ICES Journal of Marine Science, 58: 1081–1091. 2001
doi:10.1006/jmsc.2001.1085, available online at http://www.idealibrary.com on
Physical influences on recruitment to California Current
invertebrate populations on multiple scales
Louis W. Botsford
Botsford, L. W. 2001. Physical influences on recruitment to California Current
invertebrate populations on multiple scales. – ICES Journal of Marine Science, 58:
1081–1091.
Studies of recruitment to Dungeness crab (Cancer magister) and red sea urchin
(Strongylocentrotus franciscanus) populations have focused on recruitment variability
on interannual, 1000-km scales. These studies have identified correlations between
recruitment and variables indicating ENSO conditions and wind-forced larval transport. On longer scales, our understanding of biologically important physical variability
in the California Current has recently been enhanced by an appreciation of semi-basin,
decadal changes. Intensification of the Aleutian low-pressure zone in the mid-1970s
had a clear positive effect of biological productivity in the Gulf of Alaska, and less
obvious negative effects on productivity in the California Current. On shorter scales,
an increasing appreciation of the effect of dispersal patterns on population dynamics
and the potential of spatially explicit management schemes provide the impetus for
studying processes such as alongshore spatial variability in recruitment and the
underlying daily variability in circulation over 100-km distances. In the 1980s, physical
studies of coastal circulation in response to daily fluctuations in upwelling winds
identified brief periods of northward, onshore flow interrupting the offshore, southward flows associated with active upwelling. In the 1990s, concurrent monitoring of
biological and physical conditions revealed that these flows transport late-stage
invertebrate larvae from a retention zone in the lee of a local promontory to settlement
locations, producing specific spatial patterns of recruitment. Variability in recruitment
of both crabs and sea urchins is thus driven by daily temporal variability in upwelling
winds and 100-km spatial variability in coastal topography. Interannual recruitment
variability appears to depend on ENSO-related biological productivity and larval
transport in ways that vary among species, but are not completely understood.
Observations are consistent with coastwide, interannual variability being driven by
biological productivity (i.e. ENSO/non-ENSO conditions), while the upwelling relaxation mechanism sets the spatial scale, and decadal, semi-basin variability modulates
the frequency of ENSO conditions.
2001 International Council for the Exploration of the Sea
Keywords: Dungeness crab, ENSO, marine reserves, red sea urchin, regime shift,
scales, settlement, upwelling relaxation.
Published electronically 23 July 2001.
Louis W. Botsford: Department of Wildlife, Fish, and Conservation Biology, University
of California, Davis, CA 95616, USA; e-mail: [email protected]
Introduction
There is a long-standing interest in variability in recruitment to two harvested invertebrates in central
California, the Dungeness crab (Cancer magister) and
the red sea urchin (Strongylocentrotus franciscanus).
After several decades of investigation of the approximately ten-year cycles in Dungeness crab, both densitydependent recruitment and interannual variability in
environmental conditions are thought to be involved,
but the causes of the cycles are not completely understood (Botsford et al., 1989, 1998). The fishery for the
1054–3139/01/051081+11 $35.00/0
red sea urchin in northern California developed in the
mid-1980s, peaked in 1988, and has declined each year
since then (Kalvass and Hendrick, 1997). While the
fishery began only recently, there is a long-standing,
general interest in sea urchin population dynamics
(Miller, 1985; Estes and Duggins, 1995), and the spatial
distribution of recruitment in a congener, the purple sea
urchin (Strongylocentrotus purpuratus), has been related
to mesoscale features of coastal circulation in the
California Current (Ebert and Russell, 1988). Both the
Dungeness crab and the red sea urchin fishery are
managed with minimum size limits and closed seasons.
2001 International Council for the Exploration of the Sea
1082
L. W. Botsford
Like most fisheries research, these efforts have focused
on interannual temporal scales and ‘‘population’’ spatial
scales, the scales of primary interest in harvested populations. However, interest in recruitment variability on
both larger and smaller scales has increased recently. At
longer time scales, recent identification of a shift in
physical and biological oceanographic conditions in the
Gulf of Alaska (Beamish and Bouillon, 1985; Brodeur
and Ware, 1992; McGowan et al., 1996; Miller et al.,
1998) has led to the question of how that may have
affected conditions in the California Current. A better
understanding of potential decadal shifts in recruitment
to California Current invertebrates is needed to adapt
stock assessment and management, and as a natural
baseline against which to compare potential effects of
overfishing and global change.
Interest in shorter temporal and smaller spatial scales
has been fuelled by recent appreciation of the role of
dispersal in both population dynamics and management.
The influence of physical oceanographic conditions on
transport and dispersal of larvae is as important to
recruitment as their influence on the production of larval
food. Moreover, the importance of larval transport lies
not just in its influence on the number recruited each
year, but also on the pathways travelled between population segments. Marine invertebrate populations are
neither isolated spatial subunits nor completely mixed,
but rather something in between, a metapopulation
consisting of more or less continuously distributed benthic subpopulations linked by larval dispersal (Botsford
et al., 1994, 1998; Fogarty, 1998). The spatial distribution of settling pre-recruits that results from the
larvae released at each location, i.e. the dispersal kernel
at each point along the coast, is important because: (1) it
may determine population stability and the spatial scale
of recruitment variability (Botsford et al., 1998), and (2)
the primary basis for setting harvest rates is to allow
adequate recruitment for sustainability, which requires
knowing the origins of that recruitment. Spatially
explicit management could take advantage of dispersal
information combined with benthic population dynamics to determine areas that are more or less likely to be
origins of larvae (sources and sinks; Pulliam, 1988), and
to vary harvest accordingly. Two forms of spatial management in which larval dispersal and other movement
within populations become more important are marine
reserves (Quinn et al., 1994; Botsford et al., 2001) and
rotating spatial harvest (Botsford et al., 1993).
Here I describe the way in which the physical environment influences dispersal and recruitment of two invertebrates on a range of spatial and temporal scales. I first
summarize the current understanding of physical forcing
of biological production in the California Current on
annual to decadal time scales and 1000-km to semi-basin
spatial scales. I then describe recent findings regarding the
effects of intra-annual, mesoscale variability in nearshore
circulation on late larval stages of meroplanktonic larvae
and their subsequent recruitment. The population dynamics of the invertebrates probably depend on both scales of
influence, in ways that we are just beginning to understand.
Physical/biological variability
Interest in variability in the strength of the equatorward
flow of the California Current and the potential biological effects of that variability has increased with identification of a regime shift in the Gulf of Alaska in the
mid-1970s (McClain 1986; McGowan et al., 1996;
Miller, 1996; Miller et al., 1998). Intensification and a
shift in the position of the Aleutian low pressure zone
led to intensification of the Alaska Coastal Current at
the expense of the California Current (Miller, 1996).
While the positive effects of that event on biological
productivity in the Gulf of Alaska are clear [e.g.
increased salmon catch (Beamish and Bouillon, 1992)
and chlorophyll (Venrick et al., 1987); possibly caused
by changes in mixed layer depth (Polovina et al., 1994,
1995)], the proposed inverse decline in productivity in
the California Current is less obvious.
On annual time scales, although the California
Current is an upwelling area, the observed inverse
covariability between temperature and zooplankton productivity has long been believed to depend in part on the
strength of the equatorward flow. Greater southward
flow was proposed to advect zooplankton directly (Reid,
1962), but Chelton et al. (1982) later proposed the flow
of nutrients from the north as the mechanism driving
primary and secondary productivity. Furthermore, they
proposed that this variation in north–south flow was due
to inverse fluctuations in the relative strengths of the
Alaskan Coastal Current and the California Current at
the point of bifurcation of the West Wind Drift in the
North Pacific (Figure 1; Chelton, 1986; Chelton and
Davis, 1982). The abundance of larval fish and the
abundance of zooplankton in the southern part of
the California Current are marginally correlated, as are
the strength of the north–south flow and the abundance
of larval fish (McGowan et al., 1996). While the mechanism is still not completely understood, the strength of
equatorward flow in the California Current underlies
biological variability on five to ten-year time scales,
termed the El Niño/Southern Oscillation (ENSO) scale.
There have been long-term, decadal-scale physical
changes in the California Current (Roemmich, 1992).
However, in the southern part there does not seem to
have been a decline in mass transport of water from the
north during the mid-1970s (McGowan et al., 1996),
indicating that long-term change may not mimic interannual variability (Chelton et al., 1982). Rather the
effects of long-term change at those latitudes appear to
be a deepening of the mixed layer, resulting in fewer
nutrients to the euphotic zone (McGowan et al., 1996;
Influences on recruitment to California Current invertebrate populations
Point Arena
Current
ACC
C3
WWD
40°N
140°W
CC
Point
Reyes
R3
Temperature
40
12.5
0
11.0
–40
40
9.5
12.5
0
11.0
–40
40
9.5
12.5
0
11.0
–40
cm/s
WIND
STRESS
C3
27
11
25
8
22
6
20
1982 13
APR APR MAY MAY JUN JUL JUL JUL
2 dyn/cm
N3
1083
9.5
°C
13
27
11
25
8
22
6
20
APR APR MAY MAY JUN JUL JUL JUL
Figure 1. The range of scales potentially influencing California Current invertebrate recruitment. The West Wind Drift (WWD)
divides into the Alaska Coastal Current (ACC) and the California Current (CC) in varying amounts on annual to decadal scales
(left panel). Drifter paths at three mooring locations (large dots; middle panel) indicate northward, onshore flow of warm water
during relaxation of upwelling winds on daily to weekly scales (shaded periods; right panels and graphs; after Davis, 1985 and Send
et al., 1987).
Miller, 1996). Although zooplankton productivity has
declined in southern California (Roemmich and
McGowan, 1995), there has not been a clear, sharp drop
in the mid-1970s. There is a marginal inverse correlation
between zooplankton productivity in the California
Current and the Alaska Coastal Current (Brodeur et al.,
1996). Comparison of temperature and salinity on the
central California coast indicated warmer, fresher water
after the mid-1970s than before, consistent with the
regime shift (Pennington and Chavez, 2000). This shift
also may have changed physical forcing of higher
trophic levels. For example, the significant positive
correlation between upwelling and ocean survival of
Oregon hatchery coho salmon (Nickelson, 1986) before
the mid-1970s disappeared in the years thereafter, when
coho salmon survival declined (Pearcy, 1997).
Physical conditions and biological populations in the
coastal zone are also influenced by interannual variability in the strength of coastal upwelling (Bailey, 1981;
Bakun, 1996). Understanding interannual variability in
biological productivity is confounded by the correlation
between ENSO conditions and upwelling index (years of
high temperature and sea level are typically years of low
upwelling and vice versa; e.g. Kope and Botsford, 1990).
Upwelling has also varied on decadal time scales. The
increase in differential heating between the ocean and
land as a consequence of global warming proposed by
Bakun (1990) has recently been identified in seasonal
temperature signals (Schwing and Mendelsohn, 1997).
Upwelling along the coast varies seasonally, being
strongest during April through August (Largier et al.,
1993), and in terms of spatial variability is several times
stronger in central California than to the north and
south (Parrish et al., 1981; Schwing and Mendelsohn,
1997). In fact, the potential for larval wastage caused by
offshore transport during strong upwelling in this area
has led to arguments for strong genetic selection against
producing meroplanktonic larvae during the upwelling
season (Parrish et al., 1981), though many species do.
At smaller scales, the mesoscale features evident in
satellite images of surface temperature along the US
west coast, apparently the result of strong upwelling
winds and irregular topography and bathymetry, have
received considerable attention by physical oceanographers. The Coastal Ocean Dynamics Experiment
(CODE) in the early 1980s, one of the few studies of
fine-scale, nearshore physical oceanographic variability
measured the response of nearshore circulation to daily
fluctuations in the upwelling winds over two years in the
area between Pt. Reyes and Pt. Arena (Figure 1). One of
the primary results, as regards transport of meroplanktonic larvae, was the observation that flows caused by
weekly variation in upwelling winds were threedimensional, with a significant alongshore component,
rather than two-dimensional in the cross-shelf dimension. During upwelling, the strength of offshore flow
varies along the coast, with an alongshore coastal jet
meandering and even separating from the coast and
flowing offshore at headlands such as Pt. Arena and
Pt. Reyes. During relaxations or slight reversals of the
winds, however, there was considerable poleward,
alongshore flow in response to sea level and density
differences, instead of a simple cross-shelf adjustment
(Figure 1). This relaxation current was evident in surface
temperature observations from both aircraft and
satellite, current meters and drifter data (Davis, 1985).
Mesoscale CTD data south of Pt. Arena identified
low salinity, poleward flowing water on the nearshore side of the CTD grid. The nearshore poleward
flow was also seen in shipborne Doppler current
profiler tracks (Kosro, 1987). Drifters released between
Pt. Reyes and Pt. Arena would flow south and offshore
L. W. Botsford
1992
2
1.5
1
0.5
0
–0.5
Local scales
Wing et al. (1995a,b) have attempted to determine the
impact of coastal circulation on invertebrate larvae by
monitoring collector settlement and concurrent coastal
winds, temperature, sea level, and salinity on daily–
Temperature
17
34
(b)
15
33.5
13
33
11
32.5
Temperature
Salinity
Settlement per
collector day
9
4
3
Salinity
Biological response of invertebrate populations
Population scales
Studies of the impact of physical oceanographic conditions on variability in Dungeness crab recruitment on
interannual temporal scales, and broad (100–1000 km)
spatial scales have revealed several instances of covariability between physical variables and crab catch at
lags that indicate an influence on the larval stage. The
correlations with upwelling index and with temperature
both could reflect a mechanism involving either food
production or cross-shelf transport (Botsford and
Wickham, 1975; Wild, 1980). As noted above, warm
water (ENSO) years imply lower primary and secondary
productivity, and less offshore transport. Other studies
focused specifically on transport. A positive relationship
between lagged catch and southward, onshore winds
identified by Johnson et al. (1986) was proposed to
reflect onshore transport of megalopae at the surface.
That hypothesis was supported by later correlations
between cross-shore larval distributions and onshore
movement estimated from the interaction between diel
vertical migration and observed winds (Hobbs et al.,
1992). In studies of both crab catch and settlement data
off Washington, McConnaughey et al. (1992, 1994)
identified positive correlations between southward flow
and recruitment. The mechanism proposed was that
larvae were swept northward in years of strong poleward
flow, beyond good settlement areas (cf. Botsford et al.,
1998).
There have been no similar studies of long-term
variability in red sea urchin recruitment. However, Ebert
and Russel (1988) showed that the coefficient of variation in size distributions of purple sea urchins increased
with distance south of a major promontory. The proposed mechanism was less frequent recruitment in areas
with greater offshore flow caused by higher upwelling
near promontories. On a broader spatial scale, monitoring of settlement on collectors in both northern (greater
upwelling) and southern California (less upwelling)
showed lower, more sporadic recruitment in the north
(Ebert et al., 1994).
(a)
32
(c)
Cancrid Crab Settlement
Non-cancrid Crab Settlement
2
1
0
120
127
134
141
148
155
162
169
176
183
190
197
204
211
218
225
during upwelling, but during relaxation would stall or
move northward (Davis, 1985; Send et al., 1987). There
was also an area north of Pt. Arena where drifters
moved toward shore during upwelling winds, indicating downwelling (Davis, 1985). These phenomena
have significant effects on larval retention and
dispersal.
Alongshore windstress
1084
Figure 2. Daily variations in (a) longshore windstress and (b)
temperature (solid line) and salinity (broken line) in relation to
(c) weekly variations in settlement on brush collectors at
Bodega Bay (near R3 in Figure 1) in 1992 (solid line, cancrid
crab settlement; broken line, non-cancrid crab settlement) (after
Wing et al., 1995a).
weekly time scales. North of Pt. Reyes, these physical
variables vary predominantly as expected from weekly
variability in upwelling winds (Figure 2). During strong,
alongshore winds, temperature and sea level are low and
salinity is high. When upwelling winds decline or
reverse, these variables change in the opposite direction.
Surface temperatures from satellite data (AVHRR) indicated these relaxations involved alongshore flow as
identified during the CODE study (Figure 1; Send et al.,
1987).
In 1992 and 1993, the high correlation between site
temperature and settlement of crabs (primarily Cancer
species) to the north of Pt. Reyes indicated that settlement occurred primarily during relaxation events when
warmer water flowed northward along the coast (Wing
et al., 1995a,b). The low correlation at sites to the south
indicated less dependence of settlement on relaxation
events (Figure 3). This mechanism led to a specific
spatial distribution of annual crab settlement along the
coast in 1993 and 1994. Settlement to the south, where
warmer, presumably larvae-rich waters were present
more often, was higher than to the north, where warmer
waters intruded only during occasional relaxation events
(Wing et al., 1995b).
Influences on recruitment to California Current invertebrate populations
1085
Cancer crabs
1993
39°N
1994
Correlations
Site Temperature
vs.
Total crab Cancer spp.
Point
Arena
Salt Point
Bodega Bay
38°
Point Reyes
Duxbury Reef
San Francisco
3.0
1.5
0
1.0
0.5
0.655*
0.667*
0.650*
0.622*
–0.062
0.477
0.349
0.417
0
No./Collector-day
Figure 3. Settlement patterns of Cancer spp. from brush collectors in shallow waters along the California coast and correlations
between local temperature and settlement of all crabs and of Cancer spp. (after Wing et al., 1995b).
Neuston and subsurface plankton samples taken during upwelling revealed the highest concentrations of
megalopae and zoeae in the area to the south and in the
lee of Pt. Reyes (Figure 4). This suggests that this area
is the likely source of the crab larvae distributed along
the coast during relaxation (Wing et al., 1998). Some
AVHRR satellite images of surface temperature indicate
cyclonic circulation into the lee of Pt. Reyes (Wing et al.,
1995b). Larvae appear to be retained in this feature
south of Pt. Reyes during upwelling, and transported
poleward during relaxation.
Settlement of sea urchins on collectors during 1992
and 1993 was not as predictable (Wing et al., 1995a,b).
While sea urchins did not settle frequently enough to
detect a temporal response to relaxation, the spatial
distribution of recent recruitment reflected in size distributions along the coast matched the pattern expected on
the basis of our understanding of coastal circulation
from the settlement studies (Morgan et al., 2000). A
recruitment index (ratio of recent recruitment to the
abundance of unfished adults) exhibits a pattern of high
settlement just north of Pt. Reyes and just north of Pt.
Arena, with low settlement in between (Figure 5). High
settlement at the southern end and low settlement in
the middle of the region would be expected because the
mid-region would be less frequently reached by the
relaxation current (Send et al., 1987; Wing et al., 1995b).
The immediate origin of the larvae settling on the
southern end is presumably the retention zone in the lee
of Pt. Reyes. High settlement to the north of Pt. Arena
with low settlement to the south would be projected on
the basis of the CODE results described above. During
relaxation, the area immediately to the south of Pt.
Arena showed cooler surface temperatures than areas
further south and areas offshore (Huyer and Kosro,
1987). To the north, drifter data show onshore flow even
during upwelling. The retention zone in this case is
presumed to be a persistent, anticyclonic eddy south and
offshore of Pt. Arena during the upwelling season
(Washburn et al., 1993). Satellite surface temperatures
show warm offshore waters impacting the coast north of
Pt. Arena, in the areas reflecting high recent settlement
(Morgan et al., 2000).
The recruitment index provides stronger evidence for
population effects than settlement collector data because
it reflects actual recruitment to the population, not just
competent larvae available for settlement. However, the
index may also be influenced by post-settlement processes in addition to transport. A test of the only known
post-settlement influence on recruitment (reduced mortality of juveniles beneath the spine canopies of adults;
Tegner and Dayton, 1977) showed that the availability
of adult spine canopies did not explain the spatial
pattern in recruitment (Morgan et al., 2000).
Longer scales
At this point, settlement has been sampled for enough
years (eight) in Bodega Bay (Figure 3) for us to begin to
see interannual variability in this mechanism (Lundquist
et al., 2000). Physical variability is not consistent from
year to year: daily temperature and wind remain correlated over all years, but temperature and salinity do not
always show the inverse correlation expected from
upwelling/relaxation variability. Temperature and
weekly settlement are not correlated in all years, as
they were in 1992 and 1993, and they tend not to be
1086
L. W. Botsford
38.4°N
Discussion
(a)
Oceanic
Upwelled
cold
38.2
Latitude
Frontal
200.0
38.0
100.0
37.8
Upwelled
warm
37.6
Oceanic
Frontal
37.4
38.4°N
(b)
Oceanic
Upwelled
cold
38.2
Frontal
Latitude
0.0
Density
200.0
38.0
100.0
37.8
Upwelled
warm
37.6
Oceanic
Frontal
37.4
124.0°W
0.0
Density
123.5
123.0
Longitude
Figure 4. An example of the planktonic distribution of megalopae (a) and zoeae (b) of Cancrid crabs during upwelling at the
sites near Pt. Reyes in relation to various water masses (18–22
June 1994; from Wing et al., 1998).
correlated when temperature and salinity are not correlated. Also, weekly settlement of non-cancrid crabs is
rarely correlated with temperature, primarily because
their settlement period is too short to be driven by that
variability. Interannual variability in total annual
settlement is positively correlated with ENSO conditions
(less wind) for cancrid crabs at this location [Figure
6(a)], but negatively correlated with ENSO conditions
(higher temperatures) for non-cancrid crabs [Figure
6(b)]. The single exception to the latter is 1999, when the
upwelling index at this location was the highest on
record and settlement was exceptionally low (Lundquist
et al., 2000). Annual settlement of cancrid crabs in
Bodega Bay appears to depend on upwelling winds
being low enough that daily scale relaxations are possible and frequent, while annual settlement of noncancrid crabs appears to depend on non-ENSO
conditions associated with greater productivity.
Studies of physical influences on invertebrate recruitment at daily–weekly time scales and 100-km spatial
scales have improved our understanding of population
dynamics in the California Current system. We now
understand how these populations are able to persist
with larvae in the plankton during the upwelling season,
in spite of strong offshore, equatorward flows. Larvae
can be retained in retention features associated with
major promontories such as Pt. Reyes (Wing et al.,
1998). A similar occurrence of warmer, fresher water
with higher zooplankton concentrations inshore of
recently upwelled water has been observed 200 km to the
south, and they have been termed ‘‘upwelling shadows’’
(Graham et al., 1992; Graham and Largier, 1997). Also,
larval dispersal patterns can be inferred from this mechanism. Retention near promontories and poleward
transport during upwelling relaxation may create semiindependent upwelling ‘‘cells’’ in the regions between
major promontories. This would lead to a dispersal scale
set by topography and bathymetry on the order of 100s
of kilometers. This spatial scale shows up in covariability in catch along the coast, as predicted in
metapopulation modeling studies (Botsford et al., 1998).
Within each cell there will be greater recruitment just
north of promontories than further north because of
transport in relaxation flows (i.e. as in Figures 3 and 5).
Interpretation of interannual variability in settlement
is difficult because of the paradoxical effects of
upwelling: organsims benefit from upwelling for food
production, but too much upwelling has a negative effect
because of transport offshore, beyond good settlement
habitat. These mechanisms may lead to the domeshaped dependence on wind (cf. ‘‘optimal environmental
window’’; Cury and Roy, 1989; Gargett, 1997) seen in
non-cancrid crabs here, and also in some rockfishes
(Ralston and Howard, 1995; Yoklavich et al., 1996).
With regard to the Dungeness crab, we do not have a
convincing explanation for the coastwide cycles in abundance, and there is still uncertainty regarding physical
forcing mechanisms (Botsford et al., 1998). ENSO conditions appear to control coastwide, interannual variability, while local wind conditions set the spatial scale of
recruitment variability; non-ENSO conditions produce
high coastwide abundance, but low wind conditions are
required for transport to specific locations north of
promontories (e.g. Bodega Bay). While the potential
spatial scale of dispersal (such as the width of the
embayment from Pt. Reyes to Pt. Arena) may be investigated by computing the alongshore correlation scale in
the cycles (Botsford et al., 1998), conclusions regarding
the influence of the upwelling/relaxation mechanism on
population dynamics are limited in that it controls only
the last phase of dispersal, albeit the most important
one. Important physical influences might occur during
Influences on recruitment to California Current invertebrate populations
1087
Red sea urchin
1995–1996
39°N
Point
Arena
38°
Point Reyes
2.0
1.0
0
Recruitment index
Figure 5. The spatial distribution of the index of recent recruitment of red sea urchins based on size distributions collected in 1995
and 1996 (after Morgan et al., 2000).
the first three months of larval life, during which larvae
are distributed as far as 400 km offshore, far beyond the
influence of coastal circulation. Numerical evaluation of
influences during earlier stages, such as the variability in
timing of the spring transition and temperaturedependent development, indicates that these may have
substantial effects (Moloney et al., 1994).
Cancrid crab settlement
2.5
(a)
2.0
1998
1993
1.5
1996
1.0
1992
1995 1994
1997
0.5
1999
0.0
0.04
0.06
0.08
0.10
0.12
0.14
0.16
Non-cancrid crab settlement
Log10 (windstress + 1)
1.8
1994
1.6 (b)
1.4
1.2
1.0
1996
0.8
1998
0.6
1993
1997
1992
0.4
1995
0.2
1999
0.0
9.5 10.0 10.5 11.0 11.5 12.0 12.5 13.0 13.5
Temperature
Figure 6. Dependence of indices of total annual settlement of
(a) Cancrid and (b) non-Cancrid crabs in Bodega Bay on
interannual variability in windstress and temperature, respectively (after Lundquist et al., 2000).
The results obtained for the red sea urchin provide a
mechanism that explains Ebert and Russell’s (1988)
earlier observations of the dependence of recruitment
variability of the purple sea urchin on coastal topography. On the other hand, the data give us a much more
stochastic view with greater variability from year to
year. The pattern of recent recruitment (Figure 5)
cannot reflect an annually recurring pattern, if these
populations are driven by recruitment without postrecruitment density dependence, because different but
constant settlement rates at each location would merely
imply identical size distributions at different densities.
However, if there is density-dependence in the older
age classes, we would not see an influence of past
recruitment on the size structure. Additional years of
sampling will be required to confidently describe the
stochastic mechanisms of spatio-temporal variability in
recruitment to this species.
A more complete understanding of recruitment variation in these invertebrate stocks will require insight into
the relationship between the variability on intra-annual,
100-km scales and variability on annual and longer time
scales. At present, there are two major impediments to
that understanding: (1) biological and physical conditions have not been sampled at fine scales for long
enough, or over large enough areas; and (2) the links
between the interannual large-scale (e.g. strength of the
California Current) and the nearshore mesoscale physical variability on weekly time scales (e.g. alongshore
flow during upwelling relaxation) are insufficiently
known. Eight years of settlement information at one site
provides just a start to examining interannual variability
in settlement patterns. However, those years are
restricted to the period after the broad-scale regime shift
that occurred in the mid-1970s, which limits our understanding over larger time scales. Also, while we have
interpreted interannual variability in settlement in terms
1088
L. W. Botsford
of ENSO conditions in the California Current, ENSO
variability depends on varying combinations of remote
oceanographic forcing and indirect wind-forcing
through an atmospheric teleconnection (Norton and
McLain, 1994; Bakun, 1996) in ways that are not
understood. The first two years of our series (1992
and 1993) were mild ENSO years (Lynn et al., 1995;
Trenbreth and Hoar, 1995), with locally elevated
temperatures, depressed salinities, negative upwelling
anomalies, and anomalous poleward and onshore advection, which affected the distribution of some fish and
invertebrates (Lenarz et al., 1995; Sakuma and Ralston,
1995). The phytoplankton bloom in the coastal area was
diminished and delayed. Stronger ENSO conditions
prevailed in 1997 and 1998 with the latter year having
extremely low winds. In the next year (1999), there were
the strongest upwelling winds ever recorded at this site.
Other examples of the influence of nearshore coastal
circulation on recruitment and productivity support the
growing appreciation of the importance of physical/
biological interactions on a range of scales. Barnacle
larvae settle primarily during upwelling relaxation
events involving the cross-shelf movement of the
upwelling front and the larvae (Farrell et al., 1991;
Roughgarden et al., 1991). Further north, off Oregon,
monitoring of red and purple sea urchin settlement has
indicated a dependence on relaxation of upwelling winds
with an alongshore component similar to that described
here (Miller and Emlet, 1997). At another location in
Oregon, comparison of nearshore sites characterized by
different widths of the continental shelf, where different
responses of coastal flows to upwelling relaxation might
be expected, has revealed higher chlorophyll concentrations where the shelf is broader (Menge et al., 1998),
and a response of daily growth rate of the mussel
(Mytilus edulis) to the daily variability in upwelling
relaxation (Dahlhoff and Menge, 1996). Connolly and
Roughgarden (1999) noted that settlement of intertidal
barnacles was lower during the ENSO year 1997 than
in 1996.
These recruitment studies appear to reflect a global
trend toward greater emphasis on the mechanisms
underlying effects of physical conditions. Comparing the
topics addressed in earlier ICES symposia to those
addressed in this symposium, there appears to be an
evolving shift from emphasis on the effects of stock
abundance on recruitment to greater interest in physical
influences. In the last symposium on recruitment
(Parrish, 1973), most papers focused on the dependence
of recruitment on adult abundance, and few mentioned
environmental variability. A later symposium on the
biological effects of ocean variability contained most of
the themes of current topical interest (Parsons et al.,
1978). Notably, one of the papers focused on the
biological oceanographic effects of climate change
(Cushing, 1978). There was also a nascent appreciation
for the importance of considering variability on different
time and space scales (Smith, 1978), as well as the
importance of linking different scales (Walsh, 1978). A
parallel symposium on Oceanography and Fisheries
included a description of El Niño forcing of the
anchoveta fishery in the Humboldt Current (Valdivia,
1978) and the dependence of anchovy feeding on event
scale variability in upwelling winds (Lasker, 1978).
To summarize our current view on recruitment to
California Current invertebrate populations, recent
advances in our understanding of the way in which
nearshore circulation affects larval transport and recruitment on weekly time scales and 100-km spatial scales
have the potential to improve our understanding of
interannual, population-scale variability if we know how
they are affected by physical variability on decadal time
scales and basin spatial scales. Decadal-scale variability
underlies a lack of stationarity that interferes with
prediction on annual time scales, while identification of
the mechanisms underlying the shorter-term variability
may provide the mechanistic basis for explanation of the
observed annual variability. In addition, knowing these
mechanisms and the consequent dispersal patterns
provides the basis for understanding metapopulation
structure and employing spatially explicit management.
Acknowledgements
This work was supported by the US GLOBEC Northeast Pacific program of the NSF and NOAA under
OCE-9711448. I thank Andy Bakun, Lance Morgan,
Vera Agostini, and Cathy Lawrence for comments on
the manuscript. This paper about webs and scales is
dedicated to the memory of Mike Mullin.
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