilities

Armand Kuris

Introduction to locate abalone in experimen- of the shell. If worms continue to In October 1993, growers at tal aquaria by moving both with settle over a longer period of time, some commercial abalone maricul- and against the current (Kuris and the abalone takes on a teratologi- ture facilities (AMFs) in Southern Culver, unpublished results). Within cal, domed, appearance. The shell California brought an interesting a few hours after settlement, the is porous (because of many worm sabellid polychaete to our attention. worms secrete a mucous sheath tubes) and relatively fragile. Without The worm infested shells of cultured at the growing margin of the aba- continued linear extension of the red abalone, Haliotis rufescens. lone shell. Activity of the worm at shell, the abalone ceases to grow. Heavily infested abalone ceased the margin of the shell apparently Although the process of shell dam- growth. Their shells exhibited domed prevents its dislodgement and also age is obviously dependent on the teratology often lacking respiratory blocks deposition of nacre over the intensity and duration of the infesta- holes. The worms appeared to bore aperture of the tube. The ability of tion, the actual intensity-dependent into the shell. the abalone mantle to prevent settle- and time- dependent relationships We discovered that all AMFs ment of fouling organisms at the remain to be investigated. in California were infested; sev- shell margin is foiled by the sabellid. The respiratory pores of the eral were so heavily infested that The possible mechanisms used by abalone are also sabellid infesta- domed specimens were abundant. the sabellid to evade anti-fouling tion sites. These holes can become The objectives of our study were defenses are under our continuing completely clogged by worm tubes. to describe the worm (Associate investigation. In heavily infested shell, formation of principal investigator, K. Fitzhugh, Worms will not settle on dead new respiratory holes at the margin Los Angeles County Museum of (empty) shells or on hermit crab- of the shell is often impaired. Since Natural History), investigate trans- occupied gastropod shells (Culver no new holes are formed, and the mission to abalone, its mechanism and Kuris, 1997). They will settle on old ones are heavily fouled, the of attachment and the cause of glass and plastic surfaces when an function of these holes is probably shell damage. We also examined appropriate host is not present (C. less effective. the host specificity among common Culver, personal observation). Some preliminary comparative intertidal molluscs. In the course of observations have been made on our research we discovered that a Shell Damage shells of the common upper inter- natural rocky intertidal site at Cayu- The abalone, failing to dislodge tidal zone snail, Tegula funebra- cos, California had become infested. the recently settled sabellid worm, lis. This information was needed Here we sought to investigate how responds by secreting a laminar because these snails are very the worms had escaped into the layer over the tube (Kuris and Cul- rarely found in abalone mariculture adjacent facility, determine whether ver, unpublished results). Thus, in facilities (AMFs). Thus, recovery the worms had become established the immediate vicinity of each newly of infested T. funebralis shells in there, quantify transmission at that settled worm, the abalone mantle nature is convincing evidence that site and devise and supervise an is temporarily retracted so that transmission of the introduced sa- eradication plan. prismatic deposition at the growing bellid is occurring in native habitat. margin of the aperture is prevented. Within two weeks, the tubes of Life History After a period of time, the nacreous newly settled sabellids have been so The newly recognized pest is a layer over the worm tube is suf- rapidly covered with nacre that they sabellid polychaete. Fitzhugh and ficiently thick that the worm cannot are no longer detectable by tactile Rouse (unpublished results) have be seen through the laminar layers examination, and prismatic shell described the worm placing it in of shell, nor can the raised worm deposition has been renewed. Thus, a new genus. It is a simultaneous tube be readily detected by touch detection of sabellid worms on these hermaphrodite brooding its young with a fingernail or probe. At this shells requires very careful inspec- to a late, nonfeeding larval stage. point the abalone will renew pris- tion of the accretionary, as well as Released larvae lack the branchial matic deposition. Thus, growth of depositional, surfaces; worm tube crown characteristic of adult sabel- the shell is most visibly perturbed in apertures can be recognized by the lids and crawl over the benthos until the new shell below the worm. The microscopic deflection of nacreous they settle on the apertural margin more worms settling at one time, the shell below the aperture of the worm of susceptible gastropods. Benthic more evident the growth check mark tube. larvae of the sabellid pest are able on the outer (accretionary) surface

89 89 Host Specificity worm burdens. A follow-up survey could survive the marine cascade Table 1 summarizes our initial found that many of the native T. of several meters in height from the studies of host specificity. Most funebralis were also infested at this outflow pipe. prosobranch gastropods exposed site. In September 1996 we suc- The contamination incident at to the worms become infested. The cessfully conducted a sentinel snail Cayucos greatly elevated environ- Archaeogastropods (limpets, aba- experiment that demonstrated that mental concerns about the impact lone, trochids) seem most suscep- the infestation was established in of the sabellid pest on the California tible. A comprehensive evaluation of the T. funebralis population. native molluscan fauna. Research host specificity using cafeteria choice Following our recommenda- on host specificity and on habitat experiments and a comparison with tions, the AMF agreed to initiate an and host range of the sabellid in South African species is in progress. eradication program. The program its native range in southern Africa Although we have been able to consisted of three components: will enable us to assess risk of infest abalone (Haliotis rufescens) (1) installation of a screen to block establishment and spread of the as small as 2-mm long, certain the egress of live snails and shell sabellid in California. Concern over small species of gastropods are not debris from the facility; (2) removal the sabellid led to it being one of susceptible to sabellid settlement of infested and healthy hosts and the focal topics of the recent Third (Culver and Kuris, 1997). These empty shells that had been released International Abalone Symposium include species of Littorina and Mi- from the facility into the intertidal site at Monterey, California, convened trella. Cowries (whose outer surface and, (3) removal of all T. funebralis by the California Sea Grant College are laminar rather than prismatic (over 15-mm shell length) from the System. shell) are also not susceptible. The intertidal area around the discharge. few species of bivalves exposed are The screen was initially installed in Accomplishments unsuitable hosts (although the occa- late November 1996. Shell debris Our research has greatly al- sional worm can become established and live red abalone, T. brunnea tered feeding, water management on rock scallops in the presence of and T. montereyi were removed and animal handling procedures very heavily infested abalone). from the adjacent intertidal zone in California AMFs. Most of these beginning in November 1996, and recommendations are detailed in Spread of Sabellids in the Natural on several other occasions in 1997 Culver et al. ,1997. We have recom- Environment and 1998. Removal of T. funebralis mended, and industry has adopted, We surveyed most of the Califor- is ongoing and began in July 1997. antiseptic procedures in the transfer nia AMFs for sabellids (Culver and Results have been encouraging. By of animals between parts of AMFs. Kuris, 1998). We were particularly April 1998, new infestations (on the Hands and equipment are rinsed in interested in the presence of infested margin of the outer lip of the aper- freshwater. Transfer of abalone and shells in the discharge drains or in ture) could no longer be detected in kelp between tanks is minimized the natural habitats near the water a sample of 180 snails. The rate of and pathways of stock movement discharge outflows. Some facilities new infestations in July 1997 had through facilities are recorded. The include suspended infested abalone previously reached over 10% (N = presence of kelp-associated gas- in cages in situ in the environment. 500). Thus, debris screening and tropods (especially Tegula brun- Others release small numbers of removal of susceptible hosts ap- nea and T. montereyi) in AMFs is escaped abalone, dead abalone pears to have dropped the thresh- minimized. Escaped abalone, other shells and, most particularly, numer- old of transmission below the level gastropods and shell debris are ous infested individuals of Tegula to sustain the epidemic spread of removed from drains. Outflows to montereyi and T. brunnea. These the worm at Cayucos. It may have environmentally sensitive areas are snails enter certain AMFs in large reduced the transmission rate below screened. An important practical numbers, as they are present on the level required for the worm infes- concern was the recognition that kelp used for abalone food. These tation to persist at the site. Further infection dynamics and risk assess- snails can exit in the drains. Although studies are ongoing with sentinel T. ment of onshore tank AMFs were the former is normally a fully subtidal funebralis at this site. If eradication substantially different from offshore species, and large individuals of the of the sabellid from this established cage (barrel) facilities. We provided latter are lower intertidal zone inhab- site is attainable, it will represent separate recommendations appro- itants, both were recovered in large the first successful eradication of a priate to these two types of AMFs. numbers below the drains of some marine pest. At this location, release To effectively and promptly infested AMFs. from the AMF of large numbers of convey our findings to the industry In March 1995 at Cayucos, Cali- adult reproductive worms on live and the California Department of fornia, we detected cultured red aba- gastropods and shell debris appears Fish and Game (CDF&G), an Aba- lone (source evident from the pale to have been responsible for this lone Sabellid Advisory Committee green color of cultured red abalone), outbreak. This conclusion is sup- (ASAC) was formed with industry, Tegula brunnea and T. montereyi ported by the fact that few benthic CDF&G representatives and the released from the AMF into the up- larvae could be detected in water principal investigator. The Sea Grant per and mid-intertidal zones. All were discharge samples. Additionally, it trainee, C. Culver, also actively par- infested, often with high intensity seems unlikely that many larvae ticipated in these meetings.

90 Table 1. Host Specificity of Sabellid Polychaete Infestations from Infestations from Species Facility Tanks Experimental Tanks

Snails Acanthina spp. — Yes Astrea undosa — Yes Calliostoma annulatum Yes — Calliostoma canaliculatum Yes — Cypraea spadicea — None Haliotis corrugata Yes — Haliotis cracherodii — Yes Haliotis fulgens Yes — Haliotis rufescens Yes Yes Kelletia kelletii — Yes Littorina planaxis — Yes (rare; only one case) Mitrella spp. None None Norrisia norrisi Yes Yes Nucella emarginata — Yes Olivella biplicata — Yes Tegula aureotincta Yes — Tegula brunnea Yes — Tegula eiseni Yes Yes Tegula funebralis Yes Yes Tegula montereyi Yes —

Limpets Crepidula adunca Yes (uncommon and isolated cases) — Fissurella volcano Yes — Lottia gigantea Yes Yes Lottia pelta Yes Yes Lottia digitalis Yes — Lottia limatula Yes — Macclintockia scabra Yes —

Bivalves Crassadoma gigantea None Yes (rare; only one case) Crassostrea gigas — None Mytilus galloprovincialus None None

Based substantially on our work, out-planting was required. Later, all rates, and harvest infested abalone, CDF&G Director Schafer (personal outplantings were banned to prevent growth rates of abalone stock have communication) required all abalone further infestations in the wild. returned to pre-sabellid infestation aquaculture facilities to develop a We initiated training of CDF&G norms at many AMFs. sabellid eradication plan because personnel to enable them to recog- Our information on detection, all were considered infested. These nize lightly infested abalone. This host specificity and environmental plans are reviewed by CDF&G and was critical as prior to that time the contamination was transmitted to the risk at each facility is assessed industry and CDF&G were only the ASAC of CDF&G on March 22, based on the principles of infestation able to detect the teratologic domed and November 6, 1996. An impor- dynamics developed in our labora- specimens that were very heavily tant outcome of these meetings was tory. Approval of these plans and infested. Detection of lightly infested the establishment of a Sabellid Ad- progress towards eradication are stock is key to the approach of visory Subcommittee (SAS) chaired required for Aquaculture Registra- eradication in contaminated AMFs. by Robert Hulbrock, the CDF&G tion renewal. We also demonstrated these detec- Aquaculture Coordinator. The final Subsequent actions by CDF&G tion procedures to many industry report of the SAS contains the include sabellid-free certification for facility managers and scientists. Sabellid Worm Cleanup Plans of all transfers between facilities. Ini- Using these procedures to detect AMFs and a detailed status evalua- tially (1996) inspection of stock for infested stock, reduce transmission tion and risk assessment.

90 91 Our discovery of the infested to our native gastropods in natural Culver, C.S. and A.M. Kuris. Introduc- natural site at Cayucos galvanized habitats. tion of a new molluscan shell pest: several environmental organizations The California Coastal Commis- Not just another “boring” organism. and individuals to call for more care- sion used our information to evalu- Presented at the American Malaco- ful regulation of introduced marine ate permitting of an abalone culture logical Union of the Western Society species in general and the sabellid facility. of Malacologists Annual Meeting, Santa Barbara, California. June pest in particular. This information 22–27, 1997. Cooperating Organizations has been used at permit hearings Culver, C.S. and A.M. Kuris. Eradica- California Department of Fish and Game before the California Coastal Com- tion of a newly introduced species: Centre for Research on Introduced Ma- mission and CDF&G Commission. Mission possible? Presented at the rine Pests, CSIRO, Hobart, Tasmania Scientific advancements include American Fisheries Society Annual The Abalone Farm, Cayucos, California the discovery of a new type of worm Meeting, Monterey, California, August The Cultured Abalone, Goleta, California 24–28, 1997. with the unique ability to settle at the The HMAS Sterling Culver, C.S. and A.M. Kuris. An intro- growing margin of the aperture of University of Cape Town, South Africa duced polychaete pest of California abalones and other gastropods and Western Australia Fisheries Department stimulate the mantle to secrete new cultured abalone: current status and environmental concerns. Presented References laminar shell so as to form a tube at the 3rd International Symposium Culver, C.S., A.M. Kuris, and B. Beede. for the worm. This guidance of the on Abalone Biology, Fisheries and 1997. Identification and management mantle by the worm or its tube has Culture, Monterey, California, Octo- of exotic sabellid pests in California implications for the study of mol- ber 26–31, 1997. abalone aquaculture. California Sea luscan shell deposition. The worm Culver, C.S. and A.M. Kuris. Status of Grant College System. Publication may provide a new assay for the the introduced sabellid pest of abalo- No. T-041. ne and other gastropods in California. study of biomineralization and the Culver, C.S. and A.M. Kuris. 1998. Presented at the Eighth International development of novel biomaterials. Eradication of a newly introduced Zebra Mussel and Aquatic Nuisance Use of the sabellid as an experimen- species: Mission possible? Fisheries. Species Conference, Sacramento, tal probe has been initiated in our In press. California, March 16–18, 1998. laboratory in conjunction with Drs. Publications Daniel Morse (University of Califor- Lectures Fitzhugh, K. 1996. A polychaete threat- nia, Santa Barbara) and Rob Day C.S. Culver. Infestation of cultured ens California’s abalone culture (University of Melbourne, Australia). abalone by the nonindigenous sabel- industry. Terra. 33:(4):4–5. lid worm. Invited lecture. Sea Grant Extension Program Staff Training Benefits Presentations Meeting, San Francisco, California, The following abalone aquacul- Culver, C.S. and A.M. Kuris. Character- September 13, 1995. ture companies were informed about istics of cultured abalone infestations C. Culver, and K. Fitzhugh. A new genus methods to detect sabellids, reduce by an introduced sabellid polychaete. of sabellid and its impacts on Califor- infestations, prevent release of Presented at the Abalone Workshop nia gastropods. Invited lecture. Los II: An Educational Workshop on sabellids into the environment and Angeles County Museum of Natural Current Developments in Abalone quarantine infested stock. Farms History, Los Angeles, California, Enhancement Projects and the receiving onsite training or infor- December 7, 1995. Aquaculture Industry, Bodega Marine mational slide presentations are C. Culver. Status of the sabellid worm in Laboratory, Bodega Bay, California, indicated by an asterisk. California. Invited lecture. California December 2, 1995. Department of Fish and Game senior Abalone Acres*; The Abalone Culver, C.S., A. Kuris, and C.S. Fried- biologists staff meeting, Southern Farm Inc.; Abalone International*; man. Abalone aquaculture, health, California Region, Santa Barbara, Bodega Farms*; Carlsbad Aqua- management and sabellid poly- California, April 30, 1997. farms*; The Cultured Abalone; chaetes. Fish Health Session, Ca- A. Kuris. Invited lecture. Tasmania Monterey Abalone Company*; Pa- nadian Aquaculture Society Annual Department of Fisheries, Taroona, Meeting, 1996. cific Abalone Farms; Pacific Maricul- Tasmania, June, 1997. ture Inc.*; Proteus Seafarms; U.S. Culver, C.S. and A.M. Kuris. Sabellid Abalone*; Jacobsbaii Aquaculture polychaete pest of cultured abalone: (South Africa), Current exotic pest, future introduced In addition, CDF&G has used species? Presented at the California Sea Grant Nonindigenous Species our information on worm biology Workshop, San Francisco, California, to detect sabellid presence and to October 18–19, 1996. develop a sabellid-free certification Culver, C.S. and A.M. Kuris. The case program for outplanted abalone. of the sabellid worm: implications for CDF&G has used our information on future nonindigenous species intro- transmission and host-specificity to ductions. Presented at the Western develop regulatory policies to block Society of Naturalists, 77th Annual spread of sabellids among facilities Meeting, La Paz, Mexico, January and to reduce or eliminate spread 8–11, 1997.