Ontogenic Changes in Microhabitat Distribution of Juvenile Bay Scallops, Argopecten irradians irradians (L.), in Eelgrass Beds, and Their Potential Significance to Early Recruitment

14 Pages·1993·5.9 MB·English

by  Z Garcia-Esquivel

Reference: Biol. Bull. 185: 42-55. (August, 1993)
Ontogenic Changes in Microhabitat Distribution of
Juvenile Bay Scallops, Argopecten irradians irradians
(L.), in Eelgrass Beds, and Their Potential Significance
to Early Recruitment
ZAUL GARCIA-ESQUIVEL AND V. MONICA BRICELJ1
Marine Sciences Research Center, State UniversityofNew York, Stony Brook. New York 11794-5000
Abstract. Ontogenetic changes in the vertical distribu- United States, are closely associated with seagrasses, par-
tion of a cohort of juvenile bay scallops, Argopecten ticularly during their early life history. Planktonic larvae
irradians. on eelgrass, Zostera marina, were followed ofthisspeciessettleandattachbybyssusthreads, primarily
throughout the summerand early fall in two Long Island but not exclusively to submerged vegetation such as eel-
embayments (New York, USA). Despite site-specific dif- grass, Zostera marina L.; adults occupy a wider range of
ferences in eelgrass height and density, more than 95% of habitats, including bare, sandy substrata. Thus, depen-
post-settlement scallops remained attached above the dence on vegetation and habitat restriction appear to de-
bottom until they reached ashell height ofabout 1 1 mm. crease with age and size, as has been shown for a variety
Over a 5-week period, scallops gradually relocated until, ofmarine and freshwater fish that extend their foraging
atamean sizeof31 mm, all occurred onthebottom. The grounds beyond areaswith plant coveroncethey achieve
decline in percent attachment coincided with a 5-fold in- sizerefuge from predators(Ebelingand Laur, 1985; Wer-
crease (from 16 to 84 ^moles min ' g muscle dry wt~') ner and Hall. 1988).
in the activity ofoctopine dehydrogenase (proposed here In common with otherpectinidssuch astheseascallop,
as an index ofthe scallops' capacity for burst swimming Placopecten magellanicus, bayscallopscan attach byssally
activity), and in maximum rate of increase in the shell throughout life, but seldom dosoasadults(Belding, 1910;
aspect ratio. While attached to eelgrass, scallops were Stanley, 1970). Attachment ofjuveniles is reversible and
nonuniformly distributed, with greatest concentration at dynamic, because Z. marina blades have a high turnover
mid-canopy. Followingdisturbance, they rapidly regained rate and elongate rapidly, at a rate ofupto 2-5 cm day"'
above-ground position, attaining asymptotic heights in the summer (Kemp el a/.. 1987). In pectinids, byssal
within 3-10 h. This and prior studies suggest that the attachment and swimming represent antagonistic behav-
climbing behavior of the bay scallop is an adaptive re- iors (Caddy, 1972). Ontogenetic changes in attachment
sponseto high predation pressure at small sizes. Enhanced and swimmingcapacity ofpectinids have been related to
scope foractivity (predatoravoidance) may enhance sur- morphological, hydrodynamic featuresoftheirshells,such
vival ofscallops at intermediate sizes, when they become asaspect ratio(shell lengthtoheightratio), umbonal angle,
tooheavytomaintain elevation but havenotyetattained anddegreeofauricleasymmetry(Stanley, 1970; Dadswell,
effective refuge in size. 1990). Burst swimming, which provides scallops with a
Introduction mechanism toavoid predators, isassociated withthepro-
duction ofoctopine in rapidlycontractingadductormus-
Bay scallops, Argopecten irradians. which commonly cle tissue. Thisend reaction ofanaerobic glycolysis, which
inhabit shallow, sheltered baysalongthe east coast ofthe serves an important role in replenishing NAD* and thus
Received 17 May 1992;accepted 10 May 1993. maintainingglycolytic flux during functional anaerobiosis
1 Authortowhom reprint requestsshould headdressed. in highly mobile molluscs such as scallops and cephalo-
42
MICROHABITAT OF JUVENILE BAY SCALLOPS 43
pods, iscatalyzed by octopine dehydrogcnase (ODH), an scallops in two bays in the Peconic-Gardiners estuary
enzyme functionally analogous to lactate dehydrogenase (Long Island, New York, USA) which differ in eelgrass
(LDH)(GadeandGrieshaber, 1986). Ontogeneticchanges structure; (2) to determine the rate ofrelocation and the
in the activities ofglycolytic enzymes such as LDH and height attained by individual scallops in the eelgrass can-
pyruvate kinase and their relation to swimming perfor- opy following disturbance, as well as the effect ofscallop
mance have been described in several fish species (e.g., density on theirclimbing behavior in the laboratory; and
ODH
SomeroandChildress, 1980),butchangesin activity (3) to relate distributional changes observed in the field
throughout the life cycle ofpectinids have not been pre- to the swimming performance ofscallops, as assessed in-
viously documented. directly from shell morphometrics (aspect ratio) and from
As reviewed by Brodie ct ul. (1991), prey have evolved the activity of octopine dehydrogenase in the adductor
two types of defense mechanisms to curtail predation. muscle.
The first type, predator avoidance mechanisms, involves
spatial(e.g.. Palmer. 1983; Main, 1987;Wernerand Hall, Materials and Methods
1988) or temporal (e.g.. Kitting, 1985) segregation from
Laboratorystudies
predators to minimize the probability of predator-prey
encounter. The second type, antipredator mechanisms, Juvenile scallops obtained from a local hatchery on
increases the probability ofsurvival upon encounterwith 2 Mayand 1 June 1990weremaintained inaflow-through
a predator. Antipredator mechanisms include morpho- upwellersystem atSUNY's Flax Pond Marine Laboratory
logical adaptations such as large size (Crowl, 1990), in- until readyforusein experiments. Thesewerecarriedout
creased ornamentation orthickeningoftheshell (Vermeij, in rectangular plexiglass tanks (basal area = 31.5 X 78.5
1987), distastefulness, orbehavioral responses(e.g., escape cm) provided with recirculating, filtered ( 1 to 5 /urn) sea-
response or immobility; reviewed by Main, 1987). water introduced immediately below the water surface
Bay scallops are epifaunal, incapable of complete or (see Pohle el al., 1991, for a detailed description of the
prolonged valve closure, and less protected by morpho- experimental system). Eelgrassshootsweresimulatedwith
logical defenses than other molluscswith heavier, thicker artificial mimics constructed ofbuoyant, green polypro-
shells; thus they require alternate mechanisms to reduce pylene ribbon (Synthetic FibersInc., Newton, PA)0.5 cm
their vulnerability to predators. Using tethering tech- in width, woven into plastic VEXAR mesh at a density
niques, Pohle el al. (1991) demonstrated that above- of500 shoots irT:, and buried underabout 5 cm ofclean
ground attachment to the eelgrass canopy givesjuvenile sand. Seawaterwas kept at 19 to 23C and 26 to 28 ppt
bay scallops a significant refuge from benthic predators. salinity with a cooling system and freshwater dilutions,
Yet the laboratory experiments these investigators con- respectively. White fluorescent lamps provided artificial
ducted usingartificial grasssuggestedthatthisrefuge may 12 h:12 h (lightidark) photoperiod.
be ephemeral because the ability to attach above the bot- A first set of experiments tested the effect of scallop
tom decreased markedly over a narrow range ofscallop stocking density on the overall success ofattachment to
sizes (about 10 to 20 mm). The distributional pattern of vertical substrates. Three experiments were conducted
mm
theepiphytic, above-bottom habitforjuvenileA. irradians usingscallopsaveraging9.3 inshell height(H,greatest
and the transition to the adult epibenthic habit have not distance from the umbotothe ventral margin), each with
been adequately described in the natural environmentand density treatments of300, 100 and 50 scallops per tank
areInthfeorfmoactuisonofatbhoeutprtehseenrattestautdwy.hich scallopscan regain ((1H213,S4E04=,8a.n6dm2m02 sc0a.l0l9o)p,s2m8 J2,urneesp(eHctiveSlEy)=on101.10Mmamy
anelevated positionand thetimingandsizeatwhichthey 0.05), and 1 July (H SE = 9.2 mm 0.06). Shell
lose this ability is important for several reasons. First, it height was measured fora subsample ofindividuals, and
is necessary for determining the relative profitability of scallops were then randomly distributed on the bottom
=
different elevations within the eelgrass canopy in terms of each tank (water depth 30 cm; height of eelgrass
of growth and survival. Second, it is a prerequisite for mimics = 25 cm). The number of scallops attached to
predictingthe relative vulnerabilityofscallopstopredators blade mimics and tank walls was recorded every 30 min
during early ontogeny. Third, it is an important consid- during the first 3 h, every hour during the following 3 h,
eration in rehabilitating stocks ofthis commercially ex- and at the end of24 h.
ploited species because, in several states on the east coast A second set of experiments investigated individual,
ofthe United States, rehabilitation efforts mainly involve size-specificclimbingbehavior. Individuallymarkedscal-
plantingjuveniles in suitable nursery habitat. lops were followed over time for 46-49 h. Their vertical
Thiswork hasthreeobjectives: (1)todescribetemporal/ position was recorded hourly during the first 5-6 h and
ontogenetic patterns in the vertical distribution of bay at less frequent intervals thereafter. Individuals were
44 Z. GARCIA-ESQUIVEL AND V. M. BRICELJ
20KM
10
.NO
CONNECTICUT
Hallock Bay
LONG ISLAND SOUND
Napeague Harbor
LONG ISLAND Northwest Harbor
Peconic Bays
Figure 1. Location offield study sitesineastern Long Island, New York.
identified with numbered, plastic-coated, miniature wire mimics, canopyheight = 50 mm anddensity = 500shoots
markers glued with Krazy Glue to the upper valve at m 2, and two tanks containing natural, transplanted eel-
least 1 day before running experiments. For each trial, grass, canopy height = 50 cm and density = 224 shoots
20-22 scallopsofagiven sizeclasswerereleasedintoeach irT2 (ANOVAat48h, F= 1.104,df= 2, 61, .P = 0.338).
ofthree experimental tanks (density = 89 scallops nT2)
containing eelgrass shoot mimics 50 cm in length. Three Fieldstudies
mscamllo(pSEsiz=e c0l.a0s7s)esscwaelrleoptsesotned8oanntdhe1f0oJlulnoewi,ng5.d7atmesm: 1(3S.E2 I'ertical distribution ofnaturalset. The vertical distri-
= 0.04) scallops on 1 1 and 13 June, and 7.2 mm (SE bution ofnaturally occurringjuvenile bay scallopswithin
=
0.04) scallops on 14 and 16 June. The coefficient of the Z. marina canopy was characterized throughout the
variation in scallop sizes within any given experimental summerandearly fallof1990intwobaysineastern Long
tank never exceeded 13%. A preliminary experiment Island, New York, which contrasted in eelgrass shoot
showedthat the height attained by 7-mm scallopsdid not density and canopy height: Napeague Harbor (NAPH,
differ significantly between one tank containing eelgrass 4101' N. 7203' W) and Northwest Harbor (NWH,
MICROHABITAT OF JUVENILE BAY SCALLOPS 45
41 1'N, 72 15'W) (Fig. 1). Both study sitesare shallow 97% ofthe total activity in whole scallop homogenates is
(about 1 m deep in NAPH and 2-3 m in NWH), well- found in this tissue (Baldwin and Opie, 1978).
mixed, andcharacterized bygentleslopes, sandy substrate, Powdered musclesamples(ca. 1 mg)werehomogenized
and fairly extensive eelgrass(Z. marina) beds, which sup- with ma sMonicator probe (Bronwill, Biosonik III) in 1 ml of
ported productive bay scallop populations prior to the 100 Tris-HCl buffer (pH 7.5) containing Triton
occurrence of"brown tides" in the region (Hickey, 1977; x-100 (1% v/v). Homogenates were cooled in ice/water
Eckman, 1987; Bricelj el al, 1987). They have also been (0-2C) during, and for a 30-min incubation period fol-
the target ofscallop reseeding efforts in recent years (C. lowing, sonication. Theywere then centrifuged for30 min
Smith, pers. comm.. Cornell SeaGrant Coop. Extension, at 1C and 16,000 X g. The supernatant was decanted
NY; Tettelbach and Wenczel, 1991). and assayed for ODH activity at 25 C by following
Eelgrass densities at the study sites were estimated in changes in absorbance at 340 nm due to the oxidation of
the second week ofSeptember by counting the number NADH, usinga Milton Roy Spectronic 1201 spectropho-
of shoots contained in 25-cm: quadrats randomly de- tometer equipped with a thermal cell controlled by an
ployed within the survey area. Surface watertemperatures external, recirculatingwaterbath. Activitywasdetermined
were recorded with a hand-held thermometer 0.5C). by dividing the rate ofchange in absorbance by the ex-
Although scallop settlement wasfirst observed( in NWH tinction coefficient (f340 = 6.23 mM~[ cm"1) asdescribed
in mid-July, sampling for determination ofgrowth rate, by Fersht (1985). All determinations were made in du-
vertical position, and percent attachment ofthe scallop plicate, using 50 n\ oftissue extract in a total extraction
population on eelgrass did not begin until 26 July, when volumeof1 ml,andwerecompletedwithin several hours
scallops averaged 4.5 mm in shell height and could thus of tissue preparation. The composition of the reaction
mixtureandtheconcentration ofthereactantswerethose
ab1en0drOec1a9tdoiSlbeyeprstaeammtpbNleerWdaHtbyNaAdnPidvHer.esx.tIneSnaedamecpdhlibhnaegrtbwcoeore,nntainn16uaerAdeuaguwnuetslitll arenpdomOrptMieed,to197y8i)e:ld1mmaMxismoudimummenMpzyryumveateac,t0i.vi1timesMN(BAalDdHwi,n
woiftthhienatrheeaewelagsraasbsomueta2d0o0wmw:asinsNamWplHedawnedekalbyo.uTth5e0smize2 71.00). NoLc-oanrtgriolnsinweeraendru1n0f0ornonstpreicsi-fmiacleacattievibtuyffbeerca(upsHe
in NAPH. previous studies have demonstrated that in scallops, in-
cludingA. irradians, the contribution oflactate dehydro-
At each sampling, divers collected 100 to 150juvenile NADH
genase to the oxidation of is negligible (Baldwin
scallops by swimming along set transects. Using rulers, and Opie, 1978; Grieshaber, 1978;deZwaan elal. 1980;
the divers obtained in situ measurements ( 0.5 cm) of and Chih and Ellington. 1983).
thevertical position (height ofattachment abovebottom) Relocation experiments. Experiments designed to test
of each individual on the eelgrass blade, and the total the ability ofjuvenile scallops to relocate (climb and re-
length ofthe blade. Scallops found on the bottom were attach) to eelgrass blades following dislodgement were
assigned a position of cm. The organisms were placed carried out in Northwest Harborand within sandy habitat
into numbered, perforated plastic boxes and brought to in Hallock Bay (4102' N 75 15' W; mean depth at low
shore, where their individual shell height was measured tide = 0.5 m; tidal range = 0.75 m) (Fig. 1).
with digital calipers ( 0.01 mm). Thefirstrelocation experimentwascarriedoutinNWH
Subsamples of30 to 100 scallops (depending on size) on 9 August using scallops collected from natural popu-
wtheeryewterraensipmomrteeddialtievelyinfrcoozoleenrasntdostthoereldabaotra-to7r0y,Cwhunetriel SlaEti=ons0.a1t3t)haifstseirted.eDtievremrisniconlglethcetierdi1n5d0ivsicdaulalloppsos(iHti=on8.o6n,
further analysis. These scallops were individually weighed eelgrass as described earlier. Scallops were measured at
(total wetbody weight) usingan analytical balance ( 0.1 the shore, individually numbered, and held in ambient
mg),and lyophylized. Softtissueswerethendissectedand bayseawateruntil released(withinabout 1 hofcollection).
weighed usingaCahn electrobalance ( 1 jug)oranalytical Scallops were freely broadcast on the bottom ofa previ-
balance, dependingon scallopsize. Shell height and length ously marked plotwithin theeelgrassbed, where nopred-
(greatest anteroposterior dimension) were determined atorswere present. Adivingsurveyaround and inside the
prior to dissection in order to calculate the aspect ratio. plot was carried out the followingday (24 h after release)
Octopine dehydrogenase activity. Lyophylized tissues and the vertical position ofeach recovered individual was
-70C
werestoredwithdessicantat until used forenzyme recorded.
assays. The adductor muscle of individual scallops (in- A second relocation experiment was conducted using
cluding both catch and phasic portions) wasdissected out, hatchery-reared scallops(10 mm), which weretransported
weighed, and used for determination of octopine dehy- from the Flax Pond Laboratory to Hallock Bay (1.5 h) in
drogenase(ODH. EC 1.5.1.11)activity,becausemorethan coolers containing ice packs layered with wet newspaper.
46 Z. GARCIA-ESQUIVEL AND V. M. BRICELJ
Unmarked scallops were released by divers on 28 August normalize data for differences in canopy height between
wXit2himn)awi3t0h-icnm2anareeealgartastshemeceandtoerwoafvesraangdiyngpl3o2tsc(m1 min bvearytsi,cawlasdisutsreidbuttoiotnestoffosrcadlilfofpesrefncreosmbNetWweHenatnhdeNreAlaPtHiv,e
canopy heightand 249 shoots m~2 in density. No natural using the Mann-Whitney test for two independent sam-
scallop set was observed at this site in the year of the ples.
study. The perimeter ofthe plots was delimited by a gal- Data from the relocation experiment conducted in
vanized chain (4.8 mm = 3/16 in. diam.), and plot lo- Hallock Baywereanalyzed bytheaposterioriGamesand
cation was marked with bright fluorescent subsurface Howellapproximatetest forequalityofmeans,with height
buoys(Fig. 2in Pohleetat, 1991). Three hundred scallops attained ateach samplingtimeasthedependent variable.
were released in each offour experimental plots, and the For the relocation experiment carried out in NWH, the
percent attachment and vertical position of recaptured nonparametric Wilcoxon signed-rank test for paired
scallops were recorded after 3 h (plot 1), 5 h (plot 2) and comparisons was used to test for differences in the mean
24 h (plots 3 and 4). Diver surveys covered a total area position of scallops at the time of collection and 24 h
of12 m2(a 2-m2 plot plusa 10-irr-perimeterarealocated following release.
m
1 around each plot). Plots were thus sampled destruc-
tively, rather than repeatedly over time, to avoid distur- Results
bance by divers.
Laboratory studies
Statisticalanalysis Scallop stocking density, over the range tested in this
study, had no significant effect on percent attachment to
Except where otherwise indicated, statistical analyses eelgrass mimics (P = 0.293, repeated one-way ANOVA).
followed standard procedures described by Sokal and Percent attachment averaged 80% 2 h after release and
Rohlf(1981). Percent attachmentdata obtained from the 85% by the end of24 h, irrespective ofstocking density.
three stocking density trials were pooled for each time Although scallopsswam actively duringthe first 15 min
interval and scallop density (50, 100, and 300 scallops following release into the experimental tanks, very few
per tank). Differences in arcsine-transformed percent at- (< 1%) attached to the blades by swimming onto them.
tachment values obtained every hour between 1 and 6 h Swimminggenerally resulted in vertical ratherthan hori-
andat theend of24 h were analyzed with a repeated one- zontaldisplacement. Scallopsprimarilygainedanelevated
ANOVA
way (Wilkinson, 1990). position by crawling, as reported by Pohle et at (1991).
Differences in height attained on eelgrass mimics with Downward crawling was never observed, suggesting that
scallop size were analyzed by a two-step procedure. The scallops may display negativegeotaxisat thisstage oftheir
first step consisted ofa posteriori multiple comparisons lifecycle. Trackingofindividual trajectoriesshowedthat,
ofthe mean height attained by scallops(three trials pooled until theyattainedtheirfinal attachment position, scallops
for each size) at 1,3, 5, 10, 24, and 46-49 h. A Tukey- occasionally fell offthe blades and had to re-initiate their
Kramer test was used on scallop sizes that had homoge- ascent; but on average, over all trials, only 13% (range
neous variances (13.2-mm scallops), and the Games and = 5 to 29%-) fell to the bottom during ascent. Climbing
Howell test was used for those with heterogeneous vari- behavior consistently showed two phases: rapid crawling
ances (5.7- and 7.2-mm scallops). In the second step, the during the first 4-5 h after broadcasting on the bottom,
position of smaller scallops (5.7 and 7.2 mm) was (1 n followed by a slowing or complete cessation ofcrawling.
+ 1(-transformed tocorrect forheterogeneity ofvariances, Mean crawling rates, calculated over the first 4 h for an-
and the mean height ofthe scallops on eelgrass was com- imals that did not fall duringascent, were 4.5 cm h"1 (SE
pared using a repeated two-way ANOVA (Wilkinson, = 0.8, /; = 156) for small scallops (5.7- and 7.2-mm size
1990)withscallopsizeand aquariaasfactors. Timetreat- classes) and 1.2 cm h ' for 13-mm scallops (SE = 0.2,
=
mentswere selected on the basisofresultsofthe multiple 41).
comparisons tests and fulfillment of criteria for homo- Laboratory experiments showed that the vertical dis-
scedasticity among samples (Fmax test). tribution of scallops on eelgrass mimics was markedly
Thedegree ofassociation between shell height and ele- affected by size. Within a 50-cm canopy, small scallops
vation ofscallops attached to eelgrass blades in the field (H = 5.7 and 7.2 mm) reacheda near-average asymptotic
was measured with the Pearson product-moment corre- elevationof20.4 and 18.8 cm respectively, 10hafterbeing
lation coefficient. All data gathered throughout the sum- released into the tanks (Fig. 2); larger scallops (13.2 mm)
merwere included in thisanalysis, but excludingscallops reached a near-asymptotic height of 6.0 cm after 1 1 h.
found on the bottom, i.e.. at height = 0. The height at- Mean height attained by small scallops after 1 h was sig-
tained, calculated as a fraction of total blade length to nificantly different from that achieved after 24 h and
MICROHABITAT OF JUVENILE BAY SCALLOPS 47
40 Fieldstudies
= mm =
H 5.7 (SE 0.04) Vertical distribution ofnatural set. A single cohort of
30 - first-year A. irradians occurred in both embayments
throughout this study (July-October), as indicated by
NWH
unimodal size-frequency distributions obtained in
20 - and NAPH overtime. No significant new recruitment of
E post-settlement scallops wasobserved during late summer
o and early fall at either study site, except for a few new
10 - recruits (< 4% ofthe total) observed in NAPH in early
September, although spawning in these embayments is
CD
c known toextend throughout Juneand July (Bricelj etal,
1987). Growth parameters (changes in total body weight
- mm =
H 7.2 (SE 0.04)
* H - 13.2 mm (SE = 0.07) TableI
30 -
Resultsofrepeatedtwo-wa\analysisofvarianceforcomparisonof
mean heightsattainedbyArgopecten irradiansoneelgrassmimics
20 - A.
Sourceof
variation
10 -
4 8 12 16 20 24 28 32 36 40 44 48
Time
(hours)
Figure 2. Temporal changes in the mean height above bottom at-
tainedbyArgopecien irradiansofthreedifferentsizeclassesoneelgrass
mimicsinthe laboratory(mean bladeheight = 50cm). Datapointsare
fitted to a rectangular hyperbolic function (Y - aX/b + X). Vertical
barsrepresent95% confidence intervals.
46-48 h (for 7.2- and 5.7-mm scallops, respectively), but
not before (P < 0.01, Games and Howell approximate
test for equality ofmeans with unequal variances. Table
IB). A Tukey-Kramer test of multiple comparisons also
indicated significant differences (P < 0.01) in the mean
position of larger (13 mm) scallops after 1, 3, or 24 h
(Table IB). No significant size effects (P = 0.428) were
found in the mean height attained by 5.7- and 7.2-mm
scallops, or in that attained by scallops ofthe same size
=
class located in different aquaria (P 0.376, Table IA).
Meanelevation ofsmall scallops(< 7.2 mm)coincided
with mid-canopy height (0.57 ofblade height; SD = 0.286,
= 126),whereas22%ofthescalloppopulation wasfound
near the top (upper 1/10) ofthe canopy, and none at the
base ofshoot mimics. In general, however, scallops were
distributed throughout most of the length of eelgrass
mimics at the end of 48 h (from 2.5 to 48 cm above
bottom).
48 Z. GARCIA-ESQUIVEL AND V. M. BRICELJ
and dry tissue weight) ofscallops collected in NWH are (h = 0) are included in the calculation of mean heights
shown in Table II. Surface watertemperatures at this site plotted in Figure 4, showing clearly that in both bays the
averaged 27Cin August and 23C in September, attain- entirepopulation hadrelocatedtothebottom bythetime
ing maxima during the second week ofAugust. Temper- scallops reached 31 mm.
atures at NAPH were within 1C ofthose recorded at At NWH, shellgrowthrateincreased from 1.9-2.8 mm
NWH. Shell growth rate throughout the study period av- week"1 between 26 July and 30August, when mostofthe
eraged 13.3 and 12.5 mm month ' at NWH and NAPH scallops remained attached totheeelgrasscanopy, to 3.1-
mm
respectively. Based on these measured growth rates for 4.6 week"1 during the period of relocation to the
juvenile scallops and a duration of7 days for metamor- bottom (30 August to 23 September) (Table II), when
phosisofdissoconch larvae into 1.5-mm plicatedjuveniles attachment dropped sharply from 75% to 1%. Maximum
NWH
in (Eckman, 1987), we estimate that initial settle- shell growth duringthe first week ofSeptembercoincided
ment ofthis cohort occurred in the second week ofJuly. with a reduced rate ofgrowth for soft tissues, which was
Densities ofjuNveWniHle scallops were determined quan- equal to 30 mg week"1, compared to values of52 and 59
titatively only at on 16 August and 20 September, mg week ' during the preceding and following weeks re-
when they averaged 16 and 14 scallops m : respectively. spectively (Table II). At NAPH, maximum rate ofshell
mm
Although eelgrass shoot density and canopy height were growth (4.5 week'1) was recorded at the same time
1.5 times higher in NAPH (mean density SE = 704 asin NWH. Allometricchangesin shell shapewith growth
cm3)5thsahnooitnsNmW*H2; (mdeeansnitcya=no4p6y4hei2g9htshootSsEm= 23;8cano0p.y5 aerleonegvaitidoenn,ceads mbeyatshuersehdabrpytihnecraesapseectinratthieo,dbegerteweeeonfsshiezlels
height = 23.5 0.3 cm), temporal patterns in the per- of 10 and 25 mm, when scallops are gradually shifting
centage ofscallops attached to eelgrass were very similar from a byssate to a free-living habit (Fig. 5). Near-asymp-
at both sites (Fig. 3), and therefore did not appear to be toticvaluesinthisparameter(> 1.05)areattained atlarger
strongly influenced bydifferences in eelgrassstructure. In sizes.
NWH, 100% ofthe population remained attached to eel- Diver observations indicated that scallops exhibited a
grass blades until the second week ofAugust, when scal- marked increase in swimming activity (diver avoidance
lops reached 11.2 mm in mean shell height. In NAPH. response) during transition from an elevated position to
100% attachment wasalso observed until scallops reached the bottom, especially duringthe lastweek ofAugust and
1 1.3 mm, oneweek laterthan in NWH (Fig. 3). A 5-week the second week ofSeptember. This habitat shift was ac-
transitional period followed, during which scallops relo- companied by qualitative changes in vegetation charac-
cated from their elevated position on eelgrass blades to teristics, notablyan increase in the incidenceofsenescent
the bottom. At both sites, more than 90% ofnew recruits (brown ordiscolored) Z. marina blades. Furthermore, in
were found on the bottom by the time they reached a July, the drift red alga (Gracilaria vermcosa, was mostly
mean size of26-29 mm. Scallops found on the bottom restricted to the subtidal zone delimited by the lowereel-
Table H
Meantola!bodvweigh! (TBW), meandrysoft/issuemight (DTW), andshellgrowth ratesofjuvenilebayscallopscollectedfrom natural
populations inNorthwest Harbor. New York, between -6Julyand 10October
Date
MICROHABITAT OF JUVENILE BAY SCALLOPS 49
leptokurtic (g, = 0.547 and 0.151, and g2 = -0.101 and
-0.718 at NWH and NAPH respectively. Skewness was
significantonlyatNWH (/ = 5.24, P<0.001),butkurtosis
was significant at NAPH (/ = 2.95, P < 0.01). The size-
specific distribution ofscallops, expressed asa fraction of
total blade length, differed significantly between the two
na bays (P < 0.001, nonparametric Mann-Whitney test for
o twoindependent samples). In general, alargerproportion
~uo ofthe scallop population was located in the upper halfof
(ort the canopy in NAPH than in NWH (about 50 and 30%
u
.uc respectively; Fig. 6).
o
Octopine dehydrogenase activity. Octopine dehydro-
genase activity was used asan instantaneous index ofthe
scallops' capacity for burst swimming activity. Within-
ODH
individual variability in activity, determined byas-
saying two to three replicate subsamples ofground ad-
ductormuscle from each scallop collected on 10 October
(mean adductor dry weight = 266 mg). averaged 7%.
Lowest mean enzymatic activity (16 ^moles min"' g~'
1990 adductordrywt~')and lowest variation inactivityamong
similar-sized individuals were measured in early August
Figure 3. Temporal changes in mean shell height and percent at- (Fig. 7), when the entire NWH scallop population
it1na99ct0hw.moeAnletlaststoetraenneldgLarroadnssgebrIrlsoalrdasensdaroebfaayssmf,ailrdsltue-rryietnarhgacntohhetohrsetusomyfmmAebrgorolpaedncedtneoentariilnrygrafmadleilaanonsf ((sHee=Fi6g..73m).mM)earenmaOiDneHd aactttiavcihtyedintcortehaeseedelmgarrasksedclaynobpey-
shell height. Mean eelgrass(Zoslera marina) shoot densities within the tween 30 August and 23 September, during relocation to
scallopdistributional areaare indicated foreach harbor. the bottom, when attachment incidence dropped from
grass boundary, outside the scallop's main distributional ^_^
area. However, by the first week ofSeptember, G. verni-
cosawasconspicuous throughout theentire scallop zone,
intermingled with Z. marina or in irregular patches of
1 to 2 nr.
Contrarytolaboratoryresults, nosignificantcorrelation
was found between scallop attachment height (excluding
individuals found onthebottom)andscallop sizein either
NWH (r = 0.003, P = 0.176) or NAPH (r = 0.001,
P = 0.538). This also differs from the laboratory results
of Pohle el al. (1991), who found that the relative pro-
portion ofscallops attached to the upper vs. lower halfof
thecanopy decreased monotonically between scallop sizes
of6 and 20 mm.
Although scallops were found distributed throughout
theeelgrasscanopy at both study sites, theyclustered pri-
marily at or around mid-blade height, between 0.3 and
0.5 of the canopy height, as indicated by the modes of
the frequency distributions shown in Figure 6. This ob-
servation is in general agreement with laboratory results.
The frequency distributions observed in the field departed
significantly from normality (Kolmogorov-Smirnov in-
trinsictest forgoodnessoffit, Z)max = 0.048 and0.053 for
NWH and NAPH respectively, P = 0.01). These distri-
butions were skewed towards the uppercanopy and were
50 Z. GARCIA-ESQUIVEL AND V. M. BRICELJ
initial height in 72% of scallops recovered on eelgrass,
suggestingthat 24h may havebeen insufficienttoachieve
46
maximum, asymptotic height in this field experiment.
1.05 - Relocationexperimentscarriedout in Hallock Baywith
hatchery-reared scallops (H = 10 mm) resulted in rates
v of attachment similar to those found in the laboratory
.C
with scallops ofcomparable size. Three hoursafter being
released in the field, about 60% ofthe scallops recovered
1.00 - wereattached toeelgrass blades, at a mean heightof8.7 cm
(0.3 ofcanopy height), and these values remained relatively
constant thereafter (Fig. 9). Maximum percent attachment
0) 28 andmaximum heightattained(whenexpressedasafraction
.C
00
0.95 -
10 20 30 40
20 -
Mean Shell Height (mm)
Figure 5. Aspect ratio (AR = mean shell length:height (H) ratio
SE)with increasingshell heightofa natural populationofArgopecten D
eirarcahdiamnesacnollveacltueed. iFnitNtoerdthcwuersvteHiasrbdoers.crSiabemdplbeysitzheeiseiqnudaitciaotnedAfoRr -O>->
= (a- d)/[l - (H/21.242) """ + d], whered = 0.944. 10 -
75% to 1%. Maximum mean values of84 ^moles min '
g~' were recorded on 23 September, when scallops had
reached a mean size of29 mm, and appeared to decline en
CL
thereafter.
Napeague Harbor
Overthescallopsize range sampled in thisstudy, there
was an overall, significant, positive relationship between "o5 n - 407
-
octopine dehydrogenase activity (A) and muscle dry CO 20 - X 0.54
weight (W in milligrams), as described by the equation: SD - 0.274
A = 9.87 (SE = 3.52) w'U5ISE=""7> (r = 0.81; n = 57),
determined using SYSTAT iterative nonlinear curve fit-
ting (Wilkinson, 1990). It remains to be determined o
ODH C
whetheradult scallopsexhibit adecline in activities.
High individual variability in ODH activity on any given 0) 10 -
samplingdate may be partly attributabletothelargevari-
ation in scallop sizes. A comparable three-fold range in 0)
the weight ofthe adductor muscles was obtained within
any given sampling date throughout the study period.
Relocation experiments. Results of the relocation ex-
NWH
periment carried out in using individually marked
natural set are shown in Figure 8. Forty-three percent of
the scallops initially released (n = 150. H = 8.6 mm)
{
were recovered alive and 7% were found dead (crushed Relative Elevation
or with empty intact valves) by the end of 24 h. There
was no significant difference between the mean position Figure6. Distribution ofjuvenileArgopcctcn irradiansattached in
(atPt=im0e.z0e6r3o,(Wciolllceoctxioonn)saingdne2d4-rhanfkoltleoswtinfogrdpiasilroeddgecmoemn-t abtrhleeadeieenlclglerunadgsetsdh,.casAnilonlpcyei.ntdhRieevrlieadtwuiaavlsesneclooelvrlaeetlciatotenidoinassbheoixvpperbeegstsrweoeduenandseadluefvrraiatcnitgoiontnhaeonfdsttsoutidazyle
parisons; Fig. 8), although final height was lower than ofattached scallops.
MICROHABITAT OF JUVENILE BAY SCALLOPS 51
100-
E
o
en
OoT
0)
LJ
C
O
c
o
'-*^
'OOT
Q.
Scallop Shell Height (mm)
Figure8. Above-bottomattachmentheightofindividually marked,
juvenile Argopecten irradians from a natural population in Northwest
Harbor,beforeandafterdislodgementfromeelgrassblades.Opencircles
indicatescalloppositionatthetimeofinitialsampling,andclosedcircles
indicateposition24 hafterdislodgement. Meaninitialandfinal heights
(9.9 and 8.0 cm)are indicated by solid and dashed horizontal linesre-
DATE spectively. The arrow marks the mean eelgrass canopy height at the
studysite.
Figure 7. Octopine dehydrogenase activity (in ^moles ofsubstrate
min~'gfreeze-dnedweightofadductormuscle"')ofjuvenileArgopecten
irradianscollected froma naturalpopulation inNorthwest Harbor, be-
tween 2 August and 10 October. Error bars represent 95% confidence variation inscallopgrowth rateswithelevationwithinthe
intervals around the mean for each sampling date. Total number of seagrass bed was found by Ambrose and Irlandi (1992)
aisncslauydeedsitnhdrieveivdaulaulessiosbitnadiinceadtefdoripnooplaerdenrtahtehseers;thtahnein1d0ivOicdtuaolbesrammpleeasn. and Borrero and Bricelj (in prep.), an effect that may be
related to vertical gradients in food quality and quantity,
as well as to flow.
oftotalcanopy height), werethuslowerthanthoseofnatural The predator-refuge value of the eelgrass canopy for
set in NWH and NAPH, and also somewhat lower than juvenile bay scallops has been well established (Pohle et
those obtained in laboratory trials (Fig. 2). No significant al., 1991; Ambrose and Irlandi, 1992). Refugein elevation
dafitfefrer3e,nc5e, awnads2d4ethec(tFed=be0.t1w7e8e)n. the mean height attained issuecfhfeacstigvereiennthcerapbrses(eCnacrecoifnubsotmhaennoanss)w,immmuidngcrparbesda(tDoirss-
panopeus sayii), and spider crabs (Libinia spp.) (Pohle et
Discussion
Laboratory and field results demonstrate that bay scal- E *'
lopscan rapidlygain and maintain above-bottom position
in the eelgrass canopy at sizes below ca. 10-15 mm. The
adaptive significance ofthisbehavior, which allows spatial
segregation ofjuveniles from benthic predators and con-
specific adults, may involve (a) enhanced survival through
avoidance ofpredators and burial in unconsolidated sed-
iments; (b) enhanced growth by positioning scallops in
an optimum hydrodynamic regime that minimizes ex-
posure to resuspended bottom sediments and maximizes
food capture; or (c) a combination ofthese factors. Sea-
grasses are known to markedly reduce near-bottom cur-
rent velocities and water flux (e.g., Fonseca et al., 1983;
Eckman, 1987; Irlandi and Peterson, 1991) while gener-
ating increased turbulence at the water-canopy interface
(Fonseca et al., 1982; Gambi et al., 1990), thus creating
steep vertical gradients in the flow regime. Significant