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MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser
Vol. 494: 191203, 2013doi: 10.3354/meps10572
Published December 4
INTRODUCTION
A central goal of ecology is to understand patternsof abundance
and distribution of organisms. Deter-mining the key factors that
drive population dynam-ics requires knowledge of demographic inputs
(birthand immigration) and losses (death and emigration).In marine
systems, the process of larval dispersal
adds additional complexity to quantifying populationinputs as
many marine organisms release dispersivelarvae that act as the
primary agents coupling birth atone site to immigration at another.
Therefore, larvalrecruitment to coastal populations relies not only
onreproductive output of parent populations and post-settlement
processes, but also on oceanographic fac-tors that affect the
dispersal and delivery of settlers
Inter-Research 2013 www.int-res.com*Email:
[email protected]
Spatial differences in larval abundance withinthe coastal
boundary layer impact supply to
shoreline habitats
Kerry J. Nickols1,4,*, Seth H. Miller1, Brian Gaylord1,2, Steven
G. Morgan1,3, John L. Largier1,3
1Bodega Marine Laboratory, University of California at Davis,
Bodega Bay, California 94923, USA2Department of Evolution and
Ecology, University of California at Davis, Davis, California
95616, USA
3Department of Environmental Science and Policy, University of
California at Davis, Davis, California 95616, USA
4Present address: Hopkins Marine Station, Stanford University,
Pacific Grove, California 93950, USA
ABSTRACT: Explorations of the dynamics of nearshore regions of
the coastal zone are missingfrom many efforts to understand larval
transport and delivery to suitable habitats. Larval distribu-tions
in the coastal ocean are variable and depend on physical processes
and larval behaviors,leading to biophysical interactions that may
increase larval retention nearshore and bolster theirreturn to
natal sites. While recent evidence suggests that many larvae are
retained within a fewkilometers from shore, few studies incorporate
measurements sufficiently close to shore to plausi-bly assess
supply to the shoreline benthos. We measured cross-shore
distributions of larvae ofbenthic crustaceans between 250 and 1100
m from shore (i.e. just beyond the surf zone) within thecoastal
boundary layer (CBL) a region of reduced alongshore flow and
simultaneously quan-tified a suite of physical factors that may
influence larval distributions. We found high larval abun-dance
within the CBL, with a peak at 850 m from shore, and a decrease in
abundance along theshoreward edge of the sampled transect. We also
found distinctly different larval assemblages atouter stations
within the CBL, as compared to inner stations that are more
influenced by shorelinedynamics. These patterns persisted across
sample dates, suggesting that the spatial structure ofnearshore
larval assemblages is at least somewhat robust to temporal changes
in physical condi-tions. Thus, while larval abundance appears to be
high within the CBL, larvae appear to be sparsewithin the narrow
band of water adjacent to the surf zone. Low larval supply adjacent
to suitablehabitats has important implications for the coupling of
supply and recruitment, and resultingdynamics of shoreline
populations.
KEY WORDS: Dispersal Invertebrate larvae Retention Nearshore
Transport
Resale or republication not permitted without written consent of
the publisher
FREEREE ACCESSCCESS
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Mar Ecol Prog Ser 494: 191203, 2013
(Cowen 1985, Gaines et al. 1985, Roughgarden et al.1988, Gaylord
& Gaines 2000, Morgan 2001, Under-wood & Keough 2001,
Largier 2003, Prairie et al.2012). While larval recruitment is a
critical determi-nant of population structure (Gaines &
Roughgarden1985, Underwood & Fairweather 1989, Menge et
al.2004) and larval delivery has long been recognizedfor its role
in driving population dynamics (Thorson1946), larval transport
pathways and connectivity aredifficult to quantify due to the small
size of larvae andthe difficulty of tracking them (Levin 2006).
Thesedifficulties are exacerbated by a lack of understand-ing of
how larval supply varies over time and space.
Relatively few studies have measured larval supplyand settlement
concurrently in such a way as to ex -plicitly link them. Those that
have done so havereached mixed conclusions: some found supply
andsettlement to be coupled (e.g. Gaines et al. 1985,Bertness et
al. 1992, Gaines & Bertness 1992, Dudaset al. 2009) while
others did not (e.g. Yoshioka 1982,McCulloch & Shanks 2003,
Rilov et al. 2008). Suchdifferences may be due to the magnitude of
recruit-ment, with larval supply acting as a strong predictorof
adult dynamics in regions where recruitment islimited (Connell
1985), but less so in areas where re -cruitment is high.
Connections between supply andsettlement or recruitment may be
easier to assess inother systems; for instance those involving
dispersalof macroalgal spores (see, e.g. Reed et al. 1988, Gay-lord
et al. 2002, 2004, 2006, 2012, Reed et al. 2006).
Much of the west coast of North America is recruit-ment-limited
to one degree or another, such that lar-val supply is a critical
determinant of populationdynamics in many species. This feature
derives fromthe fact that the west coast sits within a major up
-welling region. During times of strong equatorwardwinds, the
predominant currents flow equatorwardand surface waters move
offshore. The potential forupwelling waters to move larvae offshore
has beenwidely recognized (Yoshioka 1982, Roughgarden etal. 1988,
Botsford et al. 1994), and is consistent withobservations that
larval settlement and supply in persistent upwelling regions is
higher during relax-ation events when wind speeds decrease or
reversedirections (Farrell et al. 1991, Botsford 2001). In -creases
in settlement and supply during relaxationevents can also result
from poleward advection of lar-vae (Wing et al. 1995a,b). More
recent work hasshown the persistence of sequential larval stages
innearshore plankton during upwelling conditions,indicating that
many taxa are not swept offshore inupwelling regions (Morgan et al.
2009b, Shanks &Shearman 2009). Larvae appear to be able to at
least
partially avoid offshore transport associated withupwelling
through physical and behavioral mecha-nisms. Nearshore retention
zones arising from topo-graphic effects on coastal circulation have
been ob -served (Graham & Largier 1997, Wing et al.
1998,Roughan et al. 2005), and are associated with higherlarval
abundances and settlement (Mace & Morgan2006, Morgan et al.
2009a, 2011, 2012). Avoidance ofsurface waters by larvae can favor
retention and de -crease offshore transport (Morgan et al.
2009b,c,Shanks & Shearman 2009, Morgan & Fisher 2010,Morgan
et al. 2012) and there is mounting evidencethat larval
concentrations are high close to shore,even in areas of strong
upwelling that are tradition-ally viewed as being
recruitment-limited. Here weinvestigate this phenomenon closer to
shore to see ifhigh abundances extend over the inner shelf
andinward to the shoreline.
Nearshore processes play an important role in lar-val ecology,
and may be relevant for a significantportion of pelagic larval
durations. A number of re -cent studies measured larval abundance
in cross-shore transects and found increases in abundancecloser to
shore in a range of invertebrates and fishes(Borges et al. 2007,
Tapia & Pineda 2007, Morgan etal. 2009b,c, Shanks &
Shearman 2009). For example,Morgan et al. (2009b) measured larval
abundance ofbenthic crustaceans from 1 km from shore out to
theshelf break (30 km offshore) along the open coast ofnorthern
California and found that the highest larvalabundances were within
3 km from shore. The com-bination of larval behaviors (e.g.
swimming and ver-tical migration) and nearshore processes may in
-crease retention of larvae close to shore and to theirnatal site.
Such retention is consistent with evidencefrom a range of species
and systems that shows self-recruitment is higher and dispersal
distances smallerthan previously thought (Swearer et al. 2002,
Levin2006, Shanks 2009), and further emphasizes theimportance of
understanding the role of nearshoreprocesses in larval supply and
population dynamics.
A number of nearshore processes may reducescales of dispersal.
Adjacent to the shore within thesurf zone, rip tides can create
recirculation zones(MacMahan et al. 2010) and onshore wave
transportcan lead to accumulation of water-borne material(Monismith
2004, McPhee-Shaw et al. 2011). There isalso a region termed the
coastal boundary layer(CBL) that extends beyond the surf zone and
is char-acterized by reduced speeds (Nickols et al. 2012).
Inparticular, average alongshore velocities in the CBLare an order
of magnitude larger than cross-shorevelocities (Lentz et al. 1999,
Gaylord et al. 2007), and
192
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Nickols et al.: Larvae in the coastal boundary layer
alongshore velocities increase strongly with distancefrom shore
until reaching a free-stream value off-shore (Nickols et al. 2012).
Such decreased velocitiesprovide another potential mechanism for
reducingscales of dispersal in coastal populations (Nickols etal.
2012, Nickols et al. unpubl. data), but require thatlarvae spend
sufficient time within the CBL forreduced flow to influence net
transport. Because pre-vious studies of coastal larval
distributions did notextend into the CBL or only just entered the
CBL(McQuaid & Phillips 2000, Morgan et al. 2009b,c,Shanks &
Shearman 2009), or sampled over an insuf-ficient temporal scale to
fully characterize patterns(Tapia & Pineda 2007), the general
role of the CBL ininfluencing patterns of larval transport and
supplyremains unknown.
The goals of this study were therefore to addressthe following
questions: (1) what is the spatial patternof larval abundance
within the CBL, (2) are there differences in larval assemblages
close to shore (i.e.are different larvae found inshore versus
offshorewithin the CBL), and (3) do time-dependent or space- de
pendent physical processes tend to dictate vari-ability in larval
abundance? We recognize in target-ing these goals that it is not
possible to definitivelyascribe particular mechanisms to observed
patterns;rather, our aim is to present the first description of
thespatio-temporal distribution of larval assemblageswithin the
CBL, which is critical for understandingthe potential for nearshore
transport processes toimpact larval supply to shoreline habitats.
We addi-tionally hope that this study will also inform
themethodological question of where supply should bemeasured to
best address relationships between set-tlement and supply when
exploring questions aboutmarine population dynamics, particularly
for recruit-ment- limited regions.
MATERIALS AND METHODS
Study system and species
This study was conducted along the open coast innorthern
California, USA, near Bodega Head, Cali-fornia (Fig. 1), a region
characterized by strong sea-sonal upwelling during spring and
summer thatdrives prevailing currents equatorward and pushessurface
waters offshore (Winant et al. 1987, Largier etal. 1993). When the
winds weaken or reverse direc-tion (inducing a relaxation event),
currents movepoleward, often responding within a day or less invery
nearshore regions (Send et al. 1987). Inner shelf
currents, observed previously on the scale of kilome-ters, are
slower than currents farther offshore, have ahigher tendency to
move poleward (Kaplan et al.2005), and are associated with
increases in inverte-brate settlement (Wing et al. 1995a,b).
Benthic crus -ta cean larvae can be present during both
relaxationand upwelling conditions within areas of
topographicretention and along the open coast, and many can
beretained in areas within 1 to 3 km of the shore via acombination
of physical and behavioral mechanisms(Morgan et al. 2009b, Morgan
& Fisher 2010, Morganet al. 2012). The present study focused on
waterswithin 1 km of the shore.
Our efforts focused on larvae of benthic crusta -ceans
(primarily barnacles and crabs), which are thebest-studied
meroplankton in this region. From priorwork, it is known that
larval abundance of benthiccrustaceans peaks during the spring and
summer,coinciding with the upwelling season. Barnacles moltthrough
6 larval stages (nauplii) and a postlarvalstage (cyprid) and spend
about 2 to 4 wk in the water
193
10 m
20 m 30 m
38.325N
38.3215
38.318
38.3145
38.311
Lat
itud
e
123.084W 123.076 123.068Longitude
Fig. 1. Map of the study region showing the cross-shelf
tran-sect located off Bodega Head in northern California,
USA.Circles indicate locations of moorings where plankton towsand
CTD casts began. The moorings on the 10, 15, and 22 misobaths
included bottom mounted ADCPs and thermistors.The mooring on the 15
m isobath contained a thermistorstring measuring temperature at
depths of 4, 7, 10, and 14 m.Wind velocity was measured via an
anemometer located on-shore at the Bodega Marine Laboratory,
indicated by the
square
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Mar Ecol Prog Ser 494: 191203, 2013
column (Strathmann 1987). Barnacle larval releasegenerally
begins in spring (Gaines et al. 1985, Strath-mann 1987) and is
continuous through the summermonths (Shanks & Eckert 2005).
Barnacle speciesfrom both subtidal (Balanus crenatus, B. nubilus)
andintertidal (B. glandula, Chthamalus spp., and Polli -cipes
polymerus) habitats are common in this region(Morgan & Fisher
2010). Crab larvae spend weeks tomonths in the plankton, and peak
recruitment formost species in this region is during the spring
andsummer (Shanks & Eckert 2005, Mace & Morgan2006). The
most common taxa include members ofthe families Pinnotheridae,
Porcellanidae, Cancri -dae, and Majidae.
Larval samples
Cross-shore distributions of nearshore larvae weresampled during
6 daytime cruises using a 0.5 m dia -meter, 200 m mesh net equipped
with a mech ani -cal flow meter (Model 2030, General Oceanics).
Thenet was modified with a sled to accommodate tow-ing along the
bottom. Cruise dates spanned 3 moduring the upwelling season, from
May throughJuly 2010, and occurred approximately every 10 d(Fig. 2)
under a variety of oceanographic conditions.We sampled 4 stations
in a cross-shore transectalong the 10, 15, 22, and 30 m isobaths,
correspon-ding to ap proximately 250, 425, 850, and 1100 mfrom
shore (Fig. 1). We refer to the 10 and 15 m iso-bath stations as
inner CBL stations, and the 22 and30 m isobath stations as outer
CBL stations. Weconducted a single 10 min oblique tow at each
station, which sampled from the bottom to the sur-face of the water
column. Larvae were sorted andidentified to species, or the lowest
taxonomic grouppossible, and developmental stage. Larval
abun-dances were calculated per m3 to standardize
acrossstations.
Physical data
To provide physical context during our study, wemeasured
currents, temperature, salinity, and winds.Current speed and
direction were measured through-out the water column using moored
acoustic Dopplercurrent profilers (Workhorse Sentinel ADCP,
1200kHz; Teledyne RD Instruments). Instruments werelocated on the
10, 15, and 22 m isobaths near thestarting position for plankton
tows. The ADCPs col-lected 1 min bursts of 0.75 Hz velocity data
every 2
min in 1 m vertical bins that typically extended from~1.5 m
above the bottom to ~1.5 m below the surface.The velocity record at
the 10 m station ended earlyon 10 June 2012 when its anchor was
dislodged. Toquantify general velocity patterns, the raw
velocitytime series were depth-averaged, ro tated onto
theirprincipal axes, and low-pass filtered with a 33 h cut-off to
remove dominant tidal motions (Rosenfeld1983). The major principal
axes aligned parallel toshore and along-isobath, corresponding to
an angleof 300.
Bottom temperature was recorded at the ADCPmooring sites every
minute over the duration of thestudy at the 10, 15, and 22 m
stations, and tempera-tures at depths of 4, 7, 10, and 14 m were
recorded atthe 15 m station (SBE 37 and SBE 39, Sea-Bird
Elec-tronics). During cruises, temperature, salinity, anddensity
were profiled at each station throughout thewater column using a
conductivity, temperature, anddepth profiler (SBE 19-Plus, Sea-Bird
Electronics),with the exception of the cruise on 25 June.
Wind data during this study were available from ananemometer
located on the shore at the Bodega Mar-ine Laboratory, within 1 km
of the study locations, ata height of 20 m (38 19 3.35 N, 123 4
17.20 W;RM Young 05103 Wind Monitor; data available on -line
http://bml.ucdavis.edu/boon/).
Data analysis
We performed multivariate analyses to determineif larval
abundance and larval assemblages variedwith distance from shore and
with time. We exam-ined patterns of cross-shore abundance for all
taxa,for crab and barnacle larvae separately, and accord-ing to
larval stage. All statistical analyses were con-ducted using the
multivariate statistical softwarepackage PRIMER v. 6.1.10 (Clarke
& Gorley 2006).We determined whether larval assemblages
changedwith distance from shore and with sampling dateusing
nonparametric analysis of similarity (ANOSIM)and hierarchical
cluster analysis and ordination. Datawere fourth-root transformed
to reduce the hetero-geneity of variance among samples and
assembledinto a Bray- Curtis dissimilarity matrix with a
dummyvariable of 1. The resultant dendrogram was testedfor group
differences using a similarity profile test(SIMPROF), and the
percentage contribution (SIM-PER) of each species and stage to the
significant clus-ters was as sessed to classify species-stage
combina-tions by their cross-shore distributions and samplingdate.
We used non-metric multidimensional scaling
194
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Nickols et al.: Larvae in the coastal boundary layer 195
(NMDS) to exa mine separation of assemblagesaccording to sample
date and distance from shore. Toassess if community composition was
structured inspace or time, we repeated each of these analyses
onuntransformed data that were standardized by totalsample
abundance. For all analyses, when there wassignificant structure
among samples we then deter-mined which species and stages
contributed to thepatterns.
RESULTS
Physical conditions
During the study period, we cap-tured a variety of oceanographic
con-ditions, including upwelling, relax-ation, and post-relaxation
(Fig. 2).However, our larval sampling datesgenerally occurred
during low-windconditions due to logistical constraintson field
operations. Daily- averagedalongshore wind speeds during
eachsampling date ranged from 8 m s1,indicative of northwesterly
winds, to8 m s1, indicative of southeasterlywinds, but winds were
predominantlyupwelling favor able over the studyperiod (Fig. 2A).
While depth-aver-aged alongshore currents are knownto alternate be
tween equatorwardand poleward in this region (Largieret al. 1993,
Roughan et al. 2005, Ka-plan & Largier 2006, Morgan et
al.2012), on all sampling days of ourstudy the alongshore current
waspoleward (Fig. 2B). In general, depth-averaged alongshore
velocities meas-ured at inner CBL locations (10 and15 m isobaths)
were slower than ve-locities measured at the outer CBL in-strument
on the 22 m isobath(Fig. 2B), characteristic of a coastalboundary
layer. Exceptions occurredduring onset of strong up wellingwinds on
20 May and 6 June and dur-ing flow reversals.
Water column properties duringlarval sampling dates ranged
fromwell-mixed to stratified (Figs. 2 & 3).The 17 May, 9 June,
and 25 Junesampling events represented up well - ing conditions,
with a cold homo -geneous water column across sta-
tions: temperatures below 10C and salinitiessimilarly uniform,
with the exception of some low-salinity water on the surface near
the outer station on17 May (Figs. 2, 3A & 3C). Alongshore wind
speedson the day preceding these sampling dates werefrom the
northwest and reached up to 10 m s1, characteristic of strong
upwelling conditions andaccounting for the presence of cold
isothermal condi-tions over the inner shelf. On 27 May and 4 July,
the
Fig. 2. (A) Alongshore wind velocity measured at Bodega Marine
Laboratory.(B) Alongshore depth-averaged and 33 h low-pass filtered
current velocitymeasured by bottom-moored ADCPs at the 10, 15, and
22 m isobaths. Positivealong shore velocity is poleward and
negative alongshore velocity is equator -ward. (C) Bottom
temperature measured on the ADCP moorings at the 10, 15,and 22 m
isobaths. (D) Temperature at depths of 4, 7, 10, and 14 m measured
at
the 15 m isobath. Vertical gray bars indicate when sampling
occurred
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Mar Ecol Prog Ser 494: 191203, 2013
water column was stratified at the 2 inner CBL sta-tions (Figs.
2, 3B & 3D), following a day of southeast-erly or weak winds.
After 4 July temperatures in -creased substantially, and the water
column wasstratified at all stations on the 14 July sampling
day(Fig. 2C). Winds during this period were substantiallyweaker
than previous sampling events (Figs. 2C, 2D& 3E).
Larval abundance
We identified larvae of 22 crustacean species dur-ing our study
(Table 1). The outer CBL station, alongthe 30 m isobath, had the
highest number of species,with 10 species on average as compared to
6 to 7 spe-
cies at the other stations. Throughout the study, lar-vae were
most abundant along the 22 m isobath,850 m from shore (Fig. 4A).
This pattern was drivenby high abundances of barnacle larvae (Fig.
4B).Early, middle and late stage barnacle larvae werepresent at all
stations with the highest abundancealong the 22 m isobath (Fig.
5A). Barnacle postlarvae(cyprids) were found in similar abundance
across sta-tions. Crab larvae were most abundant near the 30
misobath, 1100 m from shore (Fig. 4C). All larval crabstages were
most abundant at the 2 outer CBL sta-tions, although early stage
crab larvae dominated thesamples and abundance decreased with
increasingstage (Fig. 5B). Very few crab larvae were found atthe
inner CBL stations, and the majority of thosewere early stage
larvae.
196
0
10
20
30
0
10
20
30
0
10
20
30
0
10
20
30
0
10
20
30
Temperature (C) D
epth
(m)
Cross-shore distance (km)
15
10
15
10
15
10
15
10
15
10
E
A
B
C
D
9
1011
9
9 9
9
1011 12
11 12
13 14 15
Salinity
34
33
33.5
34
33
33.5
34
33
33.5
34
33
33.5
34
33
33.5 34
33.8
33.8
34
34
33.8 33.6
33.8
33.6
33.4
0 0.25 0.5 0.75 1 1.25 0 0.25 0.5 0.75 1 1.25
Fig. 3. Contours of temperature (left) and salinity (right) at
the beginning of larval tows along the 10, 15, 22, and 30 m
isobathson (A) 17 May 2010, (B) 27 May 2010, (C) 9 June 2010, (D) 4
July 2010, and (E) 14 July 2010. Sample locations are indicated
by
triangles
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Nickols et al.: Larvae in the coastal boundary layer
Larval assemblages
Considering all taxa, larval assemblages within theCBL differed
among stations (2-way ANOSIM av =0.322, p = 0.017) and were similar
among dates. Be -cause overall larval assemblages were not
structuredby date we performed a 1-way ANOSIM to detectspatial
differences among assemblages at the differ-ent stations. The
innermost station drove differencesbetween assemblages, and it
differed from the 2outer stations (1-way ANOSIM pairwise test: for
10 mvs. 30 m stations: R = 0.463, p < 0.01; for 10 m vs. 22
mstations: R = 0.609, p < 0.01). These differences were
echoed in the dendrogram from cluster analysis, andthe NMDS
ordination, which both revealed spatialstructure with 2 main
clusters: one defined by lownumbers of larvae, with samples
primarily from innerCBL stations, and the second defined by high
num-bers of larvae, with samples primarily from the outerCBL
stations (Fig. 6).
Partitioning the analysis by taxa, we found thatpatterns of
barnacles and crabs differed. Crab larvalassemblages by themselves
did not differ by stationor date, but barnacle larval assemblages
did differ bystation and sampling date (2-way ANOSIM: stationav =
0.322, p = 0.02; date av = 0.35, p < 0.01). Thedendrogram from
cluster analysis and the NMDSordination revealed 2 main clusters of
barnacle sam-ples. One cluster occurred early in the season
andmostly offshore, and it was composed of samplesfrom all stations
during 17 May and samples from theouter CBL stations during June
and July. The othercluster occurred late in the season (June
throughJuly) and consisted primarily of samples from theinner CBL
stations (Fig. 7). In the early-season, outerCBL assemblage,
barnacle larval abundances wereas high as 7200 larvae m3, whereas
in the late-season, inner CBL assemblage, barnacle concentra-tions
were less than 500 larvae m3.
We also analyzed changes in the composition of thelarval
assemblage. We divided our larval counts (bothspecies and stage) by
the total number of larvae ineach sample, providing a fraction of
the total samplefor each species and stage, to standardize the data
fordifferences in larval abundance across time. Larvalcommunity
composition within the CBL differedmostly among stations, but also
by date (2-wayANOSIM station av = 0.394, p < 0.01; date av =
0.282,p = 0.026). As noted previously, date was not signifi-cant
when abundance was considered in the analysisof larval assemblages.
In this analysis of composition,
197
10 15 22 300
1000
2000
3000
Cru
stac
ean
larv
ae m
3
10 15 22 300
1000
2000
3000
Bar
nacl
e la
rvae
m3
10 15 22 300
100
200
300
Cra
b la
rvae
m3
Station depth (m)
CBA
Fig. 4. Average larval abundance and standard error across date
by station for (A) all benthic crustaceans, (B) barnacles, and (C)
crabs. Note that the y-axis of (C) is an order of magnitude smaller
than (A) and (B)
Family Taxon
Cirripedia Balanus crenatus Balanus glandula Balanus nubilus
Chthamalus dalli Lepas spp. Pollicipes polymerus
Cancridae Cancer antennarius Cancer magister Cancer productus
Carcinus maenas
Grapsidae Hemigrapsus oregonensis
Hippidae Emerita analoga
Majidae Mimulus foliatus Pugettia producta Pugettia richii Scyra
acutifrons
Paguroidae Pagurid spp.
Pinnotheridae Pinnotheridae
Porcellanidae Pachycheles spp. Petrolisthes cinctipes
Thalassinidae Neotrypaea californiensis
Xanthidae Lophopanopeus bellus
Table 1. Crustacean larvae identified in the study
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Mar Ecol Prog Ser 494: 191203, 2013198
10 15 22 30 10 15 22 300
500
1000
1500
2000
2500B
arna
cle
larv
ae m
3
Station depth (m)
EarlyMidLatePL
0
50
100
150
Cra
b la
rvae
m3
BA EarlyLatePL
Fig. 5. Average larval abundance and standard error across date
by station for (A) barnacles according to early, mid, late, and
postlarval (PL) stage and (B) crabs according to early, late, and
PL stage
Sim
ilarit
y (%
)
20
40
60
80
100
10
10
10
15
10 10
15
15
30
15
22
15
30
22
30
22
30 10
22 30
22 15
30 22
Similarity 40% 55%
A
B15 10 10 10 30 10 15 15 10 30 30 22 30 15 22 22 30 15 10 22 22
15 30 22
5/17/2010 5/27/2010 6/9/2010 6/25/2010 7/4/2010 7/14/2010
Fig. 6. (A) Hierarchical clustering dendrogram (using
group-average linking) of larval assemblages of benthic
crus-taceans from 24 samples taken over 6 d (indicated by sym-bols
and legend entry) at 4 sampling stations across thecoastal boundary
layer (along the 10, 15, 22, and 30 m iso-baths, indicated by
numbers adjacent to symbols), usingtransformed data. Solid black
lines indicate significantgroup structure at the 5% level. Dashed
lines represent non-significant group structure. Sample station
isobaths are re-ported beneath each symbol. (B) Non-metric
multidimen-sional scaling plot (2D stress, 0.15; 3D stress, 0.09)
from the24 samples with superimposed significant clusters at simi
-larity levels of 40% (solid lines) and 55% (dashed lines).
Symbols and numbers as in (A)
22 30 15 30 10 10 30 10 15 15 10 30 30 22 22 15 10 22 22 15 10
22 15 30
Sim
ilarit
y (%
)
20
40
60
80
100
5/17/2010 5/27/2010 6/9/2010 6/25/2010 7/4/2010 7/14/2010
A
B
10
10 10
15
15
15 10
10
10 15
15
15
22
22
22
22
22 22
30
30
30 30
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30
Similarity 55% 75%
Fig. 7. (A) Hierarchical clustering dendrogram (using
group-average linking) of barnacle larval assemblages from
24samples taken over 6 d (indicated by symbols and legendentry) at
4 sampling stations across the coastal boundarylayer (along the 10,
15, 22, and 30 m isobaths, indicated bynumbers adjacent to
symbols). Solid black lines indicate sig-nificant group structure
at the 5% level. Dashed lines repre-sent non-significant group
structure. Sample station iso-baths are reported beneath each
symbol. (B) Non-metricmultidimensional scaling plot (2D stress,
0.12; 3D stress,0.07) from the 24 samples with superimposed
significantclusters at simi larity levels of 55% (solid lines) and
75%
(dashed lines). Symbols and numbers as in (A)
-
Nickols et al.: Larvae in the coastal boundary layer
the effect of date was driven by one particular sam-pling event
on 9 June, when there was a distinct innerCBL assemblage (10 and 15
m stations; 92% similar-ity). The dendrogram from cluster analysis
and theNMDS ordination showed 2 additional as semblages(Fig. 8): an
inner CBL assemblage (68% similarity)and a main CBL assemblage
containing nearly all ofthe other samples from the CBL, the 2 outer
CBL sta-tions as well as the 15 m station (67% similarity).
The barnacles Balanus crenatus and B. nubilus lar-vae dominated
the composition of the assemblageand drove differences between
clusters. The assem-blage at the inner CBL stations on 9 June (Fig.
8) wascomposed of >75% B. crenatus cyprids. All other
samples were composed of 30% or less B. crenatuscyprids. In
addition, the 9 June inner CBL assem-blage contained
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Mar Ecol Prog Ser 494: 191203, 2013200
da (2007) measured larval concentrations of Balanusglandula and
Chtha ma lus spp. at 3 cross-shore sta-tions within 1100 m from
shore over a period of 7 d.While concentrations of most larval
stages of B. glan-dula were similar among stations, concentrations
ofthird through sixth stage Chthamalus nauplii werelower at the
innermost station, 300 m from shore(Tapia & Pineda 2007). Even
over a short temporalperiod, barnacle concentrations exhibited
spatialstructure and nauplii may potentially have avoidedvery
nearshore waters.
Despite low concentrations of larvae in the inner-most waters of
the CBL, the high concentrations of alllarval stages of barnacles
in the CBL along the 15, 22,and 30 m isobaths suggest that many
barnacle larvaemay be retained within the CBL and develop in waters
within 1100 m from shore. All larval stagesof crabs occurred at the
2 outer CBL stations, sug-gesting that they may also complete
developmentwithin the CBL. These findings are consistent withother
studies in both weak and strong upwelling re-gions where high
abundances of all larval stages oc-curred within a few kilometers
from shore (Tapia &Pineda 2007, Morgan et al. 2009b,c, Shanks
& Shear-man 2009, Morgan & Fisher 2010, Morgan et al.
2011,2012). Benthic crustacean larvae exhibit depth pref-erences
that can aid nearshore retention for mostspecies in upwelling
regions (Miller & Morgan 2013).By remaining near the bottom,
larvae can take ad-vantage of slower velocities in the bottom
boundarylayer (in both the along- and cross-shore directions),as
well as avoid offshore transport in the surface Ek-man layer
(Morgan et al. 2009b, Shanks & Shearman2009, Morgan &
Fisher 2010, Morgan et al. 2012).
Inshore and offshore assemblages within the CBL
A distinct larval assemblage occurred closest toshore within the
CBL. Although some features of lar-val assemblages changed with
time, these assem-blages were predominantly defined by space:
notonly was there spatial structure in larval abundance,there was
spatial structure in the composition of theas semblage. This
spatial structure occurred eventhough physical conditions were
variable amongsampling dates (flow velocity, water
temperature,stratification) and on many days there was no
cleardifference in physical parameters between the inner-most
station and those within the rest of the CBL(Figs. 2 & 3).
The spatial boundary between assemblages ofinner and outer
stations within the CBL is dynamic.
Larval assemblages on half of the sampling dates atthe 15 m
station were most similar to the 10 m station,and on the other half
were more similar to the 22 mstation. There is no clear physical
difference betweenthese groupings of days apparent from our data,
asthey spanned oceanographic conditions. For exam-ple, on 9 June, 4
July, and 14 July the 15 m stationmatched most closely with the 10
m station, yet thewater column profiles from each of these days
arequite distinct (Fig. 3CE). One possible physical fac-tor we did
not explore that could influence thedemarcation of the inshore
community is the width ofthe surf zone and associated rip current
zone, whichis itself a dynamic boundary, dependent on the
sig-nificant wave height and tidal elevation (Lentz et al.1999,
Brown et al. 2009). Surf zone characteristicsappear to impact
shoreline settlement of inverte-brates, with low settlement
observed at reflectivebeaches which are characterized by high
beachslopes and standing waves and are thought to havereduced
cross-shore exchange (Shanks et al. 2010).Rocky shores are
hypothesized to be similar to reflec-tive beaches, and if so, the
associated reduction incross-shore ex change might explain low
settlementat some locations and low abundances of larvae insurf
zone waters (Shanks et al. 2010). Our studyfound low larval
concentrations in waters just beyondthe surf zone, but at distances
that could be influ-enced by surf zone processes through the action
ofrip currents. Specifically, off Horseshoe Cove (Fig. 1,just
downcoast of station locations), wave-driven cir-culation has been
observed to extend as a macro-ripup to distances ~250 m offshore
(J. L. Largier,unpubl. drifter data), comparable with the distance
toour inner CBL station along the 10 m isobath. Thissuggests that
the influence of wave-driven processeson larval transport may
extend offshore (contrary tothe idea of reduced exchange off rocky
shores, assuggested by Shanks et al. 2010).
In addition to potential physical differences be -tween the
habitat of the inshore and offshore as -semblages, predation may be
higher within the nar-row band of inner CBL water than farther
offshore.Habitat along the 10 m isobath at our study site fea-tures
rocky substrate with some areas supportingstands of the bull kelp,
Nereocystis luet keana. Incentral California, larval abundances
were found tobe negatively correlated with kelp density, and
lowerlarval abundances on the inshore edges of kelpforests were
attributed to predation (Gaines &Rough garden 1987). Although
the kelp in our regionis much more sparse than the giant kelp
Macrocystispyrifera beds in central California, predation is still
a
-
Nickols et al.: Larvae in the coastal boundary layer
possible explanation for decreased abundance at themost inshore
station of our study.
Implications of cross-shelf larval structurewithin the CBL
Larvae are clearly spending time within the coastalboundary
layer; some may even complete their entiredevelopment within the
CBL, which could impactestimates of population connectivity. During
theirtime in the CBL, larvae are exposed to slower movingalongshore
flows than farther offshore, which willhave an impact on overall
dispersal distance (Nickolset al. 2012, Nickols et al. unpubl.
data). Although wedid not have current velocity measurements
through-out the water column beyond the 22 m isobath, con-current
measurements of surface currents by high- frequency radar showed
that current velocities werefaster farther offshore (data not
shown). The radardomain begins 2 km offshore, and generally has
highagreement with measurements from ADCPs (Kaplanet al. 2005).
This gradient is also observed in a cross-shore array of moorings
deployed during WEST(Wind Events and Shelf Transport; Largier et
al.2006) and in other unpublished data from BML. Esti-mates of
dispersal distance in this region shouldtherefore consider current
velocities within 1 km orless from shore, as this is where the
majority of larvaeappear to be concentrated. Such consideration
mayimprove estimates of dispersal distance derived frompelagic
larval durations, which are often larger thandispersal distances
estimated from genetics, tagging,and natural tracers (Palumbi 2004,
Jones et al. 2009,Shanks 2009, Lpez-Duarte et al. 2012). Refining
ourunderstanding of dispersal distances will improveour ability to
accurately model population dynamicsand assess population
persistence (Botsford et al.2009, White et al. 2010, Burgess et al.
in press).
The coast of northern California generally haslower recruitment
than other regions along the westcoast of North America (Connolly
et al. 2001), and alongstanding question has been whether or not
thispattern is linked to larval supply. Although it wasproposed
that larval supply is diminished when lar-vae are forced offshore
by strong upwelling (e.g.Roughgarden et al. 1988), numerous studies
nowsuggest strongly that many larvae of multiple speciesare
retained nearshore during both upwelling andrelaxation conditions
(Tapia & Pineda 2007, Morganet al. 2009b,c, Shanks &
Shearman 2009, Morgan &Fisher 2010, Morgan et al. 2011). Our
study alsofound high abundance of larvae close to the shore,
and extended closer to shore than previous work inthis region of
strong upwelling.
An important finding of our study is the observa-tion of low
larval concentrations and a different lar-val assemblage in the
innermost waters of the CBL,indicating a potential disconnect
between high larvalabundance in the CBL and larval supply to
shorelinerecruitment habitat. Further, this disconnect appearsto
occur in waters beyond the surf zone, in contrast torecent work by
Shanks et al. (2010) that suggests thatsurf zone processes may
disrupt the supply of near -shore planktonic larvae to shoreline
habitats. Whilethese results are from a single location, they
repre-sent a diversity of oceanographic conditions and theobserved
mismatch raises important questions abouthow general this result
may be. Our study also fo -cuses attention on the need to
understand the mech-anisms that control transport of larvae to
shorelinehabitats, while highlighting methodological concernsof
studies that explore links between supply and set-tlement. As we
endeavor to better understand thelinks between larval dispersal and
population dy -namics, it is essential that the nearshore zone
bestudied in greater detail and that we work to addressthe spatial
pattern of recruitment limitation in coastalsystems.
Acknowledgements. We thank J. Demmer, R. Fontana, andN. Weidberg
for assistance in the field as well as D. Dann,M. Robart, and J.
Herum for help with deployments ofoceanographic instrumentation. J.
Fisher provided guidanceand feedback. This work was funded by
California SeaGrant (NA08AR4170669) and the National Science
Founda-tion (OCE-0927196 and OCE-0927255). K.J.N. was also
sup-ported by a Bodega Marine Laboratory Graduate
StudentFellowship.
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Editorial responsibility: Lisandro Benedetti-Cecchi, Pisa,
Italy
Submitted: March 28, 2013; Accepted: September 20, 2013Proofs
received from author(s): November 14, 2013
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