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Toxins Mediate Glaucous-Winged Gull Predation on Bivalve Prey

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Toxins Mediate Glaucous-Winged Gull Predation on Bivalve Prey SEQUESTERED PARALYTIC SHELLFISH POISONING TOXINS MEDIATE GLAUCOUS-WINGED GULL PREDATION ON BIVALVE PREY RIKK G. KVITEK 1 Departmentof Zoology,University of Washington,Seattle, Washington 98195 USA A•sllo,cr.--Glaucous-winged Gulls (Larusglaucescens) avoid paralyticshellfish poisoning by conditionedaversions developed after the regurgitationof contaminatedbivalve prey. In feeding experimentswith free-rangingGlaucous-winged Gull chicks,toxic (445 •g saxitoxin equivalentsper 100 g) butter clams(Saxidomus giganteus) were regurgitatedin <5 rain (n = 58), and nontoxic butter clamswere never regurgitated(n = 30). Chicks that had ingested toxicS. giganteusthen refusedto eat either toxicor nontoxicbutter clamsoffered later, but they acceptedother bivalve prey. In feeding experimentswith wild adult and juvenile L. glaucescens,gulls took significantlyfewer butter clamsat a site where S. giganteushas been chronicallytoxic for > 14 yr than they took at a nontoxicbut otherwisecomparable site. These preferenceswere species-specificand independentof prey toxicity or whether the live clams were intact or removed from their shells.The gulls showedno differencebetween sites in their preferencesfor three other bivalve species(Clinocardium nuttalli, Protothacastaminea, Tresuscapax), all of which containedeither no or very low levels of toxins at both sites.The aversionto intact but not to shuckedbutter clamswas more strongly developedin adults than in juveniles.Most of the gulls that ate butterclams at the toxicsite discarded the siphons (which accountfor the majorityof the toxicity in contaminatedbutter clams)of both toxic and nontoxicbutter clams,but they never discardedsiphons of other bivalves.Gulls at the nontoxicsite never discardedthe siphonsof bivalve prey. I suggestthat avian predators generallyare not at risk from paralyticshellfish poisoning toxin via bivalve vectorsbecause they can detectand avoid toxic prey. Becauseof the apparentinability of gulls to discriminate between toxic and nontoxic individuals of the same prey species,avian predation pressure on somebivalve populationsmay be greatly reduced.Received 16 [uly 1990,accepted 8 November 1990. PARALYTICshellfish poisoning (PSP) results al. 1971, Shumway 1990). Toxic "red tides" from the consumption of food contaminated (bloomsof toxigenic dinoflagellates)recur glob- with highly lethal neurotoxinsproduced by ally, appear to be increasingin frequency, and toxigenic dinoflagellates (Protogonyaulaxspp.) result in numerous shellfishery closuresand (Halstead 1978). Paralytic shellfish poisoning human illnesses and deaths every year (Hal- toxins (PSPT) can move through marine food stead1978, Nishitani and Chew 1988,Shumway chains and have been implicated in the mass 1990). mortalities of planktivorous fish (White 1977, Although many marineand coastalbirds prey 1980, 1981a, b) and seabirds (McKernan and on bivalves (Oldham 1930, Recher 1966, Barash Scheffer 1942, Coulson et al. 1968, Bicknell and et al. 1975,Sanger and Jones1982, Vermeer 1982, Walsh 1975,Sasner et al. 1975,Armstrong et al. Bourne 1984, Nettleship et al. 1984, Richardson 1978, Hockey and Cooper 1980, Nisbet 1983). and Verbeek 1986, Roberts et al. 1989) known The most common vector of the toxins in cases to concentratePSPT (Quayle 1969, Prakashet of bird mortalities has been planktivorous fish, al. 1971),avian mortalities have only rarely been yet it is suspension-feedingbivalves that pre- associatedwith PSPTcontaminated bivalve prey sent the greatestparalytic shellfish poisoning (Bicknell and Walsh 1975, Sasner et al. 1975, risk to human health (Quayle 1969, Prakashet Hockeyand Couper 1980).Indeed, it is the rar- ity of PSP-relatedavian deathsthat is most sur- prising given the extremelethality of the toxins • Present address:Moss Landing Marine Labora- and their widespread occurrence. Paralytic tories, P.O. Box450, Moss Landing, California 95034 shellfish poisoning toxins are among the most USA. potent neurotoxins known and are fatal to most 381 The Auk 108: 381-392. April 1991 382 RIKKG. KVITEK [Auk,Vol. 108 vertebratesat extremely small concentrations 1984, Nettleship et al. 1984, Richardson and (Halstead1978). The World Health Organiza- Verbeek 1986). tion has set the maximum PSPT concentration Gulls (Larusspp.) commonlyprey on bivalves allowed in shellfishfor human consumptionat by dropping them from aloft to crack open the 80 •g STX equivalents/100g. (Paralyticshell- shell (Oldham 1930, Barash et al. 1975, Roberts fish poisoningtoxins are derivativesof saxitox- et al. 1989). In the Pacific Northwest, Glaucous- in [STX], one of the two most lethal PSPT, and winged Gulls (Larusglaucescens) frequently for- mouse bioassay results are expressed in STX age on infaunal bivalves (Protothacastaminea, equivalents.)In two studieswith birds,pigeons Tapesjaponica, Clinocardium nuttalli, and Saxido- (Columbasp.) were found to have a LD50of 90 musgiganteus) (Barash et al. 1975, Vermeer 1982, •g STX equivalents/kg(see Halstead 1978), and pets. obs.). Each of these prey species retains the lethal dose for EuropeanStarlings (Sturnus PSPTfor varying lengths of time (5 weeksto 2 vulgaris)was <490 •g STX/kg (Kvitek and Beit- yr) following exposure to a toxic "red tide" let 1988, 1989). Because bivalve toxicities are (Quayle 1969, Shumway 1990). Red tides are routinelywell abovethese levels in manyareas, commonalong the west coastof North America, often measuredin the thousandsof gg STX/100 with many beachesclosed to clamming each g (Quayle 1969, Prakash et al. 1971, Halstead year (Quayle 1969, Nishitani and Chew 1988), 1978, Shumway 1990), either avian survival or but there have never been reports of gull mor- their predationon bivalvesmust be profoundly talities associated with toxic shellfish. In Wash- influenced at these times, unless the birds are ington State alone, bivalves at >50 sites con- highly resistantto PSPT. tained PSPT concentrations above the public Immunity to PSPT is not the most probable health closurelevel (80 •g STX equivalents/100 explanation for the rarity of bivalve-related g) during 1989 (Washington State Department PSPTbird mortalitiesgiven that PSPThas been of Health unpubl. rep.). implicated in bird kills via other vectorsas well My primary purpose was to resolve the par- as bivalves in a few cases.A more likely hy- adox of seabirds that prey on bivalves but do pothesis is that avian predators may develop not die as a result of PSPT-contaminatedprey. aversionsto toxicbivalve prey. Tufts (1979)cites I conducteda seriesof feeding experimentswith anecdotalaccounts of residentgulls (Larusspp.) free-ranging wild Glaucous-winged Gulls to and eiders (Somateriaspp.) avoiding toxic shell- determine (1) if experienced and naive gulls fish that kill migratory Black Ducks (Anasrub- differ in their responseto toxic prey, (2) wheth- ripes),and of a duck that regurgitated force-fed er or not naive gulls develop a conditioned toxic mussels.Acquired aversionsto toxic prey aversionfollowing the ingestionof toxic prey, have been well documented for some insectiv- and (3) at what level (individual, species,genus orous birds (e.g. Blue Jays,Cyanocitta cristata, or family) conditioned gulls discriminate be- that encounter monarch butterflies; Brower and tween prey, if an aversion is formed. I chose Fink 1985). These specieshave learned to iden- butter clams as the toxic prey because of the tify and avoid prey that is toxic or likely to be availability of highly toxic individuals due to toxic, and in some cases to circumvent the this species'tendency to retain PSPTfor > 1 yr chemical defensesof their prey by selective re- (Quayle 1969, Shumway 1990). They are also jection of the most toxic tissues. Similar re- abundant in many intertidal habitats and thus sponseshave been demonstrated in sea otters frequently eatenby Glaucous-wingedGulls and (Enhydralutris; Kvitek et al. in press) and fish other birds (Barash et al. 1975, Vermeer 1982, (Leptocottusarmatus; Kvitek MS) fed PSPT-con- Vermeer and Bourne 1984, pets. obs.).I selected taminated bivalves. three sitesfor the experiments.One was a Glau- If it occurs, avoidance of bivalve and other cous-wingedGull breeding area that does not intertidal invertebratesby avian predatorsas a supportinfaunal bivalve prey asforage for gulls; result of sequesteredPSPT could have signifi- the second, an area heavily used by foraging cant ecological and economic implications. Glaucous-wingedGulls where butter clamsbut Shorebirds have been shown to have profound not all bivalves are chronically toxic; and the effectson infaunal prey abundanceand distri- third, a similar but nontoxic site as a control. In bution (O'Conner and Brown 1977, Evans et al. this way I was able to comparethe feeding be- 1979, Quammen 1984) and to prey heavily on havior of birds chronically exposedto PSPT- commerciallyimportant bivalve species(Bourne laden butter clams with that of naive chicks at April 1991] Gullsand Shellfish Toxins 383 TAnIll 1. Bivalve communitiesat ScatchetHead (nontoxic site) and Middle Ground (toxic site). Toxicity levels aregiven for bivalvesused in gull feedingexperiments; NDT = nodetectable toxin (< 37•g STXequivalents/ 100g). All sampleswere analyzed with mousebioassay, except the cockles,which were tested with high performanceliquid chromatography. Means _+ SD are givenfor bivalvedensity (n = 5 and 6 for Scatchet Head and Middle Ground, respectively). Scatchet Head (nontoxic) Middle Ground (toxic) Toxicity Density Toxicity Density Species (ug STX/100g) (ind./0.25m 2) (ugSTX/100 g) (ind./0.25m
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