Cook of

Ecology and Demographics ofPacific Sand Lance, Ammodytes hexapterus Pallas, in Lower Cook Inlet, Alaska

By

Martin D. Robards

Athesissubminedto the Schoolof GraduateStudies

inpartialfulfillmentof the requirementsforthedegreeof

Masterof Science

Fisheries Conservation Chair DepartmentofBiology MemorialUniversity ofN ewfound1and

March2000

St.John's Newfoundland

A...ee

Distinct sandlancepopulations occurwithin therdativdysmall geographic areaof LowerCookInlet.AIasIr:a.Markedmcso--scale differencesinabundaDce. growth.and moru.lityexistedas • consequence ofdiffering oc:c:anognpbic regimes.Growthme withinpopulations (betweenyean)waspositivelyC01'TeW:cdwith tc:mpc:nture.

However,this didnotntend to inter-population comparisons where differing growth rateswerebettercorrelated to marineprodu ctivity.Opaque otoliths form injuvenilesand lance during their first summercoincidingwiththeirperiodofrapidgrowth.Subsequent opaque zones aredepo sitedduringspring,inconjunctio nwithrap idlyincreasing water tem peratures.Areal rather than radialdescript o rs of oto lithsize provide the bestrelation tosandlancelength.Asingle linearregr essionwasinsufficienttodescribethis rdationshipwithseparate linear regressionsneeded for both juvenilesandadults.No sexual.dimorphismwasobservedfor sand lance in lenitHt-weight(gonad-free) or Icngth-at-agc.Most sandLancere.achedmaturity in their second year.Fiddobservations andindices of maturity,gonaddevelopment,. and ova-sizedistributionallindicatedthat sand lance spawnonceeachyear.Males mature earlierintheseason than females.but females(31%)attain.highergooadosomatic indexthanmales (21%).sandLance spawned intertidallyinlateSeptemberandOctoberonfinegnvdfsandybeachessoon afterthe seasonalpeak:inwatertemperatures.Fecundityoffemales(93. 199nun) was proportio naltolength,ranging from 1,468to 16,08 1ova.Spawned eggs wen:1.02± 0.08nun in diameter,de mersal. sligh tly adhesive.and depo sitedinthe intertidal just below thewaterline.Sandlan ce embryos developed over 67 daysthroughperiod s of

intertidal exposure and sub-freezing air tcmpentures.Meandry-weightenergyvalue of sandlancecycles seuoDaliy.peakinginspring andearly summc:r-(20.91Idg' lformales.

21.08Idg-^Iforfemales), and subsequently decliningbyabout25%during late summer and

ran

(15.91ldg-Iformales,15,74Idg'!forfemales).Declinesin energydensity during late summerparaUdedgonadaldevdopment.,sandlancec:mc:ringthe wimer with closeto their minimum wholebody encI"8Yecntea.Dryweight~densitiesof juvenilesincreased froma minimum 16.67Idg-^Ito amaximumof19.6 8idg-^Iand are higherthan adultsinlat e summer.

iii

Table oleo. tu b

I'J&<

Ahmad

~~~ .

list of Tables

listof FJgUreS riii

.AckDowIcdgements mii

Poem:After the Sand LanceDigging ~

Chapt er1- Matuntion. fecundity, andintatidalspawningof Paci6 csand

lanceinthe DOI1hcrn Gu1fofAlasIca IJ

1.1- Abstract . l~.

1.2- lntrodu ction.._._. .._._ _ _ __ ._J.~~

1.3- Materialsand Methods._ _..__._ __ __ _._ _ _J =f.

1.4- Results_. __...•.._. __._ _ _ _ _ .l~.9.

1.S- Discussion. _ .._._..__ _ _.._ _ _._ __. _ .l~.:lJ Chapter 2 - Changesinproximat e compositio nandsomaticenergycontent

for Pacificsand lancerelati vetomaturity,season.andlocati on.

_ ____._ . . .__ ._...._.H.

2.1- Abstract ~~1

2.2- Introduction 2,:;t

2..3- Method s ~=f.

2.4- Results, ~~.I

2.5- DiscussioQ. ~:.11

Chapter3- Gro'Wthand Abundance ofpaci£icsandlanceunder differing

oceanographic regimes. l-J.

3.1- Ahmad H.

3.2- Introduction _l:;t

3-3- ~hicSemng .__ ._. J~l

3.4- MaterialsandMcthods.__._... ;t~1

3.5- ... .._._.. . .. Hl

3.6- Discussion.. . ._. _..__ .._._..__._ __ _._._ __.;t~1.7.

BibliographyandReference s . ._. _ _ _

.. "'J.

ListofTabla

TableI-I. PercentageofAmmodyteshexapterus classified into maturity stagesby month fbr fish collectedinKachemak Bay during 1996 11997.Maturi ty stageswere I=resting, ll-developing.Illeripe, IV=running. vespent,VI=recovering... ..._._ __...\~.L~.

Table 1·2. Mean gonadosomatic index (±95%CI) formale and femalesand lance collectedinOctoberof1996and1997fromspawning schools inSeldoviaBay.Numbersinparentheses are samplesizes..._. __ ...td...~.

Table1-3. Maturation statusofA.hexapterusattwo collectionareas in

sout hcentralAlaska. ...l:-J~

Table1-4. Sexratios ofsandlance collectedinKachemakBayatdifferent maturitystagesduring1996 ond 1997 _ _._._._.. H!2

Table1-5. Percentcontributionto theoverall spawning school fecundity derivedfromfemales of the differentage groupspresent in October1996and1997 ("...165).._._..._••_ ..._.l~J_~

Table2-1. Regression parameters forthe fresh wet weight-dry weight relationship of adultandjuvenilesand lance collectedinLower Cook

Inlet during 1996 ._. .__._._. _ ___._._.__7,:-.1

Table 2-2. Mean(SD)monthlyproximatecompositionfor adult male and female sandlance collectedinLower Cook Inlet during 1996.

____. ••_ •• .. .. . ._.__._. •.• ...7,:-_9.

Table 2-3. Meanproximate composition for juvenilesandlance collected inLowerCookInlet during19%._•••_._••••_•• .. ._•••••_.••••• .._7,::1..1

Table2-4. Energy value (kJ/fish)based on mean adult and juvenile fish sizes collectedbybeachseineinLowerCookInlet during 1996 ..._::'.:-Zl.

Table3-1. Relationshi pbetween root otolith area and fork-length for sand lance collected inlo werCookInlet.Relations hipisexpressed as:Fork lengthes(a-roototolitharea)+b. .. . . ;1:-J.9.

Table 3-2 MeanJuly sea-swface-temperatures(SSTs) for 1996 and1997at Chisile.Island,inner and outerKachemakBay,andthe Barren Islands . ...__._... _

Table3-3. Catchstatisticsfor sand lance coUectedinLower Cook Inlet during 1996and1997.. .. _

.,],:-.1..$.

Table3-4. Rebtionshipbetween length and weightfor sand lance collected inlower Cook Inlet during1996 and199 7.Two seasonally different

regressions aregivenforinner·Kachemak.Rd ationshipis~ as:Loglo(Weigbt)-(a·Log,oFork:Length)+b._ _---...-.J:-k J.

Table 3·5. Von BertaIanf£yparametersand(standarddeviation) for sandlance collectedwithinCook Inlet. ..._.. . ._.1~.z.4

ListorYapra

FigureI-I: Locationofsand lance collectionswithin CookInletand PrinceWilliamSound(PWS).SpawningoccurredatRaby"s spit(notvisibleatthis scale),locatedonthe west sideof

SeldoviaBay. _l:.~

Figure1-2: Seasonal vanationinmaximum and minimumairtem pera tures andsea surface temperatures (SSTs)atKachcmaJc:Bayin1996 and1991.DiamondsonSST plotsindicate onset ofsandlance spawning...__. .. .__. . .__._._ ..._._.H.Q

Figure1-3: Lengths-at -age (%1 sd)ofadultmale(A.)andfemal e (.)sandlance collected before gonad development(MayandJune ),during sexual maturation(Julyand August ), andwhile ripeandspawning(Septeukr andOctober)inKachcmakBay.Numben are samples sizes(MIF)and numbeninparen theses are overall mean lengths for sexes combined.

_ __ _ _ _ _ _ _ _ __ _ .---1012

Figure1-4: Regressionplots oflength(nun) against gonad -freebodyweight (g;Log1otransfonneddata) fo rmale(A.)andfemale (.)sand lance.

Sand lan ce were collectedbeforegonad development (MayandJu ne;

n-236male,226 female),durin gdevelopmen t (Julyand August;

rr-580male,575female). and while ripe and spawning (September andOctober;rr-475 male, 361 female).Regressionequations are

forsexescombined. Lo

i-u

Figure1-5' Seuonalchanges inmale (_)andfemale(D) gonadosomaticindices (J:95%confidence intefvals) forsandlance collectedinKac:bemak BaybetweenMay1996andOctober 199 7.Numbers aresample

sizesforeach month.. ... ... .kl.<I.

Figure1-6: Scatter plot ofmale(n=131) andfemale(n-91) GSI'sagainst bodylength forripe (stage-Ill)sandlancecollect edduring October fromspawning schoolsinKachemakBayduring1996and 1997. 1:.1.7.

Figure 1- 7; Regressi o noffecundity onbody length(mm;Iogl otransformed data)for pre-spawning (stage-II)femalesand lance collectedfrom K.achemakBay(n-51.

r'-

-0.86,P<O.Ol;loglofecundity--2.54

+(2.99·1og,~ength). HQ

Figure 1-8: Sizedistributionofew foundinovaries

ono

ripe female sand lance collected from spawning schoolJinKachemak Bayduring 1996 and 1997(n-4500,mean=1.01nun.SO-0.08mm).__ 1:2.1.

Figure 1-9: Graphicalrep resen tati o nof sandlance spawningsubstr at ein Seldovia Bay (median particlediameter=1.9nun).Phiunits

=.Iogzparticle diameter (rom). .__.. .. .__.. _

Figure2-1. Location ofKachemak. Bayand LowerCook Inlet,Alaska.

_ .\~_~_l

_..

_ --_._---- _ ._._._. __ .. _-_._-_ .. _ ._.

-_._---_~::~.

Figure2·2. Monthly energy density(kJg-1dry mass) and gonadosomatic index (OS!) for adult male(0) and female (e)sand lancecollected inKachemak Bay.Errorbarsare means±standard deviation; small circles arerangeofdata._.__. ..._.__..._...._._...._..._....__.. ._.2:J.Q

Figure2-3. Seaso nal condition factor (K')for male(··'0 "')and female (_ -) sand lance collected in Kachemak Bay.Erro rbars arc means±one standard deviation. Verticaldashed line indicates time ofspawni ng (RobardsetaJ.1999 a)...

_... ._ _

~~.u.

Figu re2-4. Totalenergy densities(kIg-tdry mass)of juvenilesand lance collected monthlyinKachemak Bay.Twobars areshown for each month sampled; replicates1 and2.Relativeenergy contributions of protein (black bar) and lipid(w hite bar)are

shown.. ._..__... ..._~~H

Figure 2-5. Relationship betweensize and condition factor(K.')fOI"juvenile sand lancecollectedinKachemak Bay.Error barsare mean and range of the twosamplesfOI"eachsize-class.__.._ ...~~J.~

Figure3-1. Location of studysitesinLower Cook Inletshowingtheprevailing currents (basedon Trasky et aI.•1977) .Study sitesareA-Barren Islands,B-outer-Kachemak Bay, C-inner-KachemakBay, D - Chisik Island.

em

transectsareshown asdark lines ;1;:1

Figure 3-2. Seasonal proportionsofotoliths withopaque edgesfor adult (-) and juvenile(....)sand lance.Thegray line depictsmean daily sea-surface temperature (SST;1996and1997) __ ._ _ J~.L+.

Figure3-3. Relationbetween squarerootof otolith area and forklength (FL) for studysites withinLowerCook Inlet, Alaska(0

=

juvenile,•

=

adult).

...Hl.

Figure3-4. Temperatureand salinity profiles for transectsinLowerCook InletattheBarrenIslands, Inner-and outer-Kachemak Bay,and Chisik:Island.Transect locationsaredepictedinFigure1with the compass direction given at the base ofeach profile _.J~J.~.

Figure 3·5. Indices of catchand abundancefrom beachseinedata collected atChisikIsland,inner- andouter-Kechemak Bay,and theBarren Islands duringJune-September1996 and 1997;_

=

juven iles,

•=mixed adultsandjuveniles,0=adults.Mediancatches are forcombinedadult andjuveniledata...

Figure3·6 . Seasonalgrowth of juvenilesand lance collected byseinefrom theBarrenIslands and Inner-KachemakBay during1996 andL997.

Plotsare derivedfrommean juvenilesizeindailycatches.Growth rates for the June to Septemberperiod in1996 and1997 respectivel y of 0.43and 0.57nunlday at theBarren Islands ,and 0.27and0.53 mm1dayatinner-KachemakBaywere observed )~~;=}

Figure3-7. Von-Benalanffy growthcurves fittedto back-calculatedlength-at-age data forChisik Island,Inner-Kachernak,and Outer-Kachemak.The growthcurve forBarren Islandssandlancerepresents observeddata due toonly2 age groups being present.... ...•••... ),;1;;;

Figure3-8. Graphicalassessment of Lee'sphenomenonusing the relationbetween back-calculatedlength atthe end ofthe firstgrowingseason(10) and ageC_:::outer-KachemakBay,...=inner-KachemakBay,

• =

ChisikIsl and) ~:~Q

AdUlo...tedlnll niU

For.

Mymother-forallher encouragement; Patricia foraworldofLoveand happiness;Dr.

lohn Piatt for hisfriendstUpand support;Mike.,Phyllis.andthe numerous residentsof Kachema1:Baywoo always had hotdrinks,hospitality,and a myriad of stories whenever wearrived.at theirbeach.

Majorfuwlcial andlo gisti csuppo rt for this projectwasprovided bytheExxonValdcz OilSpill (EVQS) TrusteeCouncil.U.S.GeologicalSurvey,andtheAla.ska Departm ent ofFlSh and Game.Igratefullyacknowledgethe assistance of Milc.e andPhyllisBalou gh fortheir dedicated helpwithobservations andcoUectionsinSeldoviaBay.Special thanksgo toDaveBlack. LillyGoodman.Arthur Kettle.,KaliMangel.AprilNielsen, Marc Romano,JennyPienon,.andStephanie ZunigaforLopghoursof hd pinthe6d d.I am alsograteful toMikeGeagd of thcUniversityofAlaska.Fairbanks (Kasitsna Bay Marine Laboratory)and TomVan Pelt (U.S .G.S.Biologi cal ResourcesDivision) for logistical help;andKathyTurcoand Nancy Tl1cstonfor supportduring analysisand writing.All sandlancewer e coUected underAlaska Departmentof Fish andGame permits.

AftertheSand lanu die&ina:

A(ylongwood-handled shovel' ssticldngjromthegravel towarclsheavenstill,

Andthere's a hucket that I didn'tfill beside it,andtheremaybe twoorthree

empty hags lay upon my bow.

ButIam donewith sand lance-diggingflOW.

Essenceofwinter sleepisonthe night, The scentofsand lance:Iamdrowsingoff.

Icannot ruh the strangenessjrommysight Igotjromstaringat a silveryfish Idugthis morningfrom the exposed earth

And heldbefore theworld ofshifting sands.

ItWiggled, and llet itf allandescape.

Butfwarwell Uponmywaytosleepbeforeitf ell,

AndIcould tell Whatfarmmy dreamingwasahouttotake.

Magnified sandIllI'ICeappearanddisappear, Headendandtail end, And everyplicae ofsilver showing clear.

Myhandnot onlyhepstheache,

It keeps the pressureof the shcwel-round.

Iconfeelthesurfswayas thetideshifts.

AndIcon hearfrom withinthe sand The squiggling sound Ofschool on schoolofsandlance digging in.

For Ihavehadtoo much ofsand /ance-digging:Iamovertired Of the great harvest thatImyselfdesired There were ten thousand thousandfish to touch,

cherish in hand,and then bag, but notlet fall Foranythat struckthe.sand, No matter ifnot not fastorslaw,

Sanksurely back into hiding.

Asifnever caught.

Onecon seewhat will trouble This sleep ofmine, whatever sleep it is.

Werehe not gone, Thebrown bear couldsaywhether it's like his

Long sleep,as 1describe it's comingon, orjust somehumansleep.

(Apologies to RobertFrost)

Clupter1

Maturation, Fecundity, and Intertid al Spawning of Pacific San d Lance in the Northe rn Gulf of Alask a.

Publishedas:

ManinD_Robardl.l0 M F.Piatt,andGeorgeA.Rose.1999.1ouma1ofFIShBiology504:

1050-1068

1.1 Abstract

We investigated seasonal maturation and spawningoCPaci6c sand lanceinKacbc:mak Bay,Alaska,betweenMay1996andOctober199 7.Nosexual dimorphismwasobserved inIengtb-at.-weight(gonad-free)orIengtlHt-age.Mostsand lancereached maturityin their secccd year.Fiddobservations andindicesof maturity,gonaddevelopmen t,and ova-size distributionallindicated that sand lance spawnedonce eachyear.Males maturedearlier in the season than females,but females (31%)attained ahigher gonadosomatic index than males(21%).Sand lance5P&wnedintertidallyinlate Septemberand October on tine gravelorsandy beachessoon after the seasonal peak in water temperatur es.Sandlance collected from elsewh ere in Cook InletandPrince WilliamSounddisplayedsimilarmaturationschedules.Schoolswere dominated2:1by males as they approached the intenidalzone atasitewhere spawni ng hastaken placefo r decades.Sand lance spawned vigorouslyindensefonnations, leaving scouredpitsin beachsediments.Fecundityof fema.les (sizerange:93-199mm)wasproporti onal to length,ranging from l,468to16,081 ovaperfemale.Abouthalfoftheoverallspawning schoo1fecunditywasderivedfrom ago-group-I femalesandlance,whichmade upSS% ofthcschoolbynumber.Spawned. eggswen: 1.02±0.08mmindiameter,demersal, slightlyadhesive, and depositedinthe intertidaljustbelowthe watertine_Sandlance emb[)'OSdevelopedover 67 daysthrough periodsof intertidal exposure and sub-freezing airtemperatures

SandIaocc (gc:oosAmmodytu)arezooplanktivorous.semi-demersaJ.sclKloling perciforms, ubiquitousinbarco-arcticregionsofthe North AtlanticandNorth Pacific oceans.Seven]speciesofAmmodyruhavebeende5cribed.butonlyA.he:raptntlS is IcDowntooccurinthe northeastern Pacific.A.hnoptentS dominates nearshoreGulfof Alaskaand Bering Sea fish communitiesand comprisesthe principal forage fishfoc many marinebird s and mammals(Blackburn and Anderson, 1997;Pian and Anderson, 1996;Springer,199 1).Despitetheirimpo rtanceinthe marine ecosystem, littleisknown about the annuallife cycleof P aci6 csand lance.

San d lanceare closelylinkedwithspecific benthi chabitats,alternatelylyingburiedinthe sub.stnl1e andswimmingpelagically in well-fonnedschools.Hence;nearshore aggregations are typically usociat ed withfinegravel and sandy substratesup toand includingthe intertidal zone(O'Connell and FIVeS,1995).Sandlanceare highly selective intheir useof bwrowing habitat(e.g.,Pintoetal., 1984),but spawning habitat andsubstratesremainundes a ibed.We are awareofno year-roundstudies of matutation phenologyforA.he:xoptenu.Mostestimates of spawning phenologyare basedOD.back- calculation from theoccarreeceof early-stagelarvae(Field,1988).larvalsurveys cond ucted aroundKodiakIsland (Alaska) suggested thatsandlancespa wnFeb ruary- March(Rogersetal.,1979;KendaUetal., 1980).McGurk andWarburton(1992) calculated thatA.hexapterusin thePortMoller estuary (Alaska Peninsula) spawned betweenmid-Janu ary andlate April.CaptiveA.hexapt erus collect edfromthe Strait of

1-3

Juande Fuca (Washington)alsoindicatedlate winter(March)sp«wnin g (Pinto,1984).In contrast:,theonlydirect observations of sp«wningconditionA.huopterw:were made off Kodiak Island(Did:andWarner,198 2)aDdCookInlet(Blac kburn andAnderson,1997) duringAugust to October.

Toaddressthis lack. ofinfonnationonPacificsandlancereprodudivebiology,we initiateda year-roundstudyin KachemakB ay,CooklnIet:(Fig.1-1).Localresiden ts indicated thatspawnin g sandlancehadusedsome beachesinthisareafordecades.In thispaper- weprovidethefirst estimates of maturationphenologyandfecu ndityfor Pacifi csand lancebasedonyear- ro und observations,and describethespawningbehavior ofthis species incoast al waters.

1.3 Materials and Mltlbods

KachemakBay(Fig.1-1)isnearthesoulhemtipofthe KenaiPeninsulainAlaska (S9.617N,IS I.4SOW).Thebayisabout 38Ianwide alitsentrancefromCook Inletand 62 kmlo ng.Mo st ofthc bayisrdmvdyshallow,ranging fromaboul3S10 90 m, with deeperdcp'.hsonthesoulhem side.Mo stwater enteringthebay originatesfromtheGulf ofAlaska,passingnonhof theBarrenIslands (Bwbank,1977).

Sand lancewere collectedaImanybeachesthroughout Kachemak.Bay.butspawningwas observed onlyalonesiteinSeldo viaBay(Raby'sspit;S9.413N,IS1.7J 8W)at the southernentrance to Kachemak Bay.Wealsocollect edadultsandlanceduringsu mmer

GULF OF ALASKA IOOkm

~ - ^,,;<

Port '. '0 - .

~- MoUe·

_ .. _•• • • 0.

Figure1-1:Location orsand lance collections withinCook Inlet and Prince William Sound (PWS). SpalWing occurred atRabY~$spit(net visibleat thisscale),located on the west side ofSc::ldovia Bay.

atCbislk Island(60.l 42N,152.S96W)and fromEleanor Islandincentral Prince William Sound(60.533N,147.600W;Figl-I).Wates-temperaturesweremeasuredat 10 minute intervalswithtempenture loggers (OpticStowA wayvenion2.02,Onset Computer Corpontion) placedat 3m depthbeowlowWales-(0m) onthe southside ofKachemalc.

B~y~tplacement) and at Raby'sSpit (only during spawning/incubationperiod of1996).Airtemperatures were collectedinHomer by the AWb ClimateCenter.

Fish werecoUected primarily withbeachseines orbydigginginintertidalsubstrates.

Knotlessseinenetswere44m longandhad4m deep ,3nun nylon stretch mesh(sm) in themiddle 15.3m,taperingto 2.3m deep with 13mmsmwings.Thenetwasset paralleltoshoreatadistance of 25mas described byCailletet af.(1986). Sampleswere collected abouteverytwoweeks fromMay toSeptemberandoncepermonththrough the winter during 1996and 1997.Spawningschoolswere caught bysettingthebeachseine tangentto thebeachand dosing theopenend whensandlance swam into the net.About once amonth,sandlancewerecollectedbydiggin ginexposedinlertidalsubstrates dwingDCgaUve tides.NosamplCSllr"C:TCcollectedinJanuary.

Approximat d y 150,000sandlancewer ecaughtinKacbemak:Bayduring 1996 and 1997, butonly 19,000 ofthesewere adults.Asubsampleof3.189adultswasanalyzedforag e andsexualstatus.Noadults were caught inseinesduringwinter (NovembertoMarch);

these fishbeingfou ndonly inintertidal sediments.Subsamp ledsandlancewere immediatelymeasured (fork length innun),blotted dry,weighed(±O.Ol g), individually

,-6

bagged, andfrozen.Gonads wereexcised frompartiallythawedindividualsto prevent rupturing, particularlyin laterdevelopmentalstages.Gonadswereidentified asovaries or testes using a dissecting microscope,weighed (:±.O.OOlg),and funher classified as stage 0- inunaturc,stage 1- resting (based onNelsonand Ross,1991),or stage II·developing, stageill-ripe,stage IV· running,stage V-spent,andstageVI- recovering (based on Macer,1966).

Fecundity was calculated using stratified (by 5 nun size classes from 90to 200 mm) samplesof stage-Il ovaries(n'"51)collected inAugustand September.Ovaries were removedandpreserved (hardened)in 5%fonnalin.Before counting,ovaries were placedinsmalltubes and vigorouslyshakenwithboilingwater to free eggs from ovarian tissue.AUeggs frombothovaries werecountedindividuallyon a partitionedpetri-dish under a dissecting microscope.Wealso collected samplesof ISO eggsfrom ripe (stage- III) females(n""30).Spawnedeggs were collectedfrom a spawning pit on Raby'sSpit (10/12196;n"(00),and on subseq uentvisits tothe spawningsite (10/24/96,11125/96, and1219196;n""78).These were kept moistinseawatertoprevent desiccationand analyzed immediately.Eggs were measured usinganocular micrometerat40"

magnification.Embryodevelopm entinspawned eggswas classified into six stages as described by Smigielskietal .(1984).

Weageda sub-sample(n=2,800)ohand lance collectedinKachemak Bay andallfish fromChisikIslandandPrinceWilliamSound. Sagitalotolithswere removed from the

1-7

saculus after making a transverseincisionbehind theskull.Fibrous material was removed fromotoliths; theywerethen cleared and bonded to microscopeslides using crystalbondthennal resin.Wedeterminedageson two separate occasions usingthe methodology ofMacer (1966) and Scott (1973).Otolithswith poorlydefined annuli that could not beconfinned using the secondoto lith.orwhere readings were inconsistent wereomitt ed from the dataset(n=4).Age designa tionsare based on aI Januaryhatch date withfirstyearfish designated as ae:e-Oandsecondyea.r6s hasage 1,uptoseventh yea.r 6 shas ag e-6.

About3kgof substrate containin gspawn ed eggs was collect ed from eachofthree spawn sites on Raby' sSpit. Sam p les wer edriedat65°C to constant mass.Each sample was sieved through16mm, 8mm,4mm,2nun, 1mm,0.5mm,0.2 5nun.0.125mm,and 0.06 3nunsieves.Percent mass of substtate retained byeach sievewascalculated.

Particlesizeswereclassifiedaccordingto theWentworth scalein phi (41) units,where4J= .IOBl diameter(mm).Median particle diameter corres po nds tothe50%markonthe cumulative curve usinga probabilitytransformedY-axis(Brownand McLachlan,1990).

A modifiedgonad osomaticindex (GSI)was used to quantifysexualmaturityon individual s of stage I - VI.All immature(stage-O) fish wereemittedfrom thisanalysis.

The GSIwascalculated as:GSI=(gonad weight/ gonad-freebody weight)" 100 (Nlkolsky, 1963 ).

To compare thelengthfweight relationshipsbetween sexes.wetested focdifferencesin sIopcaDdy..mt erceptof finearregrasiomusingthe Chowtest(Salvanes andSlocld ey.

1996).Mann-Whitneyranksumtestswerewedtoevalua tedifferencesbetweenlength at age

roc

thedifferent SCll:CSand between differentgroups ofGSIvalues.A chi-square (xl) testwasusedtoassess deviationfroma50:50 sex ratio.

1.4 Results PlrysicolEnvironment:

Seasurface tem peratures(SST)inKachemak Baydurin g1996increased steadily from lessthan ZOCinMarc h,plateauedat about11°CinAugust,and thenafter a mid- Septemberpeakof IZ"C.declinedsteadily toabout zoeinJanuary199 1.Temperatures in1997followed asimilarpatternwitha slightly highef"peak tem peratureofaboutIl"C in August (Fig.1·2).Wedidnotobserve any difference between SST'sinKachemak Bayandthose at the spawni ngsiteinSeldoviaBay.

Air temperaturessteadily increased fromalowinJanuuy.and byAprilweregenerally abovefreezing.AirtempentureswereusuallyhighestinAugust,anddeclined~d1y duringSeptember" (Fig.1-2).BeginninginOctober".sub-freezingtem pcntures were commonandduringmost ofNovemba"and December.temperaturesneverroseabove freezin g.

3 0 ,-- - - - - - - - -- - ,

20 10

~'10

i

^·20

r~~~~~~~~~~~~~~_1

~

¹²

~ 10

8 , ... .··· · ,r ··· ··· ·~

6

IFMAMJJASO NDJFMAM I JASOND Date

Figure 1-2:Seasonalvariationinmaximum and minimum air temperaturesandsea surface temperatures(SSTs) at KachemakBayin1996 and1997. Diamonds onSST plotsindicate onsetofsandlance spawning.

ReproductiveCbaraaerim cs:

Male and femalelen gths-at-a g e (Fig.1-3)did notdiffer significantlyforany age prior to gonadal development (Maynuoe),during sexualmaturati on (July/August).or at spawning (September/October;Mann-Whitneyrank sum[est; allP>O.OS) . Chow tests indicatedno significant differences between maleand female length/somaticweight relationshipsduring pre-gonaddevelopment,gonad development,orat spawning stages (Fig1-4;p....0.851,P>O.05;p.=0.000. P>O.05; F*...0.067 .1'>0.05respectively) .

No age0fish(n'"419) showedsigns ofdevelo ping gonads,although11 fish(3%) had passed fromthe stage-O to stage-r phase in October.Gonadsofsome of the age-l through-4fish did notappear to develop andremained at the immature,stage-aphase (19 %of 1310.3%of697.0.3%of287,2%of 62 respectively) .The smallestripe male and femalefish were age-I(88 mm and 113mm,respectively).Theoldest maturing fish wereamale and female ofage-6(16 3mmand 173mm.respective ly).InSeptember, mo st age-lsand lance were develo pingorripe (72%.n=234). and the proportion increased duringspawnin g inOctober(97 %.n=230).Someof these fish (15%)were also spent.

Theseresultsindicate that sand lance mature atanage of about21 months.Age-l(50%) and ege-z (31 %) sand lance dominated spawning schools.Ages-3,-4,-5.and-6 made up 14%. 4 %.1%. and<1%. respectively, of the overall school composition.

180 160

140 120 100 80

E

¹⁶⁰

S

¹⁴⁰

~

120

.!l

₁₀₀

80 160 140 120 100 80

MaylJun e

It H

H

^4/6

H

¹⁰¹¹⁷

55/44

54/"

t !

^{I08ll 0 l}

'11K) 129 140 lSI 163

July/August

P ^.

H

¹

H ^It

H

^{1021105 32158 m 3/6}

3381302

1361 "61

113 14> 1>1 (l73)

September/October

t

f ! ., .

1/3 1

If Jl

^{4 L 1416}

238/224

124 142 l>2 (lSI 1631 163

3 4

AgeGroup

Figure1-3:Lengths-at-agc (±lsd) ofadultmale (A)andfemale(_) sand lancecollected beforegonad development(MayandJune),duringsexual maturation(JulyandAugust), andwhileripeandspawning(SeptemberandOctober)inKachcmakBay.Numbersarc samplessizes(MIF)and numbersin parentheses arc overallmean lengths forsexes combined.

1-11

May/June 20 10 S

Log{Wlj--5.84+(3./ 7·LogfLgj) n-4621-0.91

~20

~10

~ ^S

~

^I

July/August

Log(Wt}--5.84+(3.19•Log{ LgJ)

n-J155 1-0.96

September/October

20

t~.~

Log{Wlj--4.92+(2. 72•LogfLgj) n-8 36 1-0.93

' \<\.) Oo~

eP

~""""() ~"~~""~""~V~Oot:!>

Length(mm)

Figure1-4:Regressionplouofl ength(mm) against gonad -free bodyweight(g;LoglO transformed data)formale (A)andfemde(_)sand lance.S....d lancewer-ecollected before gonad development (Mayand June;n=2]6male.226female),during development(Julyand August;"-580male,S7Sfemale),and while ripe andspawning (September and October;n-475 male,361 female).Regression equations are forsexes combined.

FromFebruarytoMay,most sandlancewerein theresting phase.anda few fishwere stillrecoveringfromspawning(Table I- t).Gmadalrecrudescence began inJuneand July,whena smallpro portion (6-9%) offi sh displayeddevel o pingzgo nads . Gonadal dcvdopmc:n1 increased rapidly(Fig. 1-5)inAugustassea.surfacetemperalUrereached maximallevds(Fig.1-2).Spa'Mling-<:ondition gonadsdevelo peda,sSST'sdeclined fromseasonalpeaksand spawningoccurredwhen theseSST's rea c:J!ed

approxirnatdy IO°C.Gonadoso nwicindices(GSn indicated thatD1IUesdevelopedearUCI"

than females,butultimatelyattain ed a lowerindexatsp awni ng(2 1%males.31% females).GSI' sdifferedsignifi can tly among sexesinboth1996andIl99 7(Mann- Whitney rank sum tests;allP<0.01 ).Maximum GSI forindividual males and females were47%and5S%respectively.Overall GSIfOl'"malesand femal-esfrom spawning schools (fable1· 2)weresimilarin1996and 1997,withno signifi cant difference detectedforeithc:r"sexbetween years(Mann-Wbitneyranksumtests;P>O.S).

By theendofNo~,67%ofsandlancecollected(n-24)wer-einpost-spawning condition(spent. recovering,01'"resting).No fishinspawning condillionwerefoundafter- thistime(TableI- I).ADsizes of adultsandlanceweregroupedfor:analysis based on no significant relati onshipexisting between GSI andbodylengthofripefish collectedin October(Fig.1-6).

Table1·1. PercentageofA .hex.cpteruscJassifiedinto maturitystagesbymonth for fishcollectedinKachemak Bayduring 1996/1 997.Maturitystageswere I=resting,Ijed evelcping,ffi=ripe.IV-running, V-spent,VI=reco vering.

Month S= Maturity Stage ToWNo.

I II ill IV V VI

Fob Male 95 5 21

Female 75 25 12

MM Male 100 8

Female 100 8

Apr Male 92 24

Female 95 21

May Male 100 69

Female 99 81

lun Male 93 7 173

Female 93 7 160

101 Mole 91 9 210

Female 94 6 239

Aug Male 39 57 301

Female 59 41 287

Sep Male 14 45 39 167

Female 26 67 7 163

Dot Mole 1 7 44 41 310

Female 1 4 47 43 19'

Nov Male 20 27 27 27 IS

Female 11 11 22

"

⁹

Dec Male 100 1

Female 100 2

Table1-2.Meangonadoso matic index (±95%CI) for maleand femalesand lance collectedinOctoberof1996and1997fromspawningschoolsinSeldovia Bay.Numbersinparentheses are samplesizes.

Mole Female

1996 21.12±1.65 (141) 31.27±2.66 {89}

L·15

199 7 21.57±l.S9 (164) 31.81±2.09 n03}

35

30

.g

25

.5

"

²⁰

.~

~

^[5

]

10

"

0

SO

330 2'

588

0 33 16 45 [SO287

3~~ ^{I n} ~

³

JanFeb Mar Apr MayJun JulAugSep Oct Nov Dec Month

Figure1·5:Seasonalchangesin male(.)andfemale(0)gonadosomaticindices(::1:95% confidence intervals)forsandlance collectedinKachemak BaybetweenMay1996and October199 7.Numbers arcsamplesizesforeach month.

Fema le . • • - -. -. :..··..·z· ;.:~

:-- .;;.-: .

: .~_. e.

150 160 170 180 140

: ..

• • • Ie

.-:~ t: .

..:*:.. . :... :~~ : ~.' . ... ... ^{- .. -.,..}

120 130 Male

50 ,..-- - - -- - - - - - - --,

40 30

~ 20 -c ..5 10

"

.~

0

j -- - -- - - -- - j

E 50

~ ⁴⁰

.g 30

§ 20

o 10

0 '--- - - - - - - -

^--1

110

Length(mm)

Figure 1--6:Scatter plot of male(n-131)andfemale (n-91) GSI'sagainst bodylength forripe(stage-Ill) sandlance collectedduringOctober fromspawningschoolsin KachemakBayduring l996and 1997.

1- 17

Indices of manuityrevealed(Table1-3)thatfishcollect edfromEleanorandChisik Islandswerematuring at time ofcapture(JulyandAugustrespeccivdy).Buedona mean resting GSI(calculatedfromstage-Ifishc:oUectedduringApril throughJune from KachemakBay) of0.46.sand lancefrom ChisikandEleuJOl"isWKfs displayed significant gonad recrudescenceover Gsrsobservedatresting(Mann-Whitneyranksumtests;aD P<n.OI).These resultsweresimilarto those found fortheKachemak:Baypopulation (TableI-I,Fig.1-5).

Duringtherestinganddeveloping stages(Stage-Iand-II)inspringandsummer,sex ratio swere relatively even.Duringthespawni ng periodhowever.ripe andspawning malespredominat ed (Tab le 1-4).Males were the predominantsex in all ageclasses (with theexceptionof ageclass-5inwhich only 3fishwere collected) during this period.

Fecundityranged from1,4 68 to16 ,0 81 ovapel"femaleforsand lanceranging from93 to 199mmforlelength (Fig.1-7).Fecundity was significantly correlated with body length (P<JJ.O1)_Abouthalfoftheoverall spawning school fecunditywasderived from age- group-lfish.which made up 55%oftheschoolbynumber(Table1-5). AgesI·]

accounted for95%ofthe totalfecundity.Ova diameterexhJbitedaunimodal distributionineach of the 30 females investigated,andoverall (Fig.1- 8).Eachegg typicallycontained asinglebrightyellowoil g1obu.le

e m

2 femalesabou t 5%ofova containedtwooilglobules).

Table1-3.MaturationstatusofA.hexaplenaAttwocoUcctionareasin

Location Oues CoUected S~ n Stage GSI(:t95%CI)

ChisikIsland August1996197 M 22 t.m 4.69 ±1.60

F 23 I-II 2.8 1±O.76 Overan 45 I-m 3.64±1.06

Eleanor Island July1997 M 18 I-II 5.81±1.32

F 24 I-II 3.11±O .53 Overall 42 I-II 4.27±O.7S

Table 1-4.Sexratios ofsand lance collectedinKachemakBayAtdifferent maturitystagesduring 1996and1997.

S.... MAla FomoIes n X' ^P

0 13 1.0 350 6.6 NS

I 1.0 1.1 1319 5.5 NS

II 1.1 1.0 563 2.7 NS

m

2.1 1.0 321 38.4 P<O.OO I

IV 1.6 1.0 218 11.5 P<O.OOI

V 1.9 1.0 3S 3.5 NS

VI 1.0 1.5 20 0.8 NS

Table1-5.Percentcontributio n totheoverallspawningschoolfecundity derived from femaJes ofthedifferentage groupspresentin October1996and

1997 (1'F"16S).

AgeGroup %To tal Fish

o

55 26 IS 3 I

1-19

%TotaIFe:omdity

o

48 28 19 4 1

20000 15000

~ 10000

~

...

. € ⁵⁰⁰⁰ ..

"0

c 4000

:::l

3000

o ...

~

2000 ,

. ^.. - .. _.

.. ^\ .

... r' ~O .86

So "00 "" 0 "<'0

".1

0 " "'0 "$0 "6'0 ">o"6'o"si'oo Length(mm)

Figure1-7:Regressionoffecundity onbodylength (mm; 10gI otransfonned data)forpre- spawning [stage-If)femalesand lance collected from Kachemak: Bay(n'"51,

r' ...-

0.86, P<0.01;I0810fecun dity"'--2.54+(2.99.I0 81OIength ).

1·20

WOO

800

E;-

600

5 "

^0-

J: ⁴⁰⁰

200

0

0.6 0.8 1.0 1.2

1.4

Egg Dlameter (mm)

Figure1-8;Size distributionofeggs"oundinovaries of30ripe female sandlance collectedfromspawningschoolsinlC:achemakBayduring 1996 and 1997 (n=4500, mean=1.01rom,SO

=

0.08mm).

SpawningHabitat and nming:

SpawningoccurredinIIshallow open bay on thesouthern,. sheltCl'Cdside of Raby'sspit, within 100m. ofroutindyused sand lance burrowinghabitat..Localresidentsindicated thatsandlance(JocaJname:"need.Iefishjhad spawnedatthis site duringthe monthof Octoberrocatleastthepast20yean.Nospawningwasobservedon theouterexposed sideof tile spit in 1996 or199 7.Thesubstrateofthespa wnin g area. consistedofcoane sand andgravel(Fig.1.9)of whichabout20%wushell fragments.

During 1996, sandlance werefirstobservedspawning at18;45on 30 September (1.5 hoursafterhightide,3daysafter spring tides,and3days prio r tothenextneaptide) whe n SST! wer e 9.4° C.Initially.weobservedlater ally compressedschools(about1-8m in lengthand up to Im across) of adultsandlanccathightidemoving back and fonh alongthelengthofthebeach.within 5mofshore.,andinlessthanIm of water.

Spawning was preceded immcdiatdybysand lance moving bade and forth along a20m stret chofbeach(whCf"eaUspawnin gwasobserved);thenthe school movedtothe tide lineandcompressedinto atight spherical formationjust abovethe botto m(withthefish movingrapidlywithinthis fonnation).Miltwuobserved in the watersoonafterthe schooladopted this formation. Sand lance wereagainobservedsp&wning at18:25 (0.5h afterhightide)on1OCtober,at 18:30(2.5h afterlow tide [neap})on 5 OCtober,and at 08:20 (2.5hbeforehightide)on6 October.Demersal eggswerefound intertidallyin shallo w

«

50 rom)dep ressi o ns ("pits")up to OAmindiameterfrom about2-5 m above the lowtideline.Thepitswere fanned at thetimeofspawni ngbysand lance asthey

100

~ ⁸⁰ ::E

#. ⁶⁰

"

> 40

.~

:;

E 20

U::J

0

Mud

-5

-4

-3

-2 -I 0

1

4

Phi Units

Figure1-9:Graphicalrepresentationofsandlancespawning substrateinSeldoviaBay (medianparticlediameter-1.9nun).Phiuniu--IOibparticlediameter(nun).

1-2)

schooled near thebonom.Sandlance(Xlnt!ooedto spawnintheseshallo ws.andnewpits containingeggswer-eobservedthrough12 November (spring tide).Duringmominglow tideswe periodicallyfound egg-filledpitsthathadnot been noted the previousevening.

indicatingthatsand lance alsospawnatnight.

We first observedspawnin gin1997duringtheneap tideseries on 8Octoberat16:00 (2.5hafterlow tide)whe nSSTswereabout1O.O"C.Spawning was observedagainon9 Octoberfrom17:00to20;00(mid- floodtide) ,10 October at 08:30(1.5hbeforehigh tide),andIIOctober at09;00(hightide).Highwindsandsnow prevented observations afterthis,although no spawni ngpitswere observedonanysubsequ entlow tide s.After spawning, adult sandlance were notobserved swimminginthenearsh or eand theywere notcaught in beach seinesuntilthe following spring.

Sandlanceeggs are cryptic and blendinwellwithsmallfragmentsof shellandgravel This prevented us frommalcinganacaJnteassessmentofeggdistnbutionover-the entire beach.Eggs wereobservedon the sandsurfaceof spawning pits at•density of up to7 cm-2and within the substrateto adepthof about30RUn.Eggs weredeme:rsaJ.slightly adhesive, translucent,and almostsphericalin shape (mean diameter 1.02mm,SO-0.08 rom,n-100).Someeggs were adhered tosandgrains oreachother,butmanyothers were foundindividually and unattachedwithin thegravel.

Stage 1 eggs(<2dold;SmigielskietaI.,1984) were collectedon12October, 1996 from

a freshJ.yfonned spawning pit.Anincomplete blastodennalcap characterizedthese eggs.

Yolk cloudinesswas not observed at this orsubsequ ent stages.Atthesamepit on24 October,eggs wereat stage 3 andnoblastodennal capwas evide nt.By 25 November, egg density at this pit had declineddramatically,andonly nine eggs wereobserved.Only one of these nine eggs was adheredto the lightly frozen gravelparticles.Each of thenine eggs containeda stage 5 embryo between 3.75and3.8mm inlength.Eyes were pigmented (0.18nun diameter), myomeres were visiblealongmost of the embryo's length,abeating heart was observed,andadeveloping alimentarycanalwas visible.On 9Decembera final sampleof 3 eggswas foundatthisspawning pit.Allthreeeggs contained a stage6embryo which exhibitedconvulsivemovementsat frequent interval s (every10- 15 seconds). Assuming the eggs from this spawning pitwereaUpart of the 12 October spawning, development over the observ ed58days (until 9 December,when stage-S embryos were observed) occurred inanaverage sea and air temperatureof 6.4"C and -2.5"C,respectively.

1.5 Discussion

Second year spawningis commonamongotherspecies of sand lance,occurring inA.

personatus(Kitaguchi,1979),A.americanus(Richards,1982), andA.tobtama (O'Connelland Fives, 1995).Incontrast,A.dubius (Scott, 1968;Winters,1983) andA.

marirrus(Reay,1970 ) can matureas second-yearfish,butoften mature atlat er ages.In our study,onlya single age-group-O fish (immature)was observed within thespawning schools,altho ughexclusive lyege-o schoo lswere caughtelsew hereinthebay atthe same

1_2 5

time.The maximumlife-span forA.hexaptenuwas7years,whichisalsothe upper age fOUDdforA.tob ianus (O'ConnellandFives.,1995).Forfishpopulations such as those studiedhere.whereina single cohortatege-Icontributes SO%of the population fecundity, any large variations inreauitment are,intum,Iikdy to have large and immediateeffectsonpopulationsize.

Gonadaldc:vd op mentwas initiallyslowanddifferedbetweenthe sexes.Nosc:xuaI dimorphismwas observedfor maturesandlance,eitherintheirlength -to-weight ratios01"

length-at-agerelati on ship.Wecan therefore attributegenderdifferencesinthe GSI to variable ratesofgonadaldevelopmentindependentof differen cesinbodysize between sexes.Gonadsmaturated rapidly in August asadultsandlan celeavethe nearshore zone (Robardsetai,unpubl.dat a).During AugustandSeptember,meanGSIsformalesarc higher,indicating thatmales mature morequicklyandearlier duringthe reprod uctive season.InitialmaturationinA.cbIbilaisalsoquiteslow(Winters.,1983),andA.cbIbillS (Nelson andRoss, 1991),A.tobianus(O'ConncUandFlVC5,1995),A. marimlS(Reay, 1970),and A.personatus (Okamoto etaI,1989)alldisplaydifferential rates of maturationbetween malesand females.While testes ofA.haoptervspeakedin development earlier,ovaries eventually attainedagreater rdative weight.Gonad maturati on timeCor A.hcxaptc11lSwas comparabletothat found forfall-spawning Atlanticsandlance(ca.3 month s).Incontrast, wint er.and spring-spa wningAtlantic sand lance require from5-7mo nths10reach maturity(Rea y,1970).

1·26

Our data (maturitystages,GSI)indicatethatA.hexaplerusspawnsonly onceperyearin latefall Thepresenceof afewrecovering fishas lateas May(TableI-I) indicatesthat some iDdividuals mayspawnlat~ in the wint~(asinA.dIIhnu-.Wmte:n, 1983).

However.wefoundno evidencefOl"differentspawningJI'OUPSwithinthepopulation,.Le., onethatalso spawns during thespring (asinA.tohianus; O'Connelland Fives,1995).A.

JrexapterusfromChisikIslandand Prince Wtlliam Sound (PWS)alsoappearto spawn during the&11.

Sandlance(A.hexapterus) spawnedinKachemak Bayduring a 1-3 week periodin Octoberof1996 and1997.Inthenorthwest Atlantic,A.dubiusand A.amertcama spawn over a periodofabout 3 monthsin late fall and earlywinter (Winters,1989).InIapanA.

personam lspawnsovera1.5monthperiod(Okamoto eta/.•1989).Althoughour observationsindicate a sboner window of spawningwithin KachemakBay.spawning may occur over alongerperiodthroughouttheentireGulfofAlasIcaregion.

Malesand.lanceOUtrlUmbered females byabout2:I in the nearshore zoneduring spawning. butnot duringearlier stages of development.nushasalsobeenobserved for A.nrarimu(Macer ,1966;GauJd and Hutcheon,.1990).A higher ratioofmalesat spawning mayindicate thattheyremaininthe spawning areaovera longerperiod [similactocape1in(Mallotus villosus;Templeman, 1948)].Meanwhile,slower - developingfemalesthat are notfully mature probablyremain buriedinsedimentsuntil ready to spawn.

We found aunimodalsizedistnbutionofovainthe develop ing ovariesof Pacific sand lance.Unimodalsize distributionsolovainA.hexaptUin (Pinto.19&4).A.dMbius (Sco tt, 1972a),andA.MOri/fUS(Macer, 1966)atesuggestiveofsingle-batcb,onceyearly spawninginthesespecies.Egg diametersforA.hexapu11ISinKachcmaJc.Bay were comparablewith other observations fOl"thisspecies[e.g.,about 1mmfor Murmansand lance(Andriyashev,19 54 ) andameanoflnunforsandlance in thePacific Northwest (Pinto ,1984;Penttila, 1995)]. Williamseta!(1964)and Pinto(1984) bothobservedthat eggs containedone oilglobul e.How ev er,we occasionallyobservedmultiple oil globules,which does occurinfrequentlyinthisgenus (Garrison and Miller.1982).

Fecundity ofA.hexapterusfrom Kachcmak Bayranged from 1500-1 6,000 ova.This is similar to fecundity observedinmo stother sandlancespeciesand popula tions:Japanese A.hexapte11lS(Hashimoto.19 84);A.americanus(WestHutaL,1979);A.marlnus (MaceI",1966);andA.robianra(O'ConnellandFives.1995).However,Nelson(1990 ) reportedlowes-values forA.dIIbiusand Hashimoto (1984) greater values forA.

per"""""-<

Pits formedinthe substRteduringspawning probablyresult from females boringthrou gh loo segravel,and whilstdoing sodischargingeggsintothe surroundingmedium as reportedforA.tobianu s (McIntos h and Mastcnnan,1897).We observed nosignifican t dumping (Smigielskiet01.,1984)or cloudiness(pinto.L9 84) ofspawn ed sandlance eggs as reported inlabo ratorystud ies. Althoughslightly adhesive,theeggs did not

appear to remain on thebeachin large numbersover the course ofincubation.Perhaps looseadherence togravelover timeallows eggstobe dispersedbytidal actionboth interstitiallyandwithinthewatercolumn.Adherenceof eggsto gravel and fine substrateswould help preventdesiccationwhen they areexposedto air at low tides.

Theegg developmenttime demonstrated inthis study islonge rthan totalincubation timesreported forotherspeciesof sand lanceatsimilarwater temperature s.Smigielski etal.(1984)and Inoueet01.(1967) reported maturati ontimes of39 days at -roC forA.

americanus,and33daysat6.2°C forA.personat es, respectively.Judgingfroma mid- stage 6development,Kachemak Baysandlance were at 88%development on9 December; suggestinga67day total incubationperiod.Thus,hatchingshouldhave occurredon or around December 17.Ourtotal incubationtimesweresimilar tothe 62 daysincubationperiod reported forA.americanus eggsat2°C(Smigielskiet al.,1984) Wesuspectthatthe longincubationperiod observedinKachemakBayresu lts from exposureofeggstoverycold air temperaturesduring theapproximately 12 hour sof intertidalexposure each day(Fig.1-2).McGurk and Warburton(199 2)reponed comparable resultsforA.hexapterusinthePort MoUerestu aryon theAlaskan Peninsula (45-94 days ofincubation with a hatching period of41-63days).

Thelocation of depo sited eggs within the intertidal hasasubstantialinfluenceon developmentand survival rates.Similar to Taylor (1984 )wefound thatA.hexapterus eggsdeposited in the intertidal developed slowerthan for other sandlance speciesthat

1-29

layegg s immersed in the sub-tidal.Increasedeggsurvival inthe intertidal comparedto the subtidalhas been attributedtolower temperaturesfor surf smelt(Hypomesus preliosus;Loosaneff 1937),and to increasedoxygenationforPacific herring(Clupea paiJasi:Jones, 1972).

During the spawningperiod,sandlanceappeared tospawn with littleregard fortidal stage or time of day.Howeve r,spawning may occur morefrequently at high tideas evidenced bythehighposition of spawning pits onthebeach.Penttila(1995) observed a similar vertical spreadofintertidalspawningpits,i.e.,withina fewmeters of thehigh water line witheggdepositioninthe top 30nun ofgravel.

Wefound noindicationthat sandlance moveabove thehigh waterlineas described for grunions(Leuresthesspp.,Thompson,1919) and capelin (Templeman,1948). Reportsof sand lance foundabove the waterline inthe intertidalzone(e.g.,Dick: and Warner,1982) may result from sandlance beingstrandedon low angled beaches byra pidlyretreating tides.Strandingmay alsobe the resultofpredators (intentionallyor inadvertentl y) herding sand lance intothe shallow swherethey may be sweptabovewaterline bythe surf(e.g .,Beston,1928).

SpawningofA.herapterusoccurred on fine gravel and sandybeachesas istypicalof this species (penttila,199 5).Resultsofour z-yearstudyandlon g-term observationsaflocal residents suggestthatsandlance use the same sitesfor spawningyear afteryear for

decades.Penttila(199 5) alsodocum ented repeateduse ofspawning sites.Per enni aluse of me same beaches has direct implications forthe conservationof thi5 species and CO"

the predators thatrelyonsand lance. Sand lance maybe particularly vulnerable to pollutionofcoastalareasanddevelopmentof beacb- front habitats.Itwould be usefulto establish. quantitative libratyof beach substrates tohelpidentify potential spawning habitatfor thiskeyspecies.

Ourstudy did notallo wusto determine ifPaci6c sand lance are obligateintertidal spawners.Penttila (1995)collectedsubtidal samples inthe vicinity offreshintertidal sand lance spawn and didnotfind anyevidencefor coincidentsubtidalspawn depo sition.

We foundnopublishedrefer ences to offsho respawningbyA.hexapterus,unlikefor capeJinthatspawn intertidallyaswellasindee peroffsho re waten (Templeman,1948).

Theintertidalspawnin gof pelagic speciessuch ascape1inappearstobeoptional(Taylor, 1990).Our results corroboratewithReay(1970) whosuggest ed sand lance spawnwithin their oonnaI range,ratherthanmigratingtospecialspawning areas.A.tobiamLris the only other sand lance speciesknown to sp81NDintertidally(Mcintosh andMasterman, 1897).A..marimu(Reay,1970),A.ameriCXlnUS(Westinet01.,197 9) ,A..dubius (Wint ers.

1983).andA.personatus(KimuraetaL,1992)aUspa1ND subtidally in nearshore areas ancVoron shallow offsho re banks

Latefallspawningintheintert idalisunusual.Eggs andlarva e areexposed toharsh winterconditio nsleading toprol ongedincubationand hatch periods.Pelagicsand lance

1-31

larvaeappearinlate March and April (Haldononet aL,199 3),well inadvanceofthe:

spring phytoplanktonbloomorthe berbivorous copepodmaxirrwn.TIlisis unlikemany other fish larvaewhich occurI'talCh bter (May)inapproximate synchronywithmaximum zooplankt on densities(HaIdononet aL,1993).The ecological significanceofthistiming isthought.tobeadaptiveinsituations wherepreyavailabilityisunpredictab le (Haldo rson et aL,I993). However,othef"factors ofecologicalsignifi c.ancemaybeto1)utilizethe:

fullperiodof prey abundance,2)avoidinter-specificcompetitio n,and3)developata timeofl ow predatorabundance(WrightandBailey,1996).Hence,adaptationssuchas delayedandvariableeggdevelopment, larval feed ingbefo re absorptio nof yolksac (YamashitaandAoyama, 1985),reducedmetaboli sm at coldtemperatures(Haldorsonet al.,1993),and resultantred uctio n in caloricrequirements(BuckleyetaL,1984)all appear to increasethe: survivorshipand chanceof sand lance larvae being able tofully- capitalize on thespring planktonbloom.

Cbapcer1

Changes in proximate composition and somatic energy content for Pacific sand lance relative to maturity, season,

and location

Published as:

MartinD.Robards. JillA.Anthony.John F.Piatt,andGeorgeA. Rose. 1999.Journalof Expe rimen tal MarineBiologyandEcology 141:245-258.

1.1 Abstnd

Thebodyconditionand energydensity of adult Pacificsandlancecydesseasonally.

Meandry.weightenergyvalue peakedinspring andearlyIUIJUtler(20.91 kJg-¹foemales., 21.08 Idg-¹forfemales).andsubsequen tly declinedbyabout25%duringlatesummer andfall(15.91kIg-¹formales.15.74Idg-¹forfemales).Declinesinenergydensity during lateSWIUJIC£paral.leledgonadaldevelopment.Gender differencesinenergy density (males<females)were onlyapparentfrom August toOctober.Aduhsand lance spawninOctoberentering the winterwithclose totheirminimumwhole body energy content.Juvenilesand lance exhibited a relatively constantprotein tolipid ratio until they reached 80 mm fork:length.Thereaft er,relative pro portions of protein remained constantwhilelipidpropo rtionsincreasedsignificantly_Dryweight energydensitiesof juveniles increased from aminimum 16.67k:Jg-¹toamaximumof 19.68kJg-¹andare higher than aduluinlate sununer.'Thefoodvalue ofaduhsand lance to predators varies marl::edIywithin1C&SOf\S.However,maximumenergeticvaluetopredatorscoincides withimpJrtant feedingperiodsformarine manunals.,fish, and seabirds.

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Pacificsandlance(AMmodyte.shnopteru.s)arc commoninmanyneanho£e areasoftbe Gulfof Alaska and BeringSeaand arc a principle preyfOl"many marinebirds.

commen::iaIfish.and marinemammals(Field,1988;Springer.1991 ;Piatt andAnderson.

1996;Blackburn and Anderson. 1997;RobardsetaI,1999c:).Despitethe food web imponaoceof sandlanceforhigher-ttophiclevelpredators,seasonaJor geographic variability in theirnutritionalvalueis poorly known.Suchknowledge iscriticalfora better wxlc:rstandingof tto phic interactionsinthe NorthPacific environme nt.

Adultsand lancehave beenconsidered asahigh-qu alityfor ag e fish(An thonyand Roby, 1997;Van Peltetal.;1997).How ever,thevalue ofsand lance as preychanges as a functionof theirsizeand energydensi ty(kJg-1wetmass) whichis determinedprimarily bylipid content(percent dty mass;Anthony andRobr,1997).Lipidcont ent varieswith season.locati o n. gender, age. feeding rate.and ilctivitylevel(Soofiani andHawkins, 198 5;Anthonyand Roby.1997).Markedseasonal variationinlipidcont cn1bsbeen doaJrnCntedfor other forag efishincluding anAtlanticandIancc(A .marinus;lfuIopet aI,1991 ),capdin. (Ma/Ionuvdlosus:Iangaard. 1974 ),herring(Clupeo harenps;Paul et a/..1998)andsevcnIfreshwatCl"species (Bryanetal.,1996).Seasonalenergystorage istypicallyrelated toenvironmental. productioncycles(Dygert, 1990 ),as a consequence ofintcnsefeedingdurin g secondary production bloo ms.Withsand lance, however,these cycles ofenergy storagemay be outofphaseandlead physiological processes such as

spawnin g,whichoccursabout fourmonths afterthestrongspringprimary productio n bloom(Damkaer.1977;Dick.andWat'rI«.1982).

Inthis paper weexamineenergystonge in relationtosexual development andwinter dormancyof adults.,plus energeticch&JJgesduringdevelopment in juveniles.

1.3 Metbods

Sand lancewere sampledfromKachemak Bay in LowerCookInlet,Alaska(Fig.2-1) wherewe were concurre ntlystudying breedingseabirds.We collectedsand lance from int erti dal substrates(byrandomdigging at known habitat beache s on extreme low tides) andbybeachseine (Robardseta!.•1999 c).Adultsandlance werecollect edinFebruary , and then monthlyfrom June toNovemberinKachemak Bay.Weconfirmedadults collected in October were in pre-spawningconditionby the appearance of gonads and fieldobservations.

Sand lance were measured (forlc.length,nun),blotted dry.weighed(:t:O_OIg).

individually bagged, and frozen.Gonads wereeJl;ciscdfrompa.rtiaIIy-thawcdindividuals toprevent rupture.Ovaries and testes were identified using a dissecting microscopeand weighed(±O.OOIg).Gonadswer e retainedwiththerestof thebodyforproximate analysis.

Figure2-1. Locationof Kachemak BayandLower CookInlet.Alaska.

2 -'

SagittalotolithswerecoUectedventnllytothe spinal columnand anterior110 atnnsver5e incisionmadeattheskull'sposteriormarginofebe5IcuU(visible throughthte skin) Otolithswere cleaned of fibrous tissue, and stored dryinEpindorftubcs

ro..

later analysis.

Theleftotolithwasmountedonamia-oscape slideinthesagittal planeusimg CrystalBondthenna!resin.Age determinations were basedon the otolith illl.terpTetations ofMacer(1966)andScott(1973 ).BasedonJanuaryIhatchdate(Dick.lUI'Id Warner, 1982),firstyear sand lanceweredesignated asagegrou~,second-yearsand lance as age grou p-I,uptotheseventh-year asage group--6.These agegroupswer-edividedinto juveniles (group-O; sexuallyinvna tur e) and adults (groups 1-6 ; sexually matlUre;Robards etal.,1999a).

Adult sandlancewere processedindividually for proximatecomposition,wthereas juveniles wereanalyzedinbatchesof10(5 nun size classes )becauseoftheiirsmallsize.

Two replicates were made foreachsizeclass Sandlancewere dried at 60-'Cto constant mass and reweighed todetermine watercceteet.Lipidcontent of dry sampaes was determined by solvent ecrecccnusingasoxhletapparatusand asolvent systemof7:2 hc:xaneflSOprOpyialcohol (Radin.198 1).Lean dry sampleswereashed inatmufll c furnaceto determine ash-freelean dry mass (AFlDM>.AFLDMis94%peceein (Montevec:chi.t!lal,1984 ),andhereaft er referred to aspro tein.Energydecsity (kIgoldry mass) and energy contcnt (kJ/fish)were calculatedfrom proximat c composbtion(water, lipid,ash-free leandrymett er.andash),using published cnergy equivale nts t(lipid-39.3 kJg",protein=17.8kJg·¹;Schmidt-Nielse n, 199 7).Inresponsetofrequenucalls Cor

standardization of results (e.g.,Montevecc hiandPiatt,1984;Hislopet a!,1991;Van PdtetaI,1997)wereport re:suhsaskJ'g.1drymass.Alldrymass:wet mass relationships passedthrough the origin.Wemodeslopeparameters toallowcalcuJation ofkJ'g-1 wetmassin Tablez-L

Stage N

?

Slope

Table2..1.Regressionparameters forthe fresh wetweight-dry weight relationshipofadultand juvenilesandlancecollectedinLowerCook Inlet dwins 1996.

Adult 243 0.87 0.25 Juvenile 14 0.99 0.25

Amodified monthlygonad osomaticindex (GSI;Nikolslcy,1963)wasused to quantify seasonali tyofreproduction for stages1 through6where OSI-(gonad weight/gonad- free bodyweight) xlOO.Conditionofsand lanceinrelationto wet, dry,lipid,and protein masswerecalc:ulatedusingamodified Fulton conditionfactor(K')proposedbyBagenaJ.

and Tesch (1978)whef"eK'-ma.ssxlO'/(lengtht.Weused the Studentt-testtocompare energetic valuesbetween sexes,timeperiods,andregions.

2.4 Results

&asonalVariation:

SandlancecollectedinFebruary wereemaciated withno Ioisiblefatreserves.ByJune andJuly,sandlance hadobservablemesenteric fat,whichdlen declined untilspawning when nomesentericfat was observed.Proximate compositio n analysesconfirmedthese visualobservations.Lipid content declined fromJuly throughNovember and February

(fable2-2),All expected(Van PehetaL,1997)cner-gydensity(kJg' I),was invencly correlatedwithwater- conten t(water-content-59.9-(0.54xto tal enet'gydensityJ,~ 0.8 1,P<O.OI,n-267).

Energy densitiesfur individualadults I'Dlged fromahighof22.79kIg' ldry massinJune toalowof14.23 Ug-'drymassinFebruary.Mean energy densities declinedbyabout 25%from apeakinJuiy (20.91Ug-^Imales.,21.08kIg^lfemales)throughtoNovem ber , withlo westvaluesobservedinFeb nwy(IS.91 Iclg"1males,15.74kJg"fem ales ).

Energydensitydeclinedsignificantly(P<O.OOI),13.1%forfemalesand 16.4%for malesbetween JulyandOctober,asgonadal development(GSI)increased (Fig.2. 2),in preparationforspawning.Energyden sitiesforfemalesweresigni fican tly(P<O.OOI) high erthanformalesinAugust,September,andOctober.Energy densi ties were further reducedby8_6%infemal esand 4.7% inmalesinOctober, correspondin g totheonsetof spawning.

PooledsamplesfromJuneandJuly(no significant difference betweenmonths.sexes,or stage of develo pment;P'I>0.05)onlyexhibitedaweakpositiverelationshipbetween fishlengthandenergydensity(~-0.13,slope-0.05).The percent ofwater- content remainedrelatively stablefromJune toOctoberthen declinedpreci pitouslyduring spawning fo rbothsexes(Fig.2. 3).Drymass remainedrelatively constantdurin g early summerbeforedeclininginAugu st (males) andSeptember(females).Proteinbiomass increasedslow lyduring su mmer,but declinedmarkedly toabout60%of peak levels

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Jan FebMarAprMaylun lui Aug SepOctNovDec

Month

Figure 2-2.Monthlyenergydensity (kIg-J drymass)and gonadosomaticindex (GS!) for adultmale(0)andfemale(.)sandlancecoUectedin Kachemak: Bay.Errorbars arc means:l::standarddeviation; smallcircles arerange ofdata.

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!

Wet Mass

Lipid Mass Dry Mass

Protein Mass

45r-~-~~-~~--~-~~~.-~-, 40

35 30 25 12

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7 1--~-~~-~-~~--~-'----;_~---1

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Jan Feb MarAprMay Iun Jul Aug Sep Oct Nov Dec

Month

Figure2-3.Seasonal condition factor(K') for male(-"0"')andfemale (_-) sand lance coUectedinKachemakBay.Errorbanare meaase one standard deviation. Vertical dashed line indicates time ofspawning (Robards et al 19998).

during spawning.LipidreservespeakedinJulyandgradtWJydeclined to minimallevels byNovember.Lipidcontent declined more rapidly for malesthan females.Lipid declines pan.Uded gonaddevd opment(Fig.2-2).and for bothevents.malespreceded females byaboutone month.

JuvenileSand Lance:

Energydensity cf'juvenilesandlance ranged from 16.67Idg-^lat 55-59nun to19.68 Idg-^l at 85-89 mm (Table2-3).Thelargest juvenilescoUectcdinAugustwere similarinenergy density (per g) toadult sandlance ,althoughappro,amate ly onesixththedry mass.

Juvenileenergy densitieswereinversely correlatedwithwatercontent(watercontent- 67.8-(0.64Ittotal energy density) ,1=0.92, P<O.OI ,fPI 4).Relativeenergeticcontent of sand lance between 55 and 80nunindicatedsimilarcontributio ns from lipidand protein(Fig.2-4).Relativeprot eincontentsteadily increased between55 and80 mm (Fig.2-5).furthef-growth was notassociatedwithproportio nal increasesinprot ein,but withrelativelipidcontent,whichincceased by over 100%betweenfork-lengths0£80

"'"90nun.

2.5 Disamikta

Adultsandlancedisplayaseasonalcycle ofenergyaccumulatio nwitha31%Increasein energydensity betweenFebru aryand June.Peak energyvaluesreportedhere were similar to those forAtlantic sand lance (e.g.,Hislopetai.,1991;Mirtenssone tal.,1996) The seasonal increase correspo ndstothespring planktonbloom inApril and May

~ ;i~~;~~~;;;~~;

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22-,-- - - -- - - -- - - - --,

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o

55-59 60-04 65~9 70-74 75-79 80-84 85-89

Length (mm)

Figure2-4.Totalenergydensities(kIg-ldrymass)ofjuvenilesand lance collected monthlyinKachemakBay.Twa bus are shownfoceachmonth sampled; replicates 1 and2.Relative energycontributio ns ofprotcin(black: bar) and lipid (whitebar) are shown.

35

30 8

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^5.5

~ 5.2

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5.0 U 4.7 4.5

l.0 0.5

WetMass

~

f · ^{! .. ! ..}

Dry Mass

f .

0:

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ProteinMass

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It:

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Lipid Mass !:

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!: !:

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55-59 60-64 65-Q9 70-74 75-79 80-84 85-89

Length(mm)

Figure2-5.Relationship betweensizeandcondition factor(K')forjuvenilesand lance collectedinKachetnakBay. Errorbarsare meanandrangeofthe twosamplesforeach

~.

(Larranceet al.,1977), like another Alaskanspecies,yellowfin sole(Pleuronectes asper;

PauletaI.,1993).Lipidcontent ofother sandlance species also increases rapidlyprior to summer(e.g.,A.personams,Sekiguchi, 1977;andA.martma,Hislopet aL,1991).

Energy density was not significantly related to fishlength although a weak positive relatio nship was observed(r=o.13).This appearsnormal for manymarine preyspecies where the relationshipis generallyweak(radj=0.35,or less;Lawsonet al.,1998).

Femalesand lanceexpend moreenergy than males in reproduction due to the production of eggs,whichrequires greater accumulation of reserves in the feeding season(Love, 1980).Inthe laboratory, Pinto (1984) observed significant loss of lipidprior to spawning bysandlance.Many other species (suchas cod) looseabout 30%oftheir energy during, ratherthanpriortospawning (SmitheraL,1990 ).Whereas gonad production may contributeto the summerenergeticlo ss, sand lancealso reduce their feeding, spending more time buriedas evidencedby late summerdeclines in catch-per-unit-effortand frequency-of-capture(\Vmslade1974;RobardsetaL,1999c).As noted forJap anese sand lance(A.personates:summarizedinField. 1988) adultsandlance may also competefor the same zooplanktonpreyspecies with recruiting juvenilesin thenearshore Feeding maybe further reducedduring the finalstages of maturationduetoshee r volume of gonads within the body cavity,reducingthe potential volumeoft he gut (as observed in gadids [Love, 1980J andherring[Clupeaharengus;Bradford,1993».Prior to spawning, A.hexopterusgonads wereturgidand completelyfilled the body cavity.CaptiveA.

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personatlLfsurvivedfor over two monthsunfedindicatingadult sandlance can endure Ioug fasts (InoueetaL,1967).

Greater rates oflipidlosswerenotobserved for eitherJell;atspawnin g compared tothe prior threemonths.However,protein content declined mariredly.Lipids compriseonly 20%(dry weight)of ~lanceovari es (rocher and Sargent,1984)and proteinisthe principleenergysource for gonadaldevelo pment (Love.1970).After spawning,sand 1ance enterthe winterseasoninpoor condition.Incoolertem peratu res, withoutplentiful foodsupplies (Damkaer,1977),and littlereservesfor metabolism,sandlanceremain dormantinnearshore substra tes through thewinter (Robards,pers.obs.).During winter donnancy meta bolism isreduced (Quinn and Schneider,1991) andgutevacu ationtimes aregready prolonged (Ciannelli,1997).Duringearlywinter,remaininglipidsare presumablymobilizedinresponse tothe low food availability(Love,198 0),priorto utiliutionof proteinreserves for metabolic needs(Maddockand Burton,1994).Sand 1aDceareregarded asahighproteinfish,asprot ein generally constitu tes greater thanIS

%of wetma.ss(Stansby,(976).Tbeproportionallyhighprotein cont ent maybean adaptation to lowfoodintakeperiods.Utiliutionof someofthisprotein (Maddock and Burt on,1994 ) wouldpro videan additionalbuffertocover metabolic needsduring fasting. Protein content varied seasonallybyover 14%(drymass)inadultsandlance fromKachemak Bay.

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