biological invasions in aquatic ecosystems: impacts on ... · pdf fileproceedings of a...

PROCEEDINGS OF A WORKSHOP:

Biological Invasions in Aquatic Ecosystems:Impacts on Restoration and Potential for Control

AT THE

California-Nevada Chapter of the American Fisheries Society32nd Annual Conference: The Science of Restoration

April 25, 1998Holiday Inn Capitol Plaza, Sacramento, California

EDITORS

Andrew N. CohenSan Francisco Estuary Institute

S. Kim WebbU.S. Fish and Wildlife Service

THIS REPORT WAS FUNDED BY A GRANT FROM THECALFED Category III Steering Committee

ADMINISTERED BY THEMetropolitan Water District of Southern California

ON BEHALF OF THECalifornia Urban Water Agencies

San Francisco Estuary InstituteOakland, California

October 2002

Cite as: Cohen, A. N. and S. K. Webb (2002) Biological Invasions in Aquatic Ecosystems:Impacts on Restoration and Potential for Control, Proceedings of a Workshop, April 25, 1998,Sacramento, California. San Francisco Estuary Institute, Oakland, California.

Additional copies may be obtained from: San Francisco Estuary Institute, 7770 Pardee Lane, OaklandCA 94621 (510-746-7334).

Biological invasions are increasinglyrecognized as a major threat to biologicaldiversity and ecosystem integrity. Recentstudies have found that invasions are akey factor contributing to the imperilment,endangerment or extinction of nativeplants and animals, ranking in moststudies second only to habitat loss andalteration and well above pollution andover-harvesting (Cohen 2002). In thewestern United States, biologists considerinvasion to be the most important threatto aquatic organisms (Richter et al. 1997).

The papers and abstracts that follow arebased on presentations made at a sessionof the 1998 Annual Conference of theCalifornia-Nevada Chapter of theAmerican Fisheries Society. They explorehow the effects of invasions poseproblems for the restoration of aquaticecosystems in California, and how avariety of approaches may offer hope forpreventing or controlling invasions in somecases. They cover habitats fromfreshwater to estuarine to marine, andaddress a broad range of exotic organismsfrom plants to invertebrates and fish.Three presentations discussed, fromdifferent perspectives, an exotic parasitethat was accidentally imported intoCalifornia, released into the environment,and became established at one site fromwhich it was ultimately eradicated. Moresuch success stories are needed.

Andrew CohenOctober 2002

Cohen, A. N. (2002) Success factors in theestablishment of human-dispersed organisms. Pages374-394 in: Bullock, J. M., R. E. Kenward and R. S.Hails (eds.) Dispersal Ecology, BlackwellPublishing, Oxford, for the British EcologicalSociety, London.

Richter, B. D., D. P. Braun, M. A. Mendelson and L.L. Master (1997) Threats to imperiled freshwaterfauna. Conservation Biology 11: 1081-1093.

CONTENTS

Silversides, Smelt, and the Slough of Dreams: Who Will Come if WeRestore It?William A. Bennett 1

Management or Eradication? Strategies for Protecting Delta Fisheriesfrom Non-native Aquatic PlantsLars W. J. Anderson 2

The Introduction of the South African Worm: Biology, History, andImplications for ManagementCarolynn S. Culver and Armand M. Kuris 3

California Department of Fish and Game’s Response to the SabellidWorm InfestationFred Wendell 8

The Release of Pest Species by Marine Aquaculture: Lessons from aSouth African Parasite Introduced into California WatersAndrew N. Cohen 9

Biological Control of Marine InvasionsKevin D. Lafferty 14

Controlling Invasive Cordgrass: A Tale of Two EstuariesDonald R. Strong and Deborah R. Ayres 20

Biological Invasions in Aquatic Ecosystems: Impacts on Restoration and Potential for Control,Proceedings of a Workshop, April 25, 1998, Sacramento, California. Cohen, A. N. & S. K. Webb (eds.),San Francisco Estuary Institute, Oakland, California (October 2002).

1

Silversides, Smelt, and the Slough of Dreams: Who Will Come if WeRestore It?

William A. BennettUniversity of CaliforniaBodega Marine LaboratoryP.O. Box 247Bodega Bay CA 94923

Unlike many other species, Delta Smelt(Hypomesus transpacificus) abundance isnot strongly associated with seasonalfreshwater outflow or position of the lowsalinity zone, frustrating management andrestoration planning in the San FranciscoBay-Delta estuary. One potentialcomplicating factor is that exotic InlandSilversides (Menidia beryllina) may beimportant in regulating the abundance ofDelta Smelt since this population crashedin 1981. Inland Silversides, though anunintentional and fairly innocuousaddition to the Delta's food web, mayhave a substantial effect as intraguildpredators of Delta Smelt, by consuminglarvae and competing for resources withjuvenile and adult Delta Smelt. Severallines of evidence are presented to supportthis hypothesis.(1) The two species are ecologically very

similar.(2) Inland Silversides are notoriously

efficient colonizers and competitorselsewhere in the United States.

(3) Inland Silversides are known to oftenoccur in schools near the shoreline inDelta Smelt spawning habitat.

(4) Inland Silversides have been shown tobe very efficient predators of StripedBass (Morone saxatilis) larvae duringexperiments using large enclosuresdeployed in Suisun Marsh.

(5) Analyses of monitoring data indicatesthat abundances of Inland Silversidesand Delta Smelt are negativelycorrelated during years of lowfreshwater outflow.

Seasonal freshwater outflow mayinfluence the degree of co-occurrancebetween the species, such that the effectsof Inland Silversides may be greatest whenthe low salinity zone is positionedlandward. While such evidence indicatesthe potential benefit of maintainingadequate freshwater outflow to transportyoung Delta Smelt away from habitatsoccupied by Inland Silversides, it alsosuggests caution be used in the design andimplementation of habitat restorationprojects, because they maydisproportionately benefit exotic species,including Inland Silversides.


2

Management or Eradication? Strategies for Protecting Delta Fisheriesfrom Non-native Aquatic Plants

Lars W. J. AndersonU.S. Department of AgricultureAgricultural Research ServiceAquatic Weed Control ResearchUniversity of CaliforniaDavis, CA 95616

Economic and ecological impacts of non-native flowering aquatic plants haveincreased dramatically over the past 25years in California. Demands on thestate's water resources have exacerbatedthese impacts which include: (1) irrigationwater delivery; (2) recreational anddomestic (drinking) uses; and (3) fisheriesand waterfowl habitats. Taken together,Hydrilla verticillata (Hydrilla), Eichhorniacrassipes (Water Hyacinth), Egeria densa(Egeria), Myriophyllum spicatum (EurasianWatermilfoil), Potamogeton crispus(Curlyleaf Pondweed) and Myriophyllumaquaticum (Parrotfeather) create nearly allof the negative impacts. Recentintroductions and spread of Lythrumsalicaria (Purple Loosestrife) also threatenthe state's riparian systems. Theseagressive invaders utilize low light levels(in the case of submersed plants) andtheir rapid, prolific, and variedreproductive abilities to out-competenative vegetation. However, of theseplants, only Hydrilla has a pest rating of"A" by the state, which requires it to beeradicated.

Costs for Hydrilla eradication haveaveraged about $1.2 million annually overthe past 20 years, but this program hasprevented the introduction of Hydrillainto the Sacramento-San Joaquin Delta.The long-term savings from Hydrillaeradication is enormous when oneconsiders that without this program,Hydrilla would have become establishedin the Delta and a multitude of other largeCalifornia waters. In contrast, twoinvaders from South America, Water

Hyacinth and Egeria, now infest severalthousand acres in the Delta. WaterHyacinth has been under management for15 years, and a bill authorizing themanagement of Egeria was passed by thestate legislature last year. Costs of theseefforts to control Water Hyacinth andEgeria may equal or exceed the Hydrillaeradication expenditures within a fewyears. Management of Water Hyacinthand Egeria via biological control agentsshould be the long-term goal, yet effectiveherbicides and selective mechanicalcontrol need to be used now to preventfurther spread of these weeds. Althoughthere are strict statutory prohibitionsagainst possessing, selling or transportingHydrilla in California, these restrictionsapply to neither Water Hyacinth norEgeria, nor to other noxious members ofthe Hydrilla family. Thus, "management"of these species may have moderatesuccess, but their continued spread cannotbe contained without more stringentconstraints on their movement and use.Ironically, Egeria should be more easilyeradicated than Hydrilla since it does notproduce seeds or tubers. Finally, thecontinued presence and movement ofthese species, particularly Egeria andother "submersed" types, increases theopportunities for introductions of theZebra Mussel (Dreissena polymorpha). Thisnon-native freshwater mussel is oftenattached to aquatic plants and maythereby become a "hitchhiker" on boatsand trailers, or be transported viacommercial shipments of theseunregulated plants.


3

The Introduction of the South African Worm: Biology, History, andImplications for Management

Carolynn S. Culver and Armand M. KurisDepartment of Ecology, Evolution, and Marine BiologyMarine Science InstituteUniversity of CaliforniaSanta Barbara, CA 93106

ABSTRACT: In the early 1990's, California cultured abalone unknowingly became host to anundescribed polychaete pest. Several years later, it was determined that the worm was anon-indigenous species. By this time, the pest had been spread throughout the industry.Native to South Africa, it has been assigned to a new genus within the family Sabellidae.Initial research efforts were aimed at understanding the effect of the pest on abalone, aswell as a means for controlling it within the facilities. However, with the determination thatthe worm was non-indigenous, research efforts shifted to the assessment of ecologicalissues. The primary concern was the release and establishment of the sabellid in Californiahabitats. Biological and physiological characteristics of the pest are well suited forestablishment in California. In fact, one established sabellid population has been found inan intertidal area near Cayucos, California. Eradication efforts are ongoing and appear tobe effective. However, additional surveys of other potential release sites are badly needed.The events surrounding the introduction of this pest are complex. Understanding thebiology, as well as the history of the introduction, is critical to assess appropriatemanagement strategies. These features and their implications for management arediscussed.

This paper has been developed as part ofa panel discussion on controlling therelease of the South African worm fromCalifornia abalone aquaculture facilities.Recently, much attention has been focusedon the evaluation of the managementresponse to this introduction. For one toassess the adequacy of the response,certain information is needed. In thispaper, we summarize general informationon the biology of the exotic species andthe history of the introduction. Inaddition, we provide basic managementrecommendations and we discussimplications of this introduction for futureintroductions. A more thoroughdescription of these topics is covered inCulver et al. (1997).

BIOLOGY OF THE SABELLID

Prior to the introduction of the sabellidinto California, this worm wasunrecognized even in its native habitat. It

has since been described and named byDr. Kirk Fitzhugh of the Los AngelesCounty Museum of Natural History(Fitzhugh and Rouse 1999). It is a memberof the family Sabellidae, a groupcollectively known as fan worms. It livesin a tube in a mollusc shell. Asimultaneous hermaphrodite, sperm arebroadcast out of the tube, while eggs arefertilized and brooded within the tube(Oakes and Fields 1996; Culver et al.1997; Kuris and Culver 1999; Fitzhughand Rouse 1999). Unlike the majority ofmarine organisms, this pest does not havea planktonic larval stage. Instead, abenthic larva develops directly within theparental tube. Transmission occurs whenthe larva crawls out of the tube andsettles at the growing edge of either theparental host or a different host. Oncesettled it produces an elongate mucussheath. The host then calcifies thistransparent, fragile sheath. Thus, theworm obtains a tube as a result of thehost's response. This process of

4 CULVER AND KURIS

establishment is unique among shell-inhabiting parasites, which normally boredirectly into the host shell usingmechanical or chemical methods (Haigler1969; Blake and Evans 1973; Zottoli andCarriker 1974). In addition, although aliving host is required for establishment ofthis pest, empty shells can retain livesabellids that became established whilethe host was alive.

Another important biological feature ofthis sabellid is that it has broad hostspecificity. This pest infests manydifferent gastropods, not just abalone(Culver et al. 1997; Kuris and Culver1999). Bivalves appear to beunsusceptible, although few species havebeen tested. Host specificity issues,including the role of habitat, hostbehavior, host size, host defense, andsabellid host preference, are currentlybeing studied.

Infestations of this sabellid directlyimpact the growth of the host, alteringboth the rate and type of shell deposition.The impact is intensity dependent. Forexample, if only a few worms are present,the host may be virtually unaffected bythe worm because growth is onlytemporarily interrupted. In contrast, highworm intensity causes prolonged impactsto shell deposition and structure. In theworst case, growth ceases and the shellbecomes very brittle and abnormallyshaped. Further, respiratory pores areoften lacking. These direct impacts ongrowth can also have indirect affects onthe host. Growers have reported increasedmortality associated with heavyinfestations (Oakes and Fields 1996).Given the lack of respiratory pores andthe abnormal growth of heavily infestedabalone, these mortalities are likely due toprolonged stress. In addition, preliminarylaboratory experiments indicate thatheavy infestations increase a host'ssusceptibility to predators (Culver andKuris unpub. data). Further, as size isaffected by sabellid infestations,fecundity is also presumably affected.

HISTORY OF THE INTRODUCTION:CALIFORNIA ABALONE AQUACULTUREFACILITIES

This pest appears to have arrived intoCalifornia with a shipment of SouthAfrican abalone being used for commercialresearch purposes. At this time, theexistence of the worm was unknown toscience. Initially, worm-infested abalonewere simply characterized as havingdomed shells, often lacking respiratorypores. However, it was later learned thatthese abnormalities only occurred inanimals with high worm intensities. Incontrast, animals with low numbers ofworms appeared normal. The failure torecognize low infestation levels allowedthe continued spread of the pestthroughout the industry. By 1995, allCalifornia abalone farms were infestedwith the sabellid. Although this pest didnot affect the meat of the abalone, nor didit cause direct mortality, growers sufferedbecause the animals were not reachingmarket size. Production levels plummeted.

Initially, control of this pest in theaquaculture facilities was a primaryresearch focus. Thus, we attempted toidentify potential sabellid predators foruse as biological control agents (Kuris andCulver 1999). We were unsuccessful.Other control methods such as exposureto freshwater, to extreme temperatures,and to various chemicas were tried, butthey too failed. The only treatment thatprovided some beneficial effect wascoating the shell surface with wax or anon-toxic shellac. This techniqueeffectively plugs the tubes and smothersthe worms. Following this treatmentgrowth resumes. However, this means ofcontrol is not currently used because it isextremely labor intensive and requiresreapplication. Presently sabellidinfestations in aquaculture facilities arecontrolled through isolation of infestedstocks, use of antiseptic procedures andsale or destruction of infested stock.

INTRODUCTION OF THE SOUTH AFRICAN WORM 5

The economic impacts have beendevastating to the industry. Somecompanies have gone out of business,while those surviving have experiencedproduction delays of up to two years.Currently, all growers are working towarderadication of the pest from theirfacilities. Some have already achieved thisgoal.

HISTORY OF THE INTRODUCTION:CALIFORNIA NATURAL ENVIRONMENT

Concern over the environment increasedwith the recognition that the sabellid is anon-indigenous species. Our researchefforts evaluated the likelihood that thesabellid had been released into theenvironment. We identified severalavenues of release including:• Aquaculture facilities (both onshore

and offshore);• Enhancement projects (outplants);• Live fish markets and distributors;• Research and educational facilities

(e.g. universities, aquariums, bioassaylabs).

Our investigations of release of thesabellid began with onshore aquaculturefacilities. These facilities had endured theheaviest infestations and contained thelargest number of infested abalone. Asonshore facilities discharge their effluentdirectly into the environment, we began byexamining areas around discharge sites.At several sites, escaped animals andempty shells were being released from thefacilities. Often these animals and shellscontained reproductively active adultsabellids. In some areas, hundreds ofadult sabellids were living in these shells.

It became obvious that the sabellid wasbeing released into the environmentthrough the discharge of infested animalsand shell debris. Thus, we began takingsamples of the native gastropods fromaround the discharge sites. Because weknew some animals were becominginfested in the facilities and then

discharged, we targeted species that werenot found in the facilities. At one site, thesabellid was found to occur frequently ina snail species, Tegula funebralis, that israrely found in the facilities. However, theinfestations were of low intensity. Tofurther illustrate that infestations wereoccurring in nature at this site weconducted a mark and recapture study.New infestations were detected at thefirst recapture date, two weeks afterrelease. Currently, eradication efforts areongoing, infestation levels have sharplydeclined and eradication seems possible.1

Despite the swift action to eradicate theone known established sabellidpopulation, additional surveys arecritically needed. We have only been ableto conduct intertidal surveys aroundonshore facilities. We have recommendedthat subtidal surveys also be conductedaround these facilities. Further, we haverecommended that the other avenues ofrelease be assessed. Preliminary surveysaround some offshore cage facilities havebeen conducted and no establishedsabellid populations have been detected.However, these surveys looked primarilyat animals collected directly below orclose to the cages. As it is likely that thelarval worms are carried away from thecage areas by water currents, additionalinformation on current patterns andbroader surveys are needed. Similarsurveys are also critically needed in areaswhere potentially infested abalone mayhave been outplanted.

MANAGEMENT OF THE SABELLID

Throughout the course of the sabellidintroduction we have provided both theindustry and CDFG with our researchfindings as they have become available.We have also provided recommendationsabout management of the problem (Culveret al. 1997). In general, we agree with some

1 NOTE ADDED IN PRESS: The eradication efforts

were successful (Culver and Kuris 2000).

6 CULVER AND KURIS

of the policies that have been developed.However, we also feel that some aspectsof the introduction have been under-regulated, while others have been over-regulated.

When assessing sabellid managementstrategies, one should consider the historyof the introduction, as well as the biologyof the organism. Important datessurrounding the sabellid introductioninclude:

1981: Known importation of SouthAfrican abalone to California.

1987: First observation of abnormalabalone in California.

1993: Identification of the pest as anundescribed sabellid.

1994: California research begins.Mechanism of shell deformationdetermined.Recognition that the pest is anintroduced species from SouthAfrican.

1995: Recognition that the pest iswidespread in Californiaaquaculture facilities.Broad host specificitydemonstrated.

1996: Established wild population ofthe pest detected in California.

1998: Examination of the pest in SouthAfrican habitats.

Given this timeline, it is likely that thesabellid has been in California for aminimum of 11 years. However, it hasonly been a few years since it has beenrecognized as an introduced species. Inaddition, only recently did we detect anestablished population in nature.

Because this sabellid was a completelyunrecognized and undescribed species, itsbasic biological characteristics wereunknown. The following biologicalcharacteristics of the sabellid have beenidentified:• It is a simultaneous hermaphrodite.• It has broad host specificity.• It lives in habitats in South Africa

similar to those available in California.

• It has a benthic crawling larval stage.• It directly affects shell deposition and

growth of host species (and indirectlyaffects survivorship and fecundity).

These features suggest that this pest has astrong potential to successfully invadeCalifornian habitats. However, its benthiclarval stage suggests that dispersal will belimited. Further, the impacts of thesabellid on its host are perceived by someas benign; this pest does not pose anyhuman health risk and it does not kill anyorganisms outright. Development of amanagement scheme requiresconsideration of all of these factors, aswell as the impact of such a strategy onaffected entities (e.g. the abalone farmingindustry). Thus, depending on perceptionof the risks, different managementstrategies could be proposed.

IMPLICATIONS FOR FUTUREMANAGEMENT OF NON-INDIGENOUSSPECIES

Like all introductions, lessons can belearned from the introduction of thesabellid. In general, we must face thereality that importation, no matter howregulated, allows for the potentialintroduction of non-indigenous species. Inthe case of the one known importation ofSouth African abalone, all animals wereinspected and quarantined. However, theexistence of the sabellid was unknown.The effectiveness of an inspection andquarantine system will be limited fororganisms that have never been studied.The sabellid is not the first, and likely willnot be the last, unknown species that isdiscovered after it has been introducedelsewhere.

ACKNOWLEDGMENTS

We would like to acknowledge the Californiaabalone industry for their continued support for ourresearch. Without their cooperation and approvedaccess to their facilities and surrounding areas ourresearch would not have been possible. This paperis funded in part by a grant from the National Sea

INTRODUCTION OF THE SOUTH AFRICAN WORM 7

Grant College Program, National Oceanic andAtmospheric Administration, U.S. department ofCommerce, under grant number NA36RG0537project number 58-A-N through the California SeaGrant College System. The views expressed hereinare those of the authors and do not necessarilyreflect the views of NOAA or any of its sub-agencies. The U.S. Government is authorized toreproduce and distribute for governmental purposes.

LITERATURE CITED

Blake, J. A. and J. W. Evans (1973) Polydora andother genera as borers in mollusk shells and othercalcareous substrates. Veliger 15: 235-249.

Culver, C. S. and A. M. Kuris (2000) The apparenteradication of a locally established introducedmarine pest. Biological Invasions 2: 245-253.

Culver, C. S., A. M. Kuris and B. Beede (1997)Identification and Management of the ExoticSabellid Pest in California Cultured Abalone.

Publication No. T-041, California Sea Grant CollegeSystem, La Jolla, California.

Fitzhugh, K. and G. W. Rouse (1999) A remarkablenew genus and species of fan worm (Polychaeta:Sabellidae: Sabellinae) associated with marinegastropods. Invertebrate Biology 118: 357-390.

Haigler, S. A. (1969) Boring mechanism of Polydorawebsteri inhabiting Crassostrea virginica. AmericanZoologist 9: 821-828.

Kuris, A. M. and C. S. Culver (1999) An introducedsabellid polychaete pest infesting cultured abalonesand its potential spread to other Californiagastropods. Invertebrate Biology 118: 391-403.

Oakes, F. R. and R. C. Fields (1996) Infestation ofHaliotis rufescens shells by a sabellid polychaete.Aquaculture 140: 139-143.

Zottoli R. A. and M. R. Carriker (1974) Burrowmorphology, tube formation, and microarchitectureof shell dissolution by the Spionid polychaetePolydora websteri. Marine Biology 27: 307-316.


8

California Department of Fish and Game’s Response to the SabellidWorm Infestation

Fred WendellCalifornia Department of Fish and Game213 Beach StreetMorro Bay CA 93442

The California Department of Fish andGame’s (Department’s) goal is theeradication of the sabellid worminfestation. The approach used toachieve the goal is guided by legislativemandate and has changed as researchinformation became available. Thispresentation will describe theDepartment’s response to theinfestation in light of those changingconditions.

The Department became aware of thesabellid worm infestation in late 1994.Biological information was limited andthe approach used by the Departmenttook advantage of the cooperation thatalready existed between the abaloneaquaculture industry and Universityresearchers. Appreciable resources toaddress what appeared to be anaquaculture problem had already beenmarshaled, including obtaining RapidResponse funding for research fromCalifornia Sea Grant. When thatresearch determined in early 1995 thatthe worm was an exotic from SouthAfrica, the Department soughtrecommendations from its AquacultureDisease Committee.

Based on those recommendations, theDepartment’s approach changed. Whilecooperative research was encouraged,the Department also committed itsresources to addressing the problem andplaced a prohibition on the planting of

cultured abalone in the wild. Departmentresources were focused on determining theextent of the infestation and assisting inminimizing its spread through California’saquaculture industry.

When research subsequently showed thatthe worm was capable of infesting othermollusks, the Department required eachfacility to develop a plan for eradicationand made its development a condition forrenewal of aquaculture registration. Thoseplans, which include specific requirementsimposed by the Department, have beenimplemented and are being evaluatedfurther by the Department. Ongoingcooperative risk assessments are focusingon the control and eradication of the oneknown infestation in the wild. Surveys arealso being conducted to determine whetherother introductions to the wild haveoccurred as a result of past abaloneenhancement efforts that used culturedabalone.

While these efforts are ongoing, theDepartment has also implemented areorganization that effectively increases itsability to focus on aquaculture issuesthrough the formation of an aquacultureteam. This team is interested in expandingexisting partnerships that are responding tothis problem and in creating newpartnerships to address a variety of relatedissues including the control andmanagement of exotic introductions.


9

The Release of Pest Species by Marine Aquaculture: Lessons from aSouth African Parasite Introduced into California Waters

Andrew N. CohenSan Francisco Estuary Institute7770 Pardee LaneOakland, CA 94621

ABSTRACT: A South African worm accidentally introduced into California abalone farmscan infest, weaken and deform the shells of abalone and other native California marinesnails, reduce growth and reproductive rates, and leave the host species more vulnerable topredation and environmental hazards. The worm was spread to all California abalonefarms via stock transfers, has bankrupted some growers, and has infested native snails inthe ocean in at least one site. Despite the potential for substantial harm to California'smarine resources, the state continues to allow abalone farming practices that can releasethis parasite into the environment.

Marine aquaculture in general is inadequately regulated to prevent the introduction ofharmful exotic organisms. To avoid such impacts, aquaculture should be governed by thefollowing principles:

• Aquaculture facilities should be required to operate in a sustainable manner withoutcausing harm to the marine environment, which includes not releasing exoticorganisms.

• Aquaculture should be based on native, local stock whenever possible. Imports andtransfers of stock should be minimized, thoroughly inspected, and quarantined for anappropriate observation period.

• Aquaculture stock infested by parasites should be isolated from the environment. Ifisolation is impossible, the stock should be destroyed.

• Proposals to import exotic stock should receive full public review, and advisory bodiesshould include all relevant stakeholders, not just the aquaculture industry.

Aquaculture activities have a long historyof introducing harmful parasites anddiseases of fish and shellfish into variousparts of the world (e.g. Farley 1992; Brock1992; Mills et al. 1993; Barber 1996;Smolowitz 1996). Outbreaks of diseasesand parasites are common in the crowdedand often stressful conditions ofaquaculture facilities (Huner and Brown1985). In some regions, parasites ordiseases accidentally imported byaquaculture have had devastating effecton native fish and shellfish populations(e.g. Mo 1994). Preventing suchintroductions in the future will requireboth better regulation of the initialimporting of organisms, and bettercontrols on the release into theenvironment of undesirable organisms thatare cultured or that become establishedwithin aquaculture facilities. The recentimportion and establishment of a harmful

shell parasite in California abalone farms,and its subsequent release into theenvironment, suggests that there issubstantial room for improvement in theregulation of marine aquaculture.

THE ABALONE PARASITE

In the early 1980s the exotic sabellidworm Terebrasabella heterouncinata(Fitzhugh and Rouse 1999), then unknownto science, was accidentally introducedinto California abalone farms withimported South African abalone, Haliotismidae.1 The worm established infestions inthe shells of the California Red Abalone,Haliotis rufescens, the species cultured inCalifornia. Intense infestations produced 1 It is unclear whether the abalone were imported

with the knowledge of California agencies.

10 COHEN

shells that were easily broken,disproportionately tall relative to the sizeof the aperture and foot, and frequentlylacking respiratory holes. In addition thegrowth of soft tissue was slowed orhalted. Overall, such infestationsproduced abalone with reducedreproductive potential and, were they tooccur in the natural environment, greatervulnerability to predators and todislodging or damage by waves or rockmovement in the surf zone. Kuris andCulver (1999) found that these worms caninfest not just Red Abalone but probablyall species of California abalone (all ofwhich are in decline and one of which, theWhite Abalone Haliotis sorenseni, isthought to be near extinction—Tegner et al.1996) and a wide variety of nativeCalifornia marine snails.

As is common in some types ofaquaculture, abalone stocks werefrequently transferred between facilities,spreading the South African worm to allCalifornia abalone farms by the mid-1990s, with the resulting infestationsbankrupting some growers. In 1994researchers determined that the problemwas caused by an exotic parasite, by 1995they had demonstrated that it can infest abroad range of marine snails, and by 1996the worm had been found in native snailsin the ocean in at least one site (Kuris andCulver 1999).

THE GOVERNMENT RESPONSE

The California Department of Fish andGame (CDFG) is the state agency with theprimary responsibility for managing andregulating aquaculture and for protectingthe marine environment. However it alsohas a potentially conflicting mandate topromote and encourage the developmentof the California abalone farmingindustry.

CDFG took no action to prevent therelease of the sabellid worm intoCalifornia waters until December 1996,

when CDFG notified abalone farmers thatit would take the following steps (CDFG1996):(1) Stop the direct out-planting of abalone

into California waters.2

(2) Require the installation of screens onthe pipes that discharge water fromon-shore abalone farms into the ocean;and require growers that rear abalonein cages and barrels in the ocean tostop dumping empty shells, kelp andother debris that could harbor sabellidworms into the ocean.

(3) Require abalone farmers to notifyCDFG when abalone are beingtransferred between facilities, so thatCDFG can inspect the shipments forsabellids.

(4) Not issue 1997 aquacultureregistrations, which are needed inorder to operate aquaculture facilitiesin California, to any abalone farmsthat do not have an approved plan foreradicating the sabellid worm.

While these are useful steps in concept,they did not go far enough, nor were manyof them implemented effectively.

For example, screening the discharge pipesfrom on-shore facilities should help toprevent the release into the ocean of shelldebris containing adult worms and of livegastropods infested with worms , butwould still allow larval worms to bedischarged into the ocean. The sabellidlarvae are not planktonic, but ratherdisperse by crawling short distances onthe shells of their host species or on otherbenthic substrates. However, they can bedislodged with aeration or when tanks areflushed, and float free in the water column(K. Ruck, pers. comm.; C. Culver pers.

2 Large numbers of cultured abalone, numbering at

least in the tens of thousands and presumablyincluding a significant number of sabellid-infested abalone, were planted in the ocean overseveral years to augment the declining abalonepopulation. These plantings were made underPrivate Stocking Permits issued by CDFG, but inmost cases the descriptions of the sites are toovague to enable them to be checked for sabellidinfestations, and the records were retained foronly three years (CDFG 1997).

RELEASE OF PEST SPECIES BY MARINE AQUACULTURE 11

comm.). A small number of sabellid larvaewere collected in the discharge from aninfested abalone farm (C. Culver pers.comm.) which, based on the relativevolumes of water sampled anddischarged, works out to over 70,000larval worms per day carried in thedischarge from this one farm (C. Friedmanpers. comm.).3 The screens installed ondischarge pipes typically have a mesh sizeof 1 cm or larger, while the sabellid larvaeare about 0.05 mm in diameter, so thescreen openings need to be made about200 times smaller if they are to catchsabellid larvae (K. Ruck pers. comm.).Furthermore, growers are allowed to rearinfested abalone in cages or barrels in theocean, with mesh or holes large enough tofreely release larvae into the environment(C. Culver pers. comm.).

Effective inspection of all transfers ofabalone stocks is essential to containingand ultimately eliminating the sabellidworm from California abalone farms, butunfortunately current procedures do notappear to be adequate for this job. For theinspections a number of abalone arerandomly selected and shucked, and theshells are examined for sabellid worms.The more shells examined, the greater thechance of detecting an infestation, butCDFG's protocols only require theexamination of 60 abalone per populationunit (defined as a tank, barrel or year-class), which can include up to 9,000abalone or more (P. Kalvass pers. comm.).Even if the individual examinationsproduce no false negatives (that is, if thereis even a single sabellid worm in the shell

3 It is unclear whether the larval worms collected

came from the abalone farm itself, or frominfested snails living in the discharge channel.However, in either case the data demonstratethat the discharge streams are capable ofcarrying large numbers of sabellid worms intothe ocean, and may in fact be doing so. If thelarvae did originate in the abalone farm, thenumber discharged may have been six timesgreater a year or two earlier, when the numberof infested abalone was that much greater (R.Fields pers. comm.). Sabellid larvae have alsobeen collected from abalone tank outflows inSouth Africa (K. Ruck pers. comm.).

of an examined abalone, it will bedetected), then examining 60 shells perunit leaves about a 5% chance of missing a5% infestation rate (meaning that oneabalone out of 20 in the shipment hassabellids) and about a 55% chance ofmissing a 1% infestation rate (C. Gowanpers. comm.) In at least one recent case, ashipment that passed inspected didcontain sabellids infested a previously"clean" abalone farm, which shortlythereafter shut down.

While requiring abalone farms to developeradication and control plans is animportant step, the content of those plansis also important. Several growers haveproposed to eliminate the sabellid wormfrom their facilities by selling off theirinfested abalone. This would essentiallytransfer the problem out of CDFG'sjurisdiction without eliminating the risk,since the sabellid worm could then bereleased into the ocean via unscreeneddischarges from the holding tanks of liveseafood distributors or retailers, or bydiscarded shells. Furthermore, althoughCDFG said at the end of 1996 that itwould not provide aquacultureregistrations to abalone farms that did nothave approved eradication plans, it hasallowed abalone farms to continueoperations even though no plans have yet(as of spring 1998) been approved.

CDFG is not the only government agencywith the responsibility and authority toaddress this problem. The U. S.Environmental Protection Agency andCalifornia's Regional Water QualityControl Boards are responsible forregulating discharges of pollutants,including biological pollutants such asexotic species, under the Clean Water Act(Cohen and Foster 2000). Other agenciescharged with protecting the coastal marineenvironment or marine organisms mayhave additional obligations and powers to

12 COHEN

prevent the introduction of this harmfulparasite.4 None have taken steps to do so.

PRINCIPLES FOR MANAGING MARINEAQUACULTURE

Such lapses are unfortunately notconfined to the sabellid worm problem orto the abalone industry. Marineaquaculture in general is inadequatelyregulated to prevent the introduction ofexotic organisms into the environment,and in many parts of the worldaquaculture activities have imported andreleased parasites, diseases, predators orcompetitors of native fish and shellfish.To reduce the risk of impacts to importantmarine resources and the marineenvironment, the development andmanagement of marine aquaculture shouldbe based on the following principles:• Aquaculture facilities should be legally

required to operate in a sustainablemanner, without causing harm tomarine resources or ecosystems, whichincludes not releasing exotic organismsinto the environment. Aquacultureoperations that cannot meet thisstandard should not be encouraged orallowed.

• Whenever possible, aquacultureshould be based on native, local stock.Imports of stock and transfers ofstock between regions should beminimized, and whenever possible thestock should be transported in the eggor larval stage. All imported andtransferred stock should be thoroughlyinspected, and held in quarantine (inisolation from the environment and

4 For example, the National Marine Fisheries

Service is responsible for protecting marinespecies listed under the federal EndangeredSpecies Act from harmful actions which caninclude "releasing non-indigenous...species into alisted species' habitat or where they may accessthe habitat of listed species;" and the CaliforniaCoastal Commission is charged by the CaliforniaCoastal Act with maintaining marine resourcesand ensuring that uses of the marine environmentare carried out in a manner that will "maintainhealthy populations of all species of marineorganisms" (Cohen and Foster 2000).

from other stock in the receivingfacility) for an appropriateobservation period.

• Any stock infested with exoticorganisms should be immediatelyisolated from the environment. Ifisolating the stock is not feasible, thestock should be destroyed andproperly disposed of. Any parasitesor disease syndromes found inaquaculture stocks that are not knownfrom the local environment should bemanaged as if they were exoticorganisms until proven otherwise—that is, stock infested with suchparasites or diseases should either beisolated from the environment ordestroyed.

• Proposals to import exoticorganisms for culturing shouldreceive full public review.Participation on governmentadvisory bodies or committeesthat address the management orregulation of aquaculture shouldinclude all relevant stakeholders,not just the representatives andconsultants of the aquacultureindustry.

LITERATURE CITED

Barber, B. J. (1996) Impacts of shellfishintroductions on local communities. In: Proceedingsof a Workshop on Exotic Species: Issues Relating toAquaculture and Biodiversity, February 8, 1996,MIT Sea Grant College Program, Cambridge,Massachusetts.

Brock, J. A. (1992) Selected issues concerningobligate pathogens of a non-native species of marineshrimp. Pages 165-172 in: Introductions & Transfersof Marine Species, Proceedings of the Conference &Workshop, Oct. 30-Nov. 2, 1991, Hilton HeadIsland, South Carolina, South Carolina Sea Grant.

CDFG (1996) Letter to "All Registered AbaloneAquaculturists" (Dec. 6, 1996) from J. E. Schafer,Director, California Department of Fish and Game,Sacramento, California.

CDFG (1997) Status of potential sabellid infestationin the wild: historic out plantings. Section 3 in:Sabellid Worm Infestation Status Report -Information Packet (December 1997), prepared forthe Aquaculture Disease Committee, CaliforniaDepartment of Fish and Game, Sacramento,California.

RELEASE OF PEST SPECIES BY MARINE AQUACULTURE 13

Cohen, A. N. and B. Foster (2000) The regulation ofbiological pollution: preventing exotic speciesinvasions from ballast water discharged intoCalifornia coastal waters. Golden Gate UniversityLaw Review 30(4): 787-883.

Farley, C. A. (1992) Mass mortalities and infectiouslethal diseases in bivalve molluscs and associationswith geographic transfers of populations. Pages139-154 in: Rosenfield, A. and R. Mann (eds.),Dispersal of Living Organisms into AquaticEcosystems, Maryland Sea Grant, College Park,Maryland.

Fitzhugh, K. and G. W. Rouse (1999) A remarkablenew genus and species of fan worm (Polychaeta:Sabellidae: Sabellinae) associated with marinegastropods. Invertebrate Biology 118: 357-390.

Huner, J. V. and E. E. Brown (eds.) (1985)Crustacean and Mollusk Aquaculture in the UnitedStates. AVI Publishing Co., Westport, Connecticut.

Kuris, A. M. and C. S. Culver (1999) An introducedsabellid polychaete pest infesting cultured abalones

and its potential spread to other Californiagastropods. Invertebrate Biology 118(4): 391-403.

Mills, E. L., J. H. Leach, J. T. Carlton and C. L Secor(1993) Exotic species in the Great Lakes: a historyof biotic crises and anthropogenic introductions.Journal of Great Lakes Research 19(1): 1-54.

Mo, T. A. (1994) Status of Gyrodactylus salarisproblems and research in Norway. Pages 43-58 in:Pike, A. W. and J. W. Lewis (eds.) Parasitic Diseasesof Fish, Samara Publishing Ltd., Tresaith, Dyfed,Great Britain.

Smolowitz, R. (1996) Diseases of bivalves. In:Proceedings of a Workshop on Exotic Species: IssuesRelating to Aquaculture and Biodiversity, February8, 1996, MIT Sea Grant College Program, Cambridge,Massachusetts.

Tegner, M. J., L. V. Basch and P. K. Dayton (1996)Near extinction of an exploited marine invertebrate.Trends in Evolution and Ecology 11(7): 278-279.


14

Biological Control of Marine Invasions

Kevin D. LaffertyMarine Science InstituteUniversity of CaliforniaSanta Barbara, CA 93106

ABSTRACT: Biological control, as used in terrestrial systems, may hold promise forapplication against exotic marine species. Marine systems, however, differ with respect tothe types of control agents available, the degree of pest-population reduction needed foreffective control, the spatial scale over which biological control must operate effectively, thepracticality of implementation, and the nature and degree of concern over safety. As anexample, Lafferty and Kuris (1996) proposed a strategy for developing a biological controlprogram against the European green crab, Carcinus maenas, which has had substantialnegative impacts where previously introduced (New England, Atlantic Canada, SouthAfrica, South Australia) and which has recently been introduced to Central California andTasmania. The green crab performs better in introduced regions, presumably because ithas left its native parasites behind. This suggests that introducing native parasites mayhave some utility in controlling its numbers. Lafferty and Kuris (1996) suggest theevaluation of the safety and efficacy of a European rhizocephalan barnacle, Sacculinacarcini, as a potential control candidate. The host specificity of this barnacle is presentlybeing evaluated in the laboratory and mathematical models used are being used to assessthe conditions under which the barnacle, a parasitic castrator, could lead to satisfactorylevels of control.

Since the 1880s, biological control forterrestrial pests has involved thedeployment of herbivores, predators,parasites or diseases. There now existsan extensive knowledge concerningbiological control based on manysuccessful applications and somenotable failures. Natural enemies canfind and track pest populations orlocate new pest populations. They alsoevade the development of resistance bypests by coevolving. When successful,they provide either a long-term or apermanent low cost solution to a pestproblem. Finally, when well chosen, theyusually have sufficient specificity to beenvironmentally safe. Despite this, inthe 40s and 50s, cheap and effectivepesticides largely replaced biologicalcontrol. The environmental damagecaused by pesticides and thedevelopment of genetic resistance ofpests has renewed interest in biologicalcontrol today.

Before using natural enemies as abiological control, it is useful to survey

introduced populations for parasites andpredators and compare them with the typesand abundance of such natural enemieswhere the pest is native. Most of thesuccessfully introduced natural enemies thatachieve good (economic) control interrestrial systems without deleterious sideeffects are parasitoid wasps, flies andnematode worms.

In marine environments, damagingintroductions are also common (Carlton1987, 1989; Zibrowius 1991). Ballast watertransport is the most important meansdisseminating exotic species (Carlton 1985,1989). Since most such introductions arriveas larvae, they generally come free ofnatural enemies (parasitic castrators,specialized predators and pathogens ofadults) that might normally control theirabundance in their native regions. Theresultant extremely high populationdensities attained by alien species is whatusually leads to economic damage (Nicholset al. 1990). Clearly, one of the mostefficient approaches to the control of marinepests is to carefully examine the use of

MARINE BIOCONTROL 15

biological control against terrestrialinsect pests for appropriate analogoustactics (Lafferty and Kuris 1996).Marine systems have some importantfeatures that contrast with terrestrialbiological control paradigms and requirespecial consideration. The potential touse natural enemies against marine pestsenjoys, in principle, a significantadvantage compared to their use againstterrestrial agricultural pests. Inagriculture, farmers must cut pestpopulations to very low levels tominimize the cosmetic damage to theircrops. In contrast, there is usually noreason to reduce marine pestpopulations to very low levels andmodest reductions in pest abundancecan provide a successful outcome.

Available control agents differ betweenmarine and terrestrial systems.Parasitic castrators are more typical ofmarine systems than parasitoids anddeserve special attention. Like theparasitoid-infected host, theparasitically castrated host has noreproductive potential. However, thecastrated host continues to exertintraspecific competitive effects againstunparasitized individuals (Lafferty1993). It also continues to be a pest.Kuris (1974) postulated that, analogousto parasitoids, parasitic castrators maybe able to control host populations.

Biological control using natural enemiesis effective because control agents buildup in local patches (Murdoch et al.1985). Predictions about populationdynamics in marine systems aresensitive to the assumptions implicit inglobal (large scale or closed recruitment)dynamics (Gaines and Lafferty 1995).In marine environments, planktoniclarval stages disperse widely, offspringrarely settle and live near their parents,and natural enemies may not respondnumerically to locally high pest density.At small scales, the apparent effect ofparasitic castration should be reducedaccording to the amount of outside

recruitment that occurs. This produces tworelevant points. The first is that it may bedifficult to assess the importance ofparasitic castration at small spatial scales.The second is that the addition of aparasitic castrator may not provide controlat a local scale in the same way that apredator, parasitoid or pathogen might.This does not mean that parasitic castratorsare ineffective control agents, only that theymight need to be employed on large scalesfor their effects to be observable. It alsoindicates, indirectly, that the benefits ofcontrol efforts at one location will be spreadover a larger area. The most efficient use ofa parasitic castrator would involve targetingsource populations while ignoring sinkpopulations of the host.

A potential disadvantage when usingnatural enemies in marine compared toterrestrial environments concerns safety.Though we may care little about impacts tonative insects such as aphids or scale, mostpeople would consider a natural enemyused against a marine pest, such as thegreen crab, to be unsafe if it were tosignificantly reduce commercially fishedcrab species. Thus, natural enemies usedagainst marine pests must meet a highsafety threshold to conserve our nativefauna.

A TEST CASE

The European green crab makes aninteresting test case because it is likely toprove to be a truly harmful introduction onthe West Coast of the United States. Basedon the history of Carcinus maenas after itsintroduction elsewhere (Ropes 1968; LeRoux et al. 1990; Cohen et al. 1995; Thresher1997), the crab is likely to devastateintertidal and subtidal shellfish beds. Sofar, measures taken to reduce predation(mesh enclosures) seem to have beensuccessful for shellfishery operations inTomales Bay (Sawyer 1994 pers. comm.)and in Martha’s Vineyard (Walton 1997).Although predicting the ultimate range ofthe green crab on the Pacific Coast is

16 LAFFERTY

speculative, temperature regimes seemsuitable from southern California northto Puget Sound, threatening the nation'slargest oyster-rearing industry inWashington state. Lafferty and Kuris(1996) estimated that the crab couldimpact fisheries worth up to aconservative $44 million per year.

A global survey (Torchin et al. 2001)found that introduced green crabs werelarger than native green crabs due toincreased growth and/or survivorship,perhaps because they suffered less frompredators and parasites. An exceptionis the introduction in Victoria, Australiawhere crabs were small, scarce andheavily infected with larval tapeworms.Such release from natural enemies maycontribute to the success of invasionsand supports the likelihood thatclassical biological control may be afeasible means to reduce the impacts ofthese introduced crabs. The onlypotential control agent known to infectgreen crabs in California is a nemerteanegg predator, Carcinonemertes epialti, thatnormally infests the shore crabHemigrapsus oregonensis (Torchin et al.1996). At this point, it is unlikely thatthe nemertean alone will affect greencrab abundance because infestationrates are apparently low.

The rhizocephalan barnacle, Sacculinacarcini, presently seems the bestcandidate for biological control. TheRhizocephala are highly host-specificparasitic castrators that cantheoretically control host populations.Determining the association between theprevalence of parasitism and thereduction of the host population by aparasitic castrator would helpdetermine the degree to which thebarnacles can depress host density inthe field. Simple models indicate that ona global scale, for a host whose numbersare directly linked to reproductiveoutput (i.e. a birth rate term is found inthe solution for the host’s equilibrium),there is a simple association between

parasitic castration and host density. Forthe most simple model, this can beapproximated as N/K = 1 - p, where N isthe number of infected and uninfected hostspresent in the population, K is the carryingcapacity of the host in the absence of theparasitic castrator and p is the prevalence(proportion of hosts infected) of theparasitic castrator. In other words, if 60%of the crabs in a population are found to beparasitized, the total density of crabs(infected and uninfected crabs) is reducedto only 40% of the carrying capacity. This isan evaluation tool and does not indicatethat parasitic castrators used in biologicalcontrol should attain high prevalences andsubstantially reduce host populations.However, reports of high prevalences ofrhizocephalan barnacles in the wild(Minchin 1997) suggest that, in Europe, thebarnacle is substantially reducing green crabdensities in some locations.

Inherent time lags can affect the stability ofthe host-parasite interaction in complexways. Preliminary work indicates fivepossible outcomes. The first isstraightforward, the host can go extinct ifexternal sources of density independentmortality exceed per capita rates ofreproduction. The second prediction is thatthe parasite might not be able to invade ahost population that is too small. A thirdoutcome is coexistence between the parasiteand the host. A fourth outcome is that theparasite invades but goes extinct while thehost persists. The fifth outcome is that theparasite may cause the host to go extinct(after which the parasite goes extinct aswell). These outcomes are all of interest to acontrol program.

Experimental evidence from field studies(Blower and Roughgarden 1989; Lafferty1993) supports a reduction of hostpopulations by parasitic castrators. Moreimportantly, a negative association betweenthe prevalence of S. carcini and crababundance in Europe (based on an analysisof Minchin’s (1997) data (R = -.38, N = 15),and not representing his conclusions)suggests that barnacles reduce the


abundance of native crab populations.In addition, infection by a barnaclesubstantially reduces the impact a crabhas on shellfish (Minchin 1997).

TESTING HOST SPECIFICITY

Although the present informationstrongly suggests that S. carcini wouldbe a safe control agent, thedocumentation of rhizocephalans withbroader host specificity (e.g.Loxothylacus panopaei infects sevenxanthid crabs (Grosholz and Ruiz1995)) stresses the need for carefullycontrolled experiments to determine ifnative species are refractory toinfections of the parasite. Høeg (1997)exposed a number of Australian crabspecies to Sacculina carcini cypridsunder laboratory conditions and foundthat settlement occurred on most(including Australian C. maenas). Undernatural conditions of exposure, cypridssettled on only 2 of 4 C. maenas and 2 of4 Paragrapsus gaimairdi (an Australianspecies). However, no evidence ofdevelopment of the parasite in a hostspecies other than C. maenas has beendemonstrated so far.

We (Lafferty, Torchin and Kuris) arepresently investigating in the laboratorythe susceptibility of crabs from the WestCoast of the United States to infectionby S. carcini. First, we built a culturefacility that has several redundantfilters to prevent the release of crab orbarnacle larvae. We are presentlydeveloping our larval rearing techniques,and have been successful at gettingbarnacles to release nauplii larvae,which we can culture to the infectivecyprid stage. These techniques weredeveloped during the fall and winterwhen barnacles release male larvae,which are not infective to crabs. In thenext several months we will be workingwith female larvae and can attempt totest for host specificity.

We will first assess the initial level of hostspecificity, the ability of larvae to settle onthe host. If larvae do settle on the test crabs,we will subject newly metamorphosed andlater stage juveniles (stages known to bemore susceptible to infection) to infectivecyprids according to the protocol of Ritchieand Høeg (1981). Following exposure, wewill maintain the crabs for three months anddissect them to check for internal stages ofthe barnacle. If internal stages are found inthe test crabs, we will also maintain asubsample of test crabs for a period of upto one year to determine if the parasites areable to mature.

We used five criteria to select native crabspecies to test: habitat overlap with thegreen crab, phylogenetic relatedness to thegreen crab, economic importance, ecologicalimportance and known susceptibility toother distantly related rhizocephalanbarnacles. For each of the three stages of thehost specificity evaluation described above,we will expose individual crabs (or, for thelarval settlement test, the limbs ofindividual crabs) to infective female cypridstages of the parasite. As a control for ourinfection techniques, we will expose greencrabs (or limbs) in an identical manner inseparate containers (separate containerswill prevent us from confusing hostspecificity with host preference). If the testcrabs are susceptible, we expect to see signsof infection in them. If the test crabs arerefractory, we expect to see signs ofinfection only in the green crabs.

Evaluating safety is different from typicalhypothesis testing. It is not sufficient todetermine that infection rates of test crabsare significantly less than infection rates ofgreen crabs. The question is, can theparasite infect test crabs? If a test crabbecomes infected, the answer isunquestionably yes. However, it isimportant to have sufficient power in thetest so that the probability of a falsenegative result is low. Increasing two factorsincreases the power of the test: theproportion of green crabs that the parasiteinfects and the number of test crabs

18 LAFFERTY

exposed. Probability theory allows acalculation of the minimum number oftest crabs needed to expose to keep theprobability of a false negative below1/1000 (our chosen alpha). In this case,we set the criteria according to themodel (1 - p)n < 0.001, where p equalsthe proportion of green crabs infected ina given trial and n equals the minimumnumber of test crabs to expose. Thisrelationship allows us to determine thenumber of test crabs needed forexposure depending on the success ofthe green crab infection rate. For eachtest, we will expose ten green crabs ascontrols and, based on the number ofgreen crabs infected, expose theappropriate number of test crabsneeded to meet the above standard. Ifthe barnacle infects only one or no greencrabs, we will consider the exposuretechnique flawed and start over.

FURTHER STEPS

Following a successful safetydetermination, techniques to raise thebiocontrol agent would needdevelopment. Improved barnacle culturetechnology would be required forinfecting large numbers of green crabs forrelease. Technological advancements inthe early detection of infected crabswould increase the efficiency of theprogram and decrease delays.Implementation of biological controlmight comprise a sustained program oftrapping and infecting crabs. This wouldalso serve as a means to monitor thesuccess of the control effort.

One safety advantage of this system isthat an initial field trial could easily bedesigned to only release femalebarnacles which would remain sterileunless male barnacle larvae wereintentionally released following theemergence of virgin externae in theinfected green crab population. Such atrial release would allow an evaluationof host specificity under field conditions

without having to introduce a breedingpopulation of the parasite.

This approach might be applicable to othermarine pests as well. One would assess theextent to which the pest is released fromnatural enemies, identify potential controlagents and select the most promisingcandidates for safety testing and potentialtrial release. In some, perhaps many, cases,biological control will not be feasible and wewill have to struggle with alternativeapproaches such as using pesticides,mechanical removal, subsidized fisheries ordoing nothing. The lessons from terrestrialbiological control indicate that host specificmetazoan parasites are most likely toprovide the level of control and safety mostappropriate for marine systems.

ACKNOWLEDGMENTS

This paper represents substantial collaborations withMark E. Torchin and Armand M. Kuris. In particular,I have liberally paraphrased from Lafferty and Kuris(1996).

LITERATURE CITED

Blower, S. and J. Roughgarden (1987) Populationdynamics and parasitic castration: a mathematicalmodel. American Naturalist 129: 730-753.

Carlton, J. T. (1985) Transoceanic and interoceanicdispersal of coastal marine organisms: the biology ofballast water. Oceanography and Marine BiologyAnnual Review 23: 313-371.

Carlton, J. T. (1987) Mechanisms and patterns oftransoceanic marine biological invasions in the PacificOcean. Bulletin of Marine Science 41: 467-499.

Carlton, J. T. (1989) Man's role in changing the face ofthe ocean: biological invasions and implications forconservation of near-shore environments.Conservation Biology 3: 452-465.Cohen, A. N., J. T. Carlton and M. C. Fountain (1995)Introduction, dispersal and potential impacts of thegreen crab Carcinus maenas in San Francisco Bay,California. Marine Biology 122: 225-237.

Gaines, S. D. and K. D. Lafferty (1995) Modeling thedynamics of marine species: the importance ofincorporating larval dispersal. Pages 389-412 in:McEdward, L. (ed.), Ecology of Marine InvertebrateLarvae, CRC Press, Boca Raton, Florida.

Grosholz, E. D. and G. M. Ruiz (1995) Does spatialheterogeneity and genetic variation in populations of


the xanthid crab Rhithropanopeus harrisii (Gould)influence the prevalence of an introducedparasitic castrator? Journal of ExperimentalMarine Biology and Ecology 187: 129-145.

Høeg, J. (1997) The parasitic castrator Sacculinacarcini as a possible biological control agent ofCarcinus maenas: background and results ofpreliminary work. Pages 69-75 in: Thresher, R. E.(ed.), Proceedings of the First InternationalWorkshop on the Demography, Impacts andManagement of Introduced Populations of theEuropean Crab, Carcinus maenas. TechnicalReport No. 11, Centre for Research on IntroducedMarine Pests, Hobart, Tasmania.

Kuris, A. M. (1974) Trophic interactions:similarity of parasitic castrators to parasitoids.Quarterly Review of Biology 49: 129-148.

Lafferty, K. D. (1993) Effects of parasiticcastration on growth, reproduction andpopulation dynamics Cerithidea californica.Marine Ecology Progress Series 96: 229-237.

Lafferty, K. D. and A. M. Kuris (1996) Biologicalcontrol of marine pests. Ecology 77: 1989-2000.

Le Roux, P. J., G. M. Branch and M. A. P. Joska(1990) On the distribution, diet and possibleimpact of the invasive European shore crabCarcinus maenas (L.) along the South Africancoast. South African Journal of Marine Science 9:85-93.

Minchin, D. (1997) The influence of the parasiticcirripede Sacculina carcini on its brachyuran hostCarcinus maenas within its home range. Pages 76-80 in: Thresher, R. E. (ed.), Proceedings of the FirstInternational Workshop on the Demography,Impacts and Management of IntroducedPopulations of the European Crab, Carcinusmaenas. Technical Report No. 11, Centre forResearch on Introduced Marine Pests, Hobart,Tasmania.

Murdoch, W. W., J. Chesson and P. L. Chesson(1985) Biological control in theory and practice.American Naturalist 125: 343-366.

Nichols, F. H., J. K. Thompson and L. E. Schemel (1990)Remarkable invasion of San Francisco Bay(California, USA) by the Asian clam Potamocorbulaamurensis. II. Displacement of a former community.Marine Ecology Progress Series 66: 95-101.

Ritchie, L. E. and J. T. Høeg (1981) The life history ofLerneodiscus porcellanae (Cirripedia: Rhizocephala)and co-evolution with its porcellanid host. Journal ofCrustacean Biology 1: 334-347.

Ropes, J. W. (1968) The feeding habits of the greencrab, Carcinus maenas (L). Fisheries Bulletin 67: 183-203.

Thresher, R. E. (ed.) (1997) Proceedings of the FirstInternational Workshop on the Demography, Impactsand Management of Introduced Populations of theEuropean Crab, Carcinus maenas. Technical ReportNo. 11, Centre for Research on Introduced MarinePests, Hobart, Tasmania.

Torchin, M. E., K. D. Lafferty and A. M. Kuris (1996)Infestation of an introduced host, the European greencrab, Carcinus maenas by a native symbiotic nemerteanegg predator, Carcinonemertes epialti. Journal ofParasitology 82: 449-453.

Torchin M. E., K. D. Lafferty and A. M. Kuris (2001)Release from parasites as natural enemies: increasedperformance in a globally introduced marine crab.Biological Invasions 3: 333-345.

Walton, W. C. (1997) Attempts at physical control ofCarcinus maenas within coastal ponds of Martha’sVineyard, MA (northeastern coast of North America).Pages 64-65 in: Thresher, R. E. (ed.), Proceedings of theFirst International Workshop on the Demography,Impacts and Management of Introduced Populations ofthe European Crab, Carcinus maenas. Technical ReportNo. 11, Centre for Research on Introduced MarinePests, Hobart, Tasmania.

Zibrowius, H. (1991) Ongoing modifications of theMediterranean marine fauna and flora by theestablishment of exotic species. Mésogée 51: 83-107.


Controlling Invasive Cordgrass: A Tale of Two Estuaries

Donald R. Strong and Debra R. AyresUniversity of CaliforniaBodega Marine LaboratoryBodega Bay, CA 92923

ABSTRACT: Open intertidal mud is a hallmark of Pacific estuaries. Shore birds, marine life,and the traditional fishing and oystering in these habitats depend upon openness. Aliencordgrasses of the genus Spartina threaten these estuaries. Growing further down theintertidal gradient than any other land plant, Spartina alterniflora (Smooth Cordgrass,introduced from the Atlantic coast) and Spartina anglica (English Cordgrass, introducedfrom the United Kingdom) form swards of dense stems and thick root-mats that excludeboth wildlife and traditional human activities.

San Francisco Bay has been invaded by Smooth Cordgrass brought from Maryland in themid 1970s. This alien species competes and hybridizes with the closely-related nativeCalifornia cordgrass, S. foliosa. The native species produces mostly hybrid seed where itgrows with the alien. Without control, the alien could cause the extinction of Californiacordgrass. Owing to concern for the native cordgrass, biological control is not an option forSan Francisco Bay. Alien and hybrid cordgrass are vulnerable to the herbicide Rodeo,which is licensed for use in aquatic systems.

Willapa Bay and Puget Sound, Washington have been invaded by Smooth Cordgrass andEnglish Cordgrass, respectively. Research has shown that both of these populations areunusually susceptible to a highly-specialized insect that feeds upon cordgrass in its nativerange; this insect does not occur in Washington, and no native cordgrasses occur thereeither. This circumstance suggests that biological control of the alien populations ofcordgrass in the estuaries of Washington State is a sensible control option.

CORDGRASSES IN AMERICAN PACIFICESTUARIES

Open mud without vegetation is ahallmark of middle and lower intertidalzones in Pacific estuaries. The highintertidal region is occupied by low-growing species, with Distichlis spicata andSalicornia virginica often holding the lion’sshare of space; the remainder is shared byvarious combinations of such species asTriglochin maritima, Jaumea carnosa, andDeschampsia caespitosa. From 20 to 30additional species complete the list ofPacific salt marsh plants (Chapman1977). California Cordgrass, Spartinafoliosa, frequently forms a modest lowerboundary to the marsh vegetation,

southward from Sonoma County, north ofSan Francisco Bay, through BajaCalifornia. No native cordgrasses arefound north of Sonoma County on thePacific coast. California Cordgrass is notan aggressive species, rarely invadingstands of other plant species. It is arelatively short cordgrass; most plants areless than 0.75 m tall. With a culm densitythat is low for cordgrasses, S. foliosa doesnot cause appreciable accretion ofsediment.

Smooth Cordgrass, Spartina alterniflora,native to Atlantic and Gulf coast marshes,occupies much lower intertidal habitatsand is distinctly more aggressive thanCalifornia Cordgrass. Smooth Cordgrass

INVASIVE CORDGRASS 21

regularly invades patches of othersaltmarsh species, grows to more than ameter tall, and forms dense monospecificswards (Adam 1990). English Cordgrass,Spartina anglica, is as aggressive asSmooth Cordgrass (Gray et al. 1991). Bothspecies have spread widely in some of thePacific estuaries to which they have beenintroduced. Both present substantialthreats to Pacific saltmarsh species,including plants, fishes, marineinvertebrates, and even marine mammals.A particularly conspicuous menace is toshorebirds, which forage upon open mud.Pacific estuaries have been greatlyreduced by human activities over the pastcentury (Macdonald 1977), and invasiveSmooth and English cordgrasses threatento accelerate this loss of habitat. Aliencordgrasses also threaten traditionalhuman uses of Pacific estuaries, hinderingaccess to the shore, interfering withmariculture and navigation, and blockingflood control channels (Daehler andStrong 1996).

Mindful of the uniqueness of the openmud vulnerable to invasion by S.alterniflora in Pacific estuaries, Adam(1990) remarked in his global overview ofsalt marshes that “...should [SmoothCordgrass be introduced] it may causeprofound change to western marshes.”Little did he appreciate the degree towhich his prediction has been realized.Smooth Cordgrass was introduced toWillapa Bay at least 60 years ago(Scheffer 1945; Sayce 1988) and hasspread widely, reducing habitat formigratory birds, promoting siltation ofmud and sand flats, and overgrowingoyster culture beds (Boyle 1991). EnglishCordgrass was introduced into PugetSound in 1961 and has also spreadwidely, causing similar impacts to theenvironment (Parker and Aberle 1979). Inthe past few years the State ofWashington has mounted a large-scale,expensive effort to control thesecordgrasses with a combination of cuttingand glyphosate herbicide treatments (J.Civille, pers. comm.).

Smooth Cordgrass was introduced to SanFrancisco Bay about twenty years ago(Daehler and Strong 1995) and hasspread widely. It now competes(Callaway and Josselyn 1992) andhybridizes (Ayres et al. 1999) withCalifornia Cordgrass throughout the southportion of the Bay. San Francisco Baysupports the largest remaining stand ofCalifornia Cordgrass in the United States.The habitat of the alien Smooth Cordgrasscompletely overlaps that of CaliforniaCordgrass, and the spread of theaggressive alien threatens the veryexistence of this important native species.

POSSIBILITIES FOR CONTROL

The complementary touchstones of safetyin biological control are (a) choice ofenemy species with very narrow diets and(b) target species with no close relatives.These reduce the chance of collateraldamage to species other than the intendedtarget. Therefore, classical biologicalcontrol is not an option in San FranciscoBay because any introduced organism thatwould harm alien cordgrass wouldprobably also harm the closely relatednative California Cordgrass. Thus, onlychemical and physical controls areoptions in San Francisco Bay. Cutting theplant and applying the herbicide Rodeo™have shown promise in preliminary trialsin San Francisco Bay (Chamberlain 1995).

One complicating factor is thehybridization that occurs between theintroduced Smooth Cordgrass and thenative California Cordgrass in SanFrancisco Bay. The hybrids are notmorphologically distinct from eitherparent, and RAPDs (randomly amplifiedpolymorphic DNA) are used fordetermining hybrid status (Daehler andStrong 1997a). Current work (Ayres et al.1999) shows that hybrids are widespreadthroughout the south end of the Bay, andthat the hybrid swarm consists ofbackcrossed as well as F1 individuals.These hybrids are fertile and are

22 STRONG AND AYRES

reproducing by seed. Morphologically,hybrids appear to be as fit as eitherparent, and they will probably becomemore common as seed disperses ever morewidely in the Bay. Eradication effortsmust be well informed about thedistribution of these hybrids.

In contrast to the situation in SanFrancisco Bay, the alien cordgrasses inWashington State are prime candidatesfor biological control. No close relatives ofcordgrass live in estuaries or near thecoast north of the San Francisco Bayregion, so Willapa Bay and Puget Soundare safe places to introduce highlyspecialized insect herbivores of cordgrass.These insects are restricted to areas wherecordgrasses are native (Strong et al. 1984:Daehler and Strong 1997b) so thepopulations of alien cordgrasses inWillapa Bay and Puget Sound have notbeen exposed to these insects during theirstay in the Pacific. Our experiments haveconcentrated upon the planthopperProkelisia marginata, which is native toCalifornia where it feeds upon CaliforniaCordgrass, and to Atlantic and Gulf coastmarshes where it feeds upon SmoothCordgrass.

Smooth Cordgrass from Willapa Bay isquite vulnerable to the planthopperProkelisia marginata (Daehler and Strong1995). We discovered this in thegreenhouse at the Bodega MarineLaboratory in Bodega Bay, California,where many Willapa Bay clones fed uponby P. marginata were severely harmed,and some were killed. High densities ofthe planthopper led to the deaths ofabout 1/3 of the Willapa Bay plants afterthe second summer of feeding by theplanthopper. The control plants withvery-low (but not zero) densities of thehopper grew normally and suffered verylow mortality. This suggests that Prokelisiamarginata could harm Smooth Cordgrassin Willapa Bay, were it introduced.Similarly, we have recently found in thegreenhouse that both Prokelisia marginataand Prokelisia dolus, a sibling species to P.

marginata that feeds upon SmoothCordgrass on the Atlantic and Gulf coastsand upon California Cordgrass inSouthern California (Denno et al. 1996),feeds upon and kills Spartina anglicaclones from Puget Sound (Wu et al. 1999).

LOST RESISTANCE

The low resistance of the exiled cordgrasspopulations to feeding by Prokelisiaspecies is unusual. In contrast, SmoothCordgrass from both native areas and SanFrancisco Bay, and California Cordgrassare quite resistant to feeding by theseinsects (Daehler and Strong 1997b). Theseplants suffered little even at high densitiesof the planthopper.

While Smooth Cordgrass in San FranciscoBay was never exiled from specialistSpartina-feeding herbivores, theWashington populations of cordgrasshave grown through a number ofgenerations in the absence of specialistinsect herbivores. Smooth Cordgrass hasbeen in Willapa Bay for at least 60 years(Scheffer 1945; Sayce 1988). This speciescan set seed within three years, so thisamounts to perhaps twenty or moregenerations of isolation from these insectsin Willapa Bay. English Cordgrass hasnever been subjected to herbivory byProkelisia spp. This plant species arose inEngland during the 19th century from across between European Spartina maritimaand S. alterniflora from North Americathat was probably introduced with cast-off ships’ ballast (Ferris et al.1997). Thisproduced the sterile Spartina x townsendii,which subsequently gave rise to the fertileamphiploid Spartina anglica.

Why are these exiled cordgrasspopulations less resistant to Prokelisiathan populations that have not beenisolated from specialist herbivores? Threegeneral ideas suggest themselves. Genesfor herbivore resistance could have beenabsent by chance from the foundingpopulation resulting in a lack of resistance

INVASIVE CORDGRASS 23

in contemporary populations. Second, thefounding population could have gonethrough a deleterious genetic bottleneck inwhich inbreeding led to a loss of vigorresulting in erosion of herbivore defenseand reduced competitive ability (Barrett1982). However, sexual reproduction andrapid population growth can sometimesstaunch such a loss of genetic diversity(Slatkin 1996), so it is not surprising thatweed populations established by a fewfounders can be genetically diverse (Colosiand Schaal 1992).

The final hypothesis is based upon thepremise that resistance or tolerance toherbivores represents a significantmetabolic and developmental cost to aplant. The plant maintains resistance at acost of slower growth or otherwisediminished capacities reducing itscompetitive ability, a major component offitness in weeds (McEvoy 1993). Thus,resistance should be selected against inplant populations that have been exiledfrom their specialist herbivores whereresistance has no value. For example,Blossey and Kamil (1996) have foundsuch a correlation in purple loosestrife;lower resistance is coupled with greatercompetitive ability in weedy NorthAmerica and Australian populationsrelative to native European populations ofthis plant. In a test of his trade-offhypothesis, Dino Garcia-Rossi (1998) ofour laboratory performed a greenhouseexperiment in which Smooth Cordgrassclones from Willapa Bay were placed incompetition with clones from SanFrancisco Bay, in the presence of very lowor very high densities of the planthopper.Confirming the susceptibility-resistancepatterns found earlier (Daehler and Strong1997b), the San Francisco Bay clonesthrived while the clones from Willapa Baywere all killed in the treatmentcombinations that included high densitiesof the planthopper. However, the trade-off hypothesis was not confirmed as therewas no difference in competitive abilitybetween the two populations.

A practical question remaining is, will theplanthoppers harm alien cordgrasses inthe field? Questions for basic science are,what is (are) the mechanism(s) that causethese phloem-feeding insects to harmvulnerable cordgrass populations, andwhy are some populations vulnerable?

LITERATURE CITED

Adam, P. (1990) Saltmarsh Ecology. CambridgeUniversity Press, New York.

Ayres, D. R., D. Garcia-Rossi, H. G. Davis, and D. R.Strong (1999) Extent and degree of hybridizationbetween exotic (Spartina alterniflora) and native (S.foliosa) cordgrass (Poaceae) in California, USAdetermined by random amplified polymorphic DNA(RAPDs). Molecular Ecology 8: 1179-1186.

Barrett, S. C. B. (1982) Genetic variation in weeds.Pages 78-112 in: Charudattan, R. and H. L. Walker(eds.), Biological Control of Weeds with PlantPathogens, John Wiley & Sons, New York.

Blossey, B. and J. Kamil (1996) Is the superiorcompetitive ability of invasive plants a result ofchanges in biomass allocation patterns? Bulletin ofthe Ecological Society of America 77: 41.

Boyle, B. J. (1991) Policy considerations. Pages 7-8in: Mumford, T.F., Jr., P. Peyton, J.R. Sayce and S.Harbell (eds.), Spartina Workshop Record(November 14-15, 1990, Seattle, Washington),Washington Sea Grant Program, University ofWashington, Seattle, Washington.

Callaway, J. C. and M. N. Josselyn (1992) Theintroduction and spread of smooth cordgrass(Spartina alterniflora) in South San Francisco Bay.Estuaries 15: 218-226.

Chamberlain, S. (1995) Comparison of methods tocontrol Spartina alterniflora in San Francisco Bay.M. A. thesis, San Francisco State University, SanFrancisco.

Chapman, V. J. (ed.) (1977) Wet Coastal Ecosystems.Elsevier Scientific Publishing Co., New York.

24 STRONG AND AYRES

Colosi, J. C. and B. A. Schaal (1992) Geneticvariation in wild proso millet. Proceedings of theNorth Central Weed Science Society 47: 21-22.

Daehler, C. C. and D. R. Strong (1995) Impact of highherbivore densities on introduced smooth cordgrass,Spartina alterniflora, invading San Francisco Bay,California. Estuaries 18: 409-417.

Daehler, C. C. and D. R. Strong (1996) Status,prediction and prevention of introduced cordgrassSpartina spp. invasions in Pacific estuaries, USA.Biological Conservation 78: 51-58.

Daehler, C. C. and D. R. Strong (1997a)Hybridization between introduced smoothcordgrass (Spartina alterniflora; Poaceae) and nativeCalifornia cordgrass (S. foliosa) in San FranciscoBay, California, USA. American Journal of Botany84(5): 607-611.

Daehler, C. C. and D. R. Strong (1997b) Reducedherbivore resistance in introduced smooth cordgrass(Spartina alterniflora) after a century of herbivore-free growth. Oecologia 110: 99-108.

Denno, R. F., G. K. Roderick, M. A. Peterson, A. F.Huberty, H. G. Dobel, M. D. Eubanks, J. E. Loseyand G. A. Langellotto (1996) Habitat persistanceunderlies intraspecific variation in the dispersalstrategies of planthoppers. Ecological Monographs66: 389-408.

Ferris, C., R. A. King and A. J. Grey (1997)Molecular evidence for the maternal parentage inthe hybrid origin of Spartina anglica C. E. Hubbard.Molecular Ecology 6: 185-187.

Garcia-Rossi, D. (1998) Consequences of the loss ofherbivore resistance for invasive cordgrass Spartinaalterniflora. M. S. thesis, Sonoma State University,California.

Gray, A. J., D. F. Marshall and A. F. Raybould(1991) A century of evolution in Spartina anglica.Advances in Ecological Research 21: 1-62.

Macdonald, K. B. (1977) Coastal salt marsh. Pages264-294 in: Barbour, M. G. and J. Major (eds.),Terrestrial Vegetation in California, John Wiley &Sons, New York.

McEvoy, P. B. R., Cox, C. S. and M. Huso (1993)Disturbance competition and herbivory effects onRagwort Senecio-Jacobaea populations. EcologicalMonographs 63(1): 55-75.

Parker, R. C. and B. Aberle (1979) A SituationReport on the Spartina Infestation in NorthwestWashington. Washington State Department of Game,Olympia, Washington.

Sayce, K. (1988) Introduced Cordgrass, Spartinaalterniflora Loisel. in Saltmarshes and Tidelands ofWillapa Bay, Washington. U. S. Fish and WildlifeService, Ilwaco, Washington.

Sheffer, T. H. (1945) The introduction of Spartinaalterniflora to Washington with oyster culture.Leaflets of Western Botany 4(6): 163-164.

Slatkin, M. (1996) In defense of founder-flushtheories of speciation. American Naturalist 147:493-505.

Strong, D. R., J. H. Lawton and T. R. E. Southwood(1984) Insects on Plants: Community Patterns andMechanisms. Harvard University Press, Cambridge,Massachusetts.

Wu, M.-Y., S. Hacker, D. Ayres, and D.R. Strong(1999) Potential of Prokelisia spp. as biologicalcontrol agents of English cordgrass, Spartinaanglica. Biological Control 16:267-273.

biological invasions in aquatic ecosystems: impacts on ... · pdf fileproceedings of a...

Documents