Assessing the importance of land and ocean subsidies to giant kelp
forests
Daniel C. Reed, Jenifer E. Dugan, Edward Beighley, Mark Brzezinski, Scott D. Cooper,
Steven D. Gaines, Sally J. Holbrook, Patricia J. Holden, Al Leydecker, John M. Melack,
Henry M. Page, Josh P. Schimel, Erika McPhee Shaw, David A. Siegel, and Libe
Washburn
Daniel C. Reed, Research Biologist and lead Principal Investigator of SBC LTER,
Marine Science Institute, University of California, Santa Barbara CA 93106 USA,
(reed@lifesci.ucsb.edu). Jenifer E. Dugan, Associate Research Biologist, Marine Science
Institute, University of California, Santa Barbara, CA 93106 USA,
(j_dugan@lifesci.ucsb.edu). Edward Beighley, Postdoctoral Scientist, Marine Science
Institute, University of California, Santa Barbara, CA 93106 USA,
(beighley@icess.ucsb.edu). Mark Brzezinski, Professor of Biological Oceanography,
Department of Ecology, Evolution, and Marine Biology, University of California, Santa
Barbara, CA 93106 USA, (brezezins@lifesci.ucsb.edu). Scott D. Cooper, Professor of
Ecology, Department of Ecology, Evolution, and Marine Biology, University of
California, Santa Barbara, CA 93106 USA, (scooper@lifesci.ucsb.edu). Steven D.
Gaines, Professor of Ecology, Department of Ecology, Evolution, and Marine Biology,
University of California, Santa Barbara, CA 93106 USA, (gaines@lifesci.ucsb.edu). Sally
J. Holbrook, Professor of Ecology, Department of Ecology, Evolution, and Marine
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Biology, University of California, Santa Barbara, CA 93106 USA,
(holbrook@lifesci.ucsb.edu), Patricia J. Holden, Associate Professor of Environmental
Microbiology, Donald Bren School of Environmental Science and Management,
University of California, Santa Barbara, CA 93106 USA, (holden@bren.ucsb.edu). Al
Leydecker, Postdoctoral Scientist, Marine Science Institute, University of California,
Santa Barbara CA 93106 USA, (al.leydecker@cox.net). John M. Melack, Professor of
Hydrology and Limnology, Department of Ecology, Evolution, and Marine Biology and
the Donald Bren School of Environmental Science and Management, University of
California, Santa Barbara CA 93106 USA, (melack@lifesci.ucsb.edu). Henry M. Page,
Associate Research Biologist, Marine Science Institute, University of California, Santa
Barbara, CA 93106 USA, (page@lifesci.ucsb.edu). Josh P. Schimel, Professor of Soil
Ecology, Department of Ecology, Evolution, and Marine Biology, University of
California, Santa Barbara, CA 93106 USA, (schimel@lifesci.ucsb.edu). Erika McPhee
Shaw, Postdoctoral Scientist, Marine Science Institute, University of California, Santa
Barbara, CA 93106 USA, (eeshaw@nps.navy.mil). David A. Siegel, Professor of
Oceanography, Department of Geography, University of California, Santa Barbara, CA
93106 USA, (davey@icess.ucsb.edu). Libe Washburn, Professor of Physical
Oceanography, Department of Geography, University of California, Santa Barbara, CA
93106 USA, (washburn@icess.ucsb.edu).
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Abstract
Few ecosystems exist in isolation, and the exchange of material across their
borders can strongly influence their structure and function. Such is the case for giant kelp
forests, a highly diverse and productive marine ecosystem that occurs on shallow reefs
near the land-ocean margin along open coasts in many temperate regions of the world.
Carbon and nitrogen subsides enter the kelp forest via a variety of land and
oceanographic processes (e.g., stream runoff, ocean currents, coastal upwelling). Here
we present findings from the Santa Barbara Coastal Long Term Ecological Research
project in southern California, USA on the delivery of land and ocean-derived sources of
carbon and nitrogen to giant kelp forest food webs. We emphasize the extent to which
material subsidies to the kelp forest can be influenced by variable terrestrial, oceanic and
atmospheric forcing that alters the supply and character of internally derived and
externally supplied resources.
Keywords: food web, giant kelp forests, nitrogen, particulate organic matter, runoff,
subsidy
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Material exchange between ecosystems is being recognized increasingly as an
important determinant of many ecological patterns and processes (Valiela et al. 2001,
Loreau et al. 2003). The movement of organic and inorganic materials across the
boundaries of discrete ecosystems is ubiquitous and has been shown to profoundly
influence population dynamics, community structure, food web complexity, and primary
and secondary production (reviewed in Polis et al. 1997). Nowhere are such material
subsidies more evident than in the coastal zone where nearshore marine ecosystems
frequently experience large inputs from both the land and the sea.
The influence of terrestrial subsidies to coastal ecosystems has been well
documented at both tropical and temperate latitudes. Atmospheric transport of dust from
deserts and ash from wildfires has been linked with increases in marine primary
production in both nearshore and offshore waters (Abram et al. 2003, Garrison et al.
2003), and the atmospheric deposition of nitrogen near urban and agricultural areas to
coastal waters has been well described (Paerl et al. 2002). The seepage of groundwater
from terrestrial aquifers into the sea is now recognized as a potential source of dissolved
material subsidies to shallow marine habitats, and approaches for more accurately
measuring these fluxes are being developed and tested (e.g., Valiela et al. 2001, Burnett
et al. 2001). Even more obvious is the delivery of sediments, detritus, dissolved
nutrients, and pollutants to nearshore waters by streams and rivers that receive runoff
from coastal catchments.
The effects of runoff from land on coastal marine ecosystems are numerous and
dose dependent. Runoff from land in many regions of the world can result in enhanced
nutrients that stimulate algal blooms and subsequent oxygen depletion (Signorini et al.
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1999, Rabalais et al. 2002, Otero and Siegel in press), altered salinities which affect
species composition and abundance (Smith and Witman 1999), and the siltation or
eutrophication of shallow marine habitats (Wesseling et al. 1999, Lenihan et al. 2001,
McLaughlin et al. 2003). Climatic change that affects the amount and intensity of
precipitation has noticeable effects on discharge rates and the hydrographic
characteristics of runoff from coastal watersheds (Inman and Jenkins 1999).
Additionally, widespread changes in land use can greatly influence the chemical
characteristics, flow rates, and frequency and amount of runoff delivered by streams to
the coastal ocean (Beighley et al. 2003, Smith et al. 2003, Turner and Rabalais 2003).
Oceanographic processes (e.g., currents, waves, upwelling) can also greatly affect
material inputs to nearshore marine ecosystems (e.g., Leichter et al. 2003). These
processes vary on tidal, seasonal, interannual and decadal time scales and across a wide
range of spatial scales. Much of what we know about the role of material exchange in
influencing nearshore coastal ecosystems has come from studies of large protected
embayments (e.g. San Francisco Bay and Chesapeake Bay) or large river systems (e.g.
Mississippi and Amazon Rivers) where the effects of ocean forcing and oceanic inputs
are muted or masked. Such habitats contrast greatly with open coastal systems such as
shallow reefs, which experience a much wider range of oceanographic conditions and
greater ocean-derived inputs. Shallow reefs frequently support dense populations of
habitat-forming species (e.g., kelps and reef building corals), which provide structure and
food for a high diversity of organisms, many of which are ecologically and economically
important. The ways in which the species assemblage and ecological function of reef
5
ecosystems are altered by inputs from land and offshore waters are likely to be numerous,
yet at present both the underlying mechanisms and their effects are poorly understood.
A new long term study of the roles of land and ocean subsidies to an open coastal
ecosystem
In recognition of the importance of integrated long-term studies of the roles of
land and ocean subsidies in coastal ecosystems, the United States National Science
Foundation established three new Long Term Ecological Research (LTER) sites in 2000
that focus on ecosystems at the land/ocean margin: the Florida coastal Everglade system,
a coastal marsh complex in Georgia, and a giant kelp forest ecosystem on shallow reefs in
southern California. Here we present an overview of our studies of the importance of
land and ocean subsidies to giant kelp forest ecosystems as part of the Santa Barbara
Coastal LTER program in southern California, which is the only LTER site that examines
material exchange between the land and the sea in an open coastal ecosystem.
The primary research focus of the Santa Barbara Coastal (SBC) LTER is on the
relative importance of bottom-up processes (driven by primary production) and external
inputs (i.e., subsidies) to giant kelp (Macrocystis spp.) forests, a highly diverse and
productive marine ecosystem that occurs on shallow rocky reefs along the land-ocean
margin on the temperate coasts of western North and South America, southern Africa,
Australia and most sub Antarctic islands, including Tasmania and New Zealand (Foster
and Schiel 1985). Because of their close proximity to shore, giant kelp forests are
influenced by physical and biological processes that occur on the land as well as in the
open ocean. Streams and rivers transport nutrients, dissolved and particulate organic
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matter (DOM and POM), sediments, and pollutants from coastal watersheds to kelp
forests, while ocean currents and other advective processes supply nutrients, DOM,
POM, larvae and plankton from adjacent offshore waters (Figure 1). In return, kelp
forests export large amounts of DOM and POM to inshore intertidal habitats, as well as to
offshore deep-water habitats (ZoBell 1971, Newell et al. 1980, Harrold et al. 1998).
Short and long-term changes in climate that alter rainfall, ocean currents, and waves may
cause a change in the relative importance of land and ocean processes in supplying
nutrients, sediments, and organic matter to kelp forest communities, which in turn can
influence the amount of organic materials exported from kelp forests to intertidal and
offshore habitats.
One of the major hypotheses underlying many of the research activities at the
Santa Barbara Coastal LTER is that the productivity, community structure, and food web
dynamics of giant kelp forests are driven by variable terrestrial, oceanic and atmospheric
forcing that alters the supply and character of internally derived and externally supplied
resources. Of particular interest in this regard is the relative importance of land and
ocean-derived sources of carbon and nitrogen to kelp forest food webs, and the extent to
which they are affected by changes in freshwater runoff and oceanic conditions. Longterm monitoring of a wide variety of state variables and ecological responses produce
information on the patterns and rates of material exchange, and their effects on kelp
forest community structure and ecosystem function (Table 1). Short and long-term
experiments are delineating the mechanisms that cause the ecological responses observed
in time series measurements. Lastly, the modeling of physical and biological processes
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extends our measurements to larger temporal and spatial scales, aids in predicting
responses to environmental change, and provides direction for future research.
Characteristics of the Santa Barbara Channel
There are several reasons why the Santa Barbara Channel is an ideal area for
investigating how variability in environmental forcing alters material flow to influence
the productivity, community structure and food web dynamics of giant kelp forest
ecosystems. First, unlike areas to the north, surface waters in this region tend to be
warm, saline, and nutrient-poor for much of the year. Consequently, nutrient subsidies
from land have the potential to enhance substantially the productivity of kelp forests.
Second, the Santa Barbara Channel is a site of dramatic physical and biological changes
related to El Niño Southern Oscillations (ENSO), which occur irregularly every three to
seven years. Terrestrial runoff and the associated transport of sediments, nutrients, and
pollutants increase because precipitation tends to be higher during El Niño events (77%
of the El Niño years between 1955 and 2003 had rainfall levels greater than the mean for
this period, compared with 25% for non-El Niño years; Figure 2a). El Niño events also
are characterized by elevated sea surface temperatures and decreased nutrient levels
engendered by a deepening of the thermocline (66% of the El Niño years between 1955
and 2000 had sea surface temperatures greater than the mean for this period, compared
with 38% for non-El Niño years; Figure 2b). Large-scale patterns of ocean circulation
also change during El Niño years, and storm disturbance from waves is often great
(Ebeling et al. 1985). Corresponding to these physical changes are numerous biotic
changes including precipitous declines in the giant kelp Macrocystis pyrifera (note the
8
disappearance of giant kelp following the large El Niño associated storms of 1969, 1983,
1998, Figure 2c), northward range extensions for many southern species, and unusual
changes in the abundance of many species of algae, invertebrates and fish (Tegner and
Dayton 1987, Dayton and Tegner 1989).
Third, catchments draining into the Santa Barbara Channel offer a rich diversity
of watersheds for experimental and observational study, typifying the types of watersheds
and land uses found in most Mediterranean climates (Figure 3). About 50 catchments
drain into the Santa Barbara Channel from the coastal Santa Ynez Mountains. Stream
runoff enters the ocean directly or through small estuaries that have little capacity to
buffer peak flows. Steep montane slopes composed of readily eroded material and
strongly seasonal rainfall produce large amounts of sediments in streams (Inman and
Jenkins 1999, Warrick and Milliman 2003). The intermittent occurrence of fire in the
catchments further enhances temporal variation in the export of sediments and nutrients
to the ocean (Florsheim et al. 1991, Keller et al. 1997). The catchments of the Santa
Barbara region vary widely in the extent of agricultural and urban development, which
has large effects on the concentrations of nutrients and pollutants in runoff.
Modifications in the frequency or intensity of droughts due to climate change or ENSO
events also will be strongly expressed in the Mediterranean climate of this region.
Hence, spatial and temporal variation in climatic and landscape conditions in coastal
catchments provides an excellent opportunity to assess the diverse effects of terrestrial
inputs on a shallow marine ecosystem (giant kelp forests).
Finally, Pt. Conception, at the western extent of the Santa Barbara Channel
(Figure 3), is a major biogeographic boundary for a wide variety of marine taxa
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(Valentine 1966, Briggs 1974). The intersection of cool southward flowing water from
the California Current with relatively warm northward flowing water in the California
Countercurrent produces one of the highest numbers of species boundaries for any single
location along the Pacific coast of the continental United States (Airame et al. 2003).
Areas adjacent to this boundary may be particularly sensitive to shifts in species
composition driven by climate change. The Santa Barbara Coastal LTER site abuts this
sharp transition zone, offering the opportunity to study the short- and long-term dynamics
of a boundary between distinct biogeographic provinces.
Kelp forest food webs and sources of material inputs
Giant kelp forest communities are characterized by a trophic structure that is rare
outside shallow reef ecosystems in that competition occurs between different trophic
levels (Figure 4). Macroalgae, which derive their nutrition from sunlight and dissolved
nutrients, are the resident primary producers in kelp forests. They compete for space on
the reef with sessile invertebrates, which obtain their nutrition by filtering plankton and
other POM from water flowing over the reef. Dissolved nutrients can be taken up by
macroalgae directly or they can enter the reef food web indirectly through phytoplankton
that is consumed by sessile invertebrates. Nutrients consumed by one type of primary
producer (e.g., phytoplankton) will be unavailable to the other (e.g., macroalgae). Thus,
competition between macroalgae and sessile invertebrates for space on the reef can be
mediated by the delivery of nutrients and/or POM. Substantial changes in the relative
supply of these resources due to variation in runoff and oceanographic processes have the
potential to significantly alter kelp forest communities. As a consequence, processes that
10
favor one trophic pathway over another could have large effects on the structure and
function of giant kelp forest ecosystems.
As noted above, sources of primary production to kelp forest food webs in
southern California include macroalgae produced on the reef (of which giant kelp is the
largest contributor), phytoplankton produced offshore and advected to the reef via ocean
currents, and terrestrial plant material delivered to the reef as POM in freshwater runoff.
The relative availability of these different sources of production to kelp forest consumers
undoubtedly varies in response to predictable (e.g. runoff, currents, waves) and
unpredictable (e.g., episodes of intensive grazing on giant kelp) events. Stable isotopes
of carbon (expressed as 13C in o/oo) and nitrogen (expressed as 15N in o/oo) in
producers and consumers have proven useful in studies of kelp forest food webs
(Duggins et al. 1989, Fredrikson 2003), and offers a promising means of examining
linkages between kelp forests and neighboring land and offshore marine ecosystems in
the Santa Barbara Channel.
The application of stable isotope analysis for identifying the sources of organic
matter fueling food webs can be constrained if values of the different food sources
overlap, or if they vary substantially in time and space. Data collected by SBC LTER
researchers suggest that the mean 13C value for offshore POM (primarily
phytoplankton), is reasonably distinct from mean values of giant kelp and coralline algae,
two of the most abundant macroalgae growing on reefs in the Santa Barbara Channel
(Figure 5). Furthermore, 13C values of POM in streams sampled during runoff events
are quite different than those of the most important marine-derived sources of production.
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The similarity of 13C values in marine producers and common reef consumers
observed during 2002 suggested that the incorporation of marine rather than terrestrial
sources of carbon dominated the reef food web (Figure 5). Such a large marine influence
is not surprising given that 2002 was characterized by very low levels of rainfall and
runoff (Figure 2a). Isotope values of kelp forest consumers suggests that the suspensionfeeders, Styela montereyensis (a solitary tunicate) and Megabalanus californicus (a
barnacle), use a mix of both offshore POM and macroalgae, whereas the sea urchin
Strongylocentrotus purpuratus, a benthic grazer, appears to use primarily macroalgae
(e.g. giant kelp and coralline algae) (Figure 5).
Our results to date suggest that long-term measurements of the isotopic
composition of producers and consumers on SBC LTER reefs that vary in the standing
crop of giant kelp and other algae, and exposure to freshwater runoff, will provide much
needed insight into the degree to which predictable and unpredictable events affect the
contribution of land-, ocean- and reef-derived sources of organic matter to giant kelp
forest food webs. Data on stream discharge, the abundance of phytoplankton,
macroalgae and stream detritus, the population sizes and dynamics of kelp forest
invertebrates and fish, and the turnover times of stable isotopes in reef consumers are
being collected routinely at numerous SBC LTER sites (Table 1), and will aid in the
interpretation of stable isotope values.
Mechanisms and rates of nitrogen transport to giant kelp forests
The transport of nitrate into the euphotic zone is arguably the single most
important factor regulating the standing crop and production of phytoplankton and
12
macroalgae (including giant kelp) in the coastal waters of southern California (Jackson
1977, Haines and Wheeler 1978, Eppley et al. 1979, Wheeler and North 1980). As a
consequence, external inputs of nitrogen to shallow reefs originating from land and
deeper offshore waters may strongly influence the productivity and food web structure of
giant kelp forest ecosystems in southern California. Identifying the modes and rates of
nitrogen delivery to kelp forests is key to understanding spatial and temporal patterns of
kelp forest structure and function.
Nitrate is the most abundant form of dissolved inorganic nitrogen in the ocean and
its concentration in waters off southern California is uniformly low at water temperatures
above 15.5 oC, and inversely related to temperatures below 15.5 oC (Jackson 1977,
Zimmerman and Kremer 1984). Seasonal variation in nitrate concentration on shallow
reefs is dominated by oceanic conditions in the adjacent basins of the Southern California
Bight. During winter, storm winds, coupled with a weak thermocline, mix surface and
deeper waters to maintain high nutrient concentrations near the surface. In contrast,
weaker winds and a stronger thermocline typically prevail in the summer, resulting in less
mixing, which can cause nitrate limitation for primary producers in surface waters.
These seasonal patterns in nutrient dynamics are punctuated by other mechanisms of
nitrate delivery that operate over time scales ranging from a few hours to several days.
Below we describe these mechanisms of nitrogen transport and discuss temporal and
spatial variation in their rates of nitrogen delivery to shallow reefs in the Santa Barbara
Channel.
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Wind-driven upwelling
The highest concentrations of nitrate in near surface waters of the Santa Barbara
Channel occur during episodic events of local upwelling. Strong westerly winds cause
warm surface waters along the mainland coast to move southward and be replaced by
deep, cold (< 12 oC), high salinity, nutrient-rich water. Such periods occur most
commonly in spring (March through May), typically last four to six days, and elevate
nitrate concentrations above 15 μmol L-1 (Figure 6a). The number of upwelling events
varies greatly from year to year, and nitrate concentrations in upwelled water can vary
depending on the depth of the thermocline. Upwelling occurs over broad stretches of the
Santa Barbara Channel with local variations due to coastal topography. One such
example occurs along the mainland coast of the Channel just east of Pt. Conception
(Figure 3). The abrupt change in the orientation of the coastline in this region promotes
strong offshore winds (Klimczak and Dorman 2000). Our analyses of data on surface
currents suggest that these winds produce strong offshore flow and upwelling near the
coast (L. Washburn and E. McPhee-Shaw, unpublished data).
Other less conspicuous processes also appear to transport deep water from
offshore to kelp forests. One such process recently discovered as part of our LTER
research involves small eddy-like features that reverse flow near shore and appear to
bring colder, high nitrate waters onto the reefs from deep offshore. The characteristics
and dynamics of this and other lesser known transport processes are not well understood
at present, but are subjects of ongoing research within the SBC-LTER program.
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Internal waves
During summer when the water column is strongly stratified, internal waves
supply nitrate stored within deep, sub-thermocline waters to kelp forests via vertical
motions of the thermocline. In the Santa Barbara Channel, internal waves produce
diurnal oscillations in the depth of the thermocline, while in other regions of the Southern
California Bight the oscillations are semidiurnal. Off southern California, diurnal winds
usually produce internal waves although surface tides can also drive them (Lerczak et al.
2001). Internal waves have long been observed to bring cold water and nutrients to
shallow ecosystems (<10 m water depths) in the Southern California Bight (e.g.,
Armstrong and LaFond 1966). The summer growth of giant kelp in at least some areas
depends on nitrate supplied by internal waves (Zimmerman and Kremer 1984).
In the Santa Barbara Channel, internal waves lift water from depths greater than
30 m up to shallow depths of 10 to 20 m where kelp occurs. Elevated nitrate
concentrations of 3 to10 mol L-1 bathe the benthic portions of kelp plants for several
hours during energetic internal wave episodes (Figure 6b), while surface nitrate
concentrations remain low ( < 0.5 mol L-1). Although internal waves supply much less
nitrate to kelp ecosystems than upwelling, they occur in summer when nutrient
concentrations in surface waters tend to be low and other delivery mechanisms are not
operating. Spatial variability in internal wave activity (and in delivery of associated
nutrients) along coastlines is poorly understood. We are currently investigating spatial
differences in nutrient delivery by internal waves using data obtained from instrument
arrays moored along the mainland coast of the Santa Barbara Channel.
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Terrestrial runoff
Considerable amounts of terrestrially-derived nitrogen can be delivered to kelp forests via
runoff from streams. Nitrate and dissolved and particulate organic nitrogen are the most
common forms of stream nitrogen. Their rates of export to the coast are highly variable
in both time and space and depend on the amount and timing of seasonal runoff, which is
determined largely by precipitation patterns and land use. Nearly all the annual rainfall
in the SBC LTER region occurs between November and April with considerable
variability in the frequency and intensity of storms during this period. As a consequence,
nitrogen export to the coast is highly seasonal and episodic; most of the annual discharge
occurs within a few days to weeks each year (Figure 7a). During storms, dissolved
nitrogen concentrations in SBC LTER streams vary within an order of magnitude
whereas discharge varies by five orders of magnitude. Intense periodic rainfall causes
very large temporal variation in the rate of nitrogen export both within and among rainfall
events (Figure 7b).
Differences in the elevation, topography, size, geology and land use of different
catchments result in substantial spatial variation in the amount of runoff and the flux of
nitrogen from the land to the sea. Like other stream water constituents, the concentration
of nitrogen in runoff depends greatly on land use both within and among catchments.
Nitrate concentrations in streams located within the SBC LTER vary over three orders of
magnitude, from a few micromoles per liter in relatively undeveloped catchments, to a
few hundred micromoles per liter in agricultural and urban watersheds, to thousands of
micromoles per liter in a watershed where intensive greenhouse agriculture dominates
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(Figure 8). Phosphate concentrations show a similar, but smaller, variation from 1 to 100
µmol L-1. Typically, stormflow concentrations of dissolved nutrients are lower than base
flow concentrations in streams with high baseflow concentrations, whereas the reverse
occurs in streams with low baseflow levels. Nitrate concentrations in all streams with
appreciable urban development on the coastal plain exhibit a dilution response (i.e.,
concentrations decrease as discharge increases), whereas phosphate concentrations rise
and fall in parallel with the hydrograph, and ammonium declines after an abrupt peak at
the beginning of storms. Although the responses of nutrient concentrations in non-urban
streams to increased storm flows appear to lack a common pattern, nitrate, phosphate and
particulate concentrations tend to follow variations in the hydrograph, and ammonium
concentrations remain consistently low.
Variation in watershed characteristics, annual rainfall and storm intensity
produces even more pronounced changes in the flux of particulate nutrients from the land
to the sea. Although dissolved nutrient concentrations in stream runoff vary within one
order of magnitude, particulate nutrient concentrations vary by more than three orders of
magnitude. Particulate concentrations are highly correlated with sediment load, which in
turn varies with storm intensity; the amounts of transported sediment and particulates
increase exponentially with increases in rainfall and storm. In 2002, a drought year
without major storms (Figure 2a), annual runoff was approximately 20 % of that in 2001.
The difference in the annual dissolved nutrient flux for watersheds throughout the SBC
LTER area was roughly the same as runoff differences (2002 was 20% of 2001), but the
particulate flux in 2002 was only about 3 % of that in 2001. When runoff enters the
ocean, the dissolved nitrogen fraction is confined to near surface waters owing to
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buoyancy of freshwater runoff plumes in seawater; however, nitrogen-containing
particles may be dispersed throughout the water column.
During periods of low discharge nutrient uptake by stream primary producers
(algae, plants) and the subsequent processing of nutrients and organic matter by stream
consumers (e.g., grazing invertebrates) have the potential to alter the forms and amounts
of nutrients and organic matter transported to the ocean both during low flow periods and
floods. Most creeks in the region go though cycles of plant growth and scouring that
follow dry and wet seasons and years. The dense vegetation found in lower stream
reaches traps large amounts of sediment, which are released en masse during high flow
scouring events. The role of a variety of in channel processes that sequester and/or
transform nutrients and sediments to influence the composition and flux of runoff
constituents is an active area of research in the SBC LTER program.
Remineralization of beach detritus
One previously unappreciated source of nitrogen for kelp forests may ultimately
derive from the kelp itself. Physical forces exerted by waves dislodge a large fraction of
kelp biomass and transport it inshore to sandy beaches. The amount of dislodged kelp
that washes up on beaches adjacent to kelp forests (termed wrack) may exceed 500 kg m1
y-1 (Hayes 1974) and it can support rich communities of invertebrate consumers, many
of which are prey for shorebirds (Dugan et al. 2003). This major organic subsidy from
kelp forests to sandy beaches may in turn constitute a significant source of dissolved
nutrients to kelp forests. SBC LTER investigators recently discovered that the
concentrations of dissolved nitrogen (nitrate and nitrite) in pore water collected from the
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upper littoral zone of sandy beaches can be as much as three orders of magnitude higher
than that of water in the surf zone. Importantly, the concentration of dissolved nitrogen
in beach pore water was highly correlated with the standing crop of accumulated wrack
on a beach.
Beaches are very porous habitats through which seawater is pumped with every
wave, flushing oxygen and organic materials into the sand and the beach water table.
The groundwater system of sandy beaches is a dynamic shallow and unconfined aquifer
with flows driven through sediments by tides and waves (Horn 2002). Dissolved
nitrogen in beach pore water may be released periodically with tidal flux and flow or
episodically with beach erosion events that occur during storms and high surf events.
Although previously ignored, the processing (consumption and burial) and transformation
(mineralization) of kelp and other kelp forest macrophytes deposited on beaches, and the
fate and transport of wrack-derived nutrients that become sequestered in beach pore water
could contribute significantly to the nitrogen budget of kelp forests. The timing and rate
of release of nutrients stored in intertidal beach pore water and its potential significance
to kelp forests are topics that SBC LTER scientists are actively studying.
Determining the nitrogen budget of an open kelp forest system
Quantification of the nitrogen budget for an open kelp forest ecosystem is needed
to assess the relative contributions of land- and ocean-derived nutrient transport processes
to nutrient fluxes. Such a budget would need to account for the influx of nitrogen to a
kelp forest from all of the mechanisms described above along with the net utilization and
re-mineralization of nutrient subsides and losses within the kelp forest itself. It is
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conceptually clear how to include boundary fluxes, such as stream runoff, into this
framework and SBC LTER researchers have developed spatially explicit hydrological
models to predict the amount of runoff and fluxes of constituents entering the ocean for
different conditions of precipitation, soil type and land use (Beighley et al. 2003). After
terrestrially-derived dissolved and particulate nitrogen enters the ocean, the quantification
of the net transport of this material in nearshore waters assumes challenges similar to
those for ocean-derived materials. Accurately quantifying the net transport of dissolved
nitrogen to kelp forests in the flow field of the nearshore region, although conceptually
simple, poses several logistical and theoretical challenges. Budget calculations require
that nitrogen transport into and out of the kelp forest be monitored across all walls of a
conceptual box that encompasses the forest. Assessing the net flux of nitrogen into such
a “control volume” from different sources and to different sinks cannot be accomplished
using a single moored instrument array because the spatial fluxes of nutrients must be
determined for the entire three dimensional surface of the kelp forest domain. Detailed
physical oceanographic measurements with spatial arrays of moored instrumentation
have been used to investigate phytoplankton consumption on coral reefs (Genin et al.
2002) opening the possibility of applying a control volume approach to the study of
material flow and nutrient dynamics in kelp forests.
Constraining the net physical oceanographic transport of nitrogen to an open kelp
ecosystem remains a challenging exercise. To resolve this issue, we are assessing the
contributions of the various nutrient delivery processes to observed nitrogen
concentrations at our reef study sites by measuring the temperature, salinity and nutrient
concentration time histories at different reef sites and ascribing different processes (i.e.,
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upwelling, current reversals, internal waves and stream runoff) to different periods of
time. The contribution of each transport mechanism is quantified by examining the net
effect of each process on in situ nitrogen concentrations measured on the reefs. Within
this framework, the quantification of boundary fluxes, such as river inputs, becomes
difficult because it is unclear over what volume the discharged river water has mixed
with ambient ocean waters. Fortunately, this can be diagnosed using the salinity time
series collected from the reef moorings as a measure of the freshwater fraction (or river
dilution) of water at the reef, which can be used in conjunction with studies of freshwater
plume dispersal and nitrogen content. By identifying and quantifying the various types of
transport mechanisms operating in the nearshore region, SBC LTER researchers are
beginning to delineate nutrient delivery pathways to the complicated open kelp forest
ecosystem.
Role of climate in nitrogen transport and ecosystem response
As noted above, there is a strong seasonal component to both ocean- and land–
derived sources of nitrogen fluxes (Figures 6 and 7). Because the different modes of
nitrogen delivery are temporally segregated, they provide complementary rather than
redundant nutrient subsidies to kelp forests in the Santa Barbara region (Figure 9). The
largest ocean signal for nitrogen is derived from wind-driven upwelling, which supplies
cool nutrient-rich water to kelp forests in the spring. Precipitation in the region is
generally confined to late fall and winter when concentrations of ocean-derived nitrogen
tend to be low. During this time of year, streams and rivers are capable of delivering
substantial amounts of dissolved and particulate nitrogen to shallow coastal waters,
21
particularly in areas adjacent to catchments where agriculture and/or urban development
are the predominant land uses. Internal waves, the release of beach pore water, and other
less understood oceanographic processes supply nitrogen to otherwise depleted surface
waters in summer and fall, and enable giant kelp to persist and grow year round except
during the most severe EL Niño events.
Aside from the seasonal cycle, ENSO is the largest climate signal over most of
the Pacific Ocean. The two phases of ENSO are generally termed El Niño (the warm
phase) and La Niña (the cool phase). The relative contributions of land- and oceanderived nitrogen to kelp forests in southern California are likely to vary between El Niño
and La Niña years. During El Niño years, warm oceanic conditions cause the
thermocline to deepen, which greatly reduces the concentration of nitrate in upwelled
water and in water transported inshore by internal waves (Figure 9a). Reduced nitrogen
in surface waters leads to lower kelp productivity (Zimmerman and Robertson 1985),
which in turn is likely to decrease the amount of dissolved nitrogen supplied to kelp
forests via the transport of remineralized kelp nitrogen in beach pore water. The
reduction in ocean-derived nitrogen fluxes to kelp forests during El Niño years may be
compensated, in part, by an increased flux of nitrogen from land to the reef due to
elevated stream runoff caused by above average precipitation. The situation reverses in
cool La Niña years when ocean-derived nitrogen fluxes to the kelp forest tend to be high
and the flux of nitrogen from land is low due to below average rainfall (Figure 9b).
It is important to note that no two ENSO events are identical, differing in
intensity, timing, duration, and ecological response (Wolter and Timlin 1998). As a
consequence, the absolute and relative contributions of different mechanisms of nitrogen
22
delivery to kelp forests during El Niño and La Niña years (as shown in Figure 9) almost
certainly vary among ENSO events. Climatic cycles with return frequencies of decades
may contribute to this variability in the intensity of and subsequent responses to ENSO
events. Most notable in this regard is the Pacific Decadal Oscillation (PDO), a recently
described phenomenon of alternating cold, nutrient-rich and warm, nutrient-poor regimes
in the Pacific Basin lasting 20 to 30 years with abrupt transitions between regimes
(Mantua et al. 1997). The PDO can have strong influences on Pacific ecosystems. For
example, the shift to a warm, nutrient-poor regime during 1976-2000 was accompanied
by abrupt declines in ocean productivity in the Southern California Bight (McGowan et
al. 1998) that led to dramatic declines in the abundances of reef invertebrates and fish, as
well as a northward shift in the distribution of many southern species (Holbrook et al.
1997, Brooks et al. 2002).
The major regime shift from cold to warm waters in 1976 is evident in the sea
surface temperature (SST) record for the Santa Barbara Channel (Figure 2b; mean SST
for the cold (1955-1975) and warm (1976-2000) regimes was 15.5 oC and 16.2 oC ,
respectively). Interestingly, the PDO may also influence the nitrogen flux from the land
to the kelp forest because the mean precipitation for the cold regime was considerably
less than that for the warm regime (Figure 2a; 58.4 vs. 70.4 mm for the cold and warm
periods, respectively). The shift to a warm regime during 1976–2000 coincided with
some of the most severe El Niños on record (Wolter and Timlin 1998). The extent to
which the PDO interacts with ENSO to influence variation in the delivery of nitrogen to
kelp forests and the subsequent ecological responses are at present unknown. Long-term
studies such as those done as part of the SBC LTER program should provide much
23
needed insight into how various climatic processes, occurring at different temporal
scales, interact to influence the ecological response of nearshore marine ecosystems that
rely on subsidies from both the land and the ocean.
24
Acknowledgements
The work described in this article was broadly supported by the National Science
Foundation’s Long Term Ecological Research program. Additional collaborative funding
was provided by the Partnership for Interdisciplinary Studies of Coastal Oceans funded
by the David and Lucile Packard Foundation, the University of California Coastal
Toxicology Program, and NASA.
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Table 1. Variables for which long-term measurements are taken. More information on
sampling methodology, frequency and location can be found at www.sbc.lternet.edu.
Habitat
Spatial extent
Variables measured
Land
11 watersheds
Stream chemistry (nitrate, ammonium, phosphate, total
dissolved nitrogen, total particulate nitrogen, total
dissolved phosphorus, total particulate phosphorus,
particulate organic carbon, C13, N15, total suspended
sediments, conductivity)
Stream discharge
Precipitation
Reef
9 sites
Population dynamics of > 100 species of kelp forest
algae, invertebrates, and fish
Bottom temperature
3 sites
Net primary production of giant kelp
Stable C & N isotope analyses of a diverse assemblage of
kelp forest producers and consumers
Dissolved and particulate nutrients (C, N, P, Si)
Concentrations of suspended particles, & chlorophyll a
Current speed and direction throughout water column
32
Conductivity
Offshore
Channel wide
Chlorophyll a
Phytoplankton productivity
Surface and subsurface current speed and direction
Sea surface temperature
Conductivity
Suspended sediments (via water leaving irradiance)
Dissolved and particulate nutrients (C, N, P, Si)
33
Figure legends
Figure 1. Sources of material inputs to kelp forests from watersheds and the coastal
ocean and the export of materials from kelp forests to other coastal habitats. Dashed
arrows from land to the kelp forest indicate atmospheric and below ground subsidies.
Figure 2. (a) Annual precipitation for the city of Santa Barbara, (b) mean sea surface
temperature at Stearns Wharf, Santa Barbara, California, and (c) maximum canopy
biomass of giant kelp at Naples, near Santa Barbara for El Niño and non El Niño years
during the period 1955 to 2003. El Niño and Non El Niño years were determined by the
Multivariate ENSO Index (Wolter and Timlin 1998). Data on giant kelp in (c) were
provided by ISP Alginates Inc and cover the period 1968 – 2000. Years with no kelp are
shown as zero (kelp data available at http://sbc.lternet.edu/data/CRSData.html).
Figure 3. Map depicting various land uses within the Santa Barbara Coastal Long Term
Ecological Research site. Study watersheds are outlined in black.
Figure 4. Simplified kelp forest food web showing subsidies from land and adjacent
offshore waters.
Figure 5. Stable carbon and nitrogen isotope values for the major land, ocean and reef
sources of production in giant kelp forests (○) and representative reef consumers (●).
Figure 6. Near-bottom (10 to 13-m depth) nitrate concentration in the kelp forest at
Arroyo Quemado. (a) Mean daily nitrate concentration during 2002. Data are
reconstructed from hourly-averaged temperature records. The large peaks in March
through May reflect coastal upwelling events. (b) Nitrate concentration during the period
June 26 through June 30, 2002. Hourly data were averaged from samples taken at 20-
34
minute intervals using a W. S. Oceans in-situ nitrate auto analyzing sensor. Peaks in
nitrate exceeding 2 μmol L-1 for periods of 6 to 9 hours reflect pulses delivered via
diurnal internal waves.
Figure 7. Temporal variability in the flux (discharge rate x concentration) of dissolved
nitrate from Arroyo Burro Creek, Santa Barbara, CA. (a) Nitrate flux for all discharge
events during water year 2003. (b) Nitrate flux from a single discharge event during
March 2003.
Figure 8. Annual mean (± SE) nitrate concentrations for seven streams in water year
2002. The streams typify coastal plain land uses in the SBC LTER: Franklin Creek,
industrial agriculture (greenhouses and nurseries); Santa Monica Creek and Carpinteria
Creek, traditional agriculture (row crops and orchards); Mission Creek, urban; and
Arroyo Hondo and Rattlesnake, undeveloped National Forest and/or fallow ranchland.
All streams were sampled at the tidal limit.
Figure 9. Diagram showing the temporal patterns of nitrogen delivery to giant kelp
forests from different supply mechanisms during (a) warm nutrient-poor El Niño years,
and (b) cool nutrient-rich La Niña years. Colored horizontal lines represent different
mechanisms of nitrogen delivery and the thickness of the lines indicates an estimate of
their relative contributions.
35
Figure 1.
Creeks
Mountains: Shrub
Forest
Foothills: Agriculture
Suburban
Coastal plain: Agriculture
Suburban
Urban
Land
Estuary
Beach
Nutrients, Sediments, Pollutants
Kelp Forest
Nutrients, Plankton, Larvae
Open Ocean
36
POM,
DOM
Annual Precipitation (cm)
Figure 2
El Nino
175
150
125
100
75
mean = 65.1
50
25
0
1955
18
o
Mean SST ( C)
Non-El Nino
a)
1960
1965
1970
1975
1980
1985
1990
1995
2000
b)
17
16
mean = 15.9
15
14
1955
3
Kelp (tons x 10 )
5
1960
1965
1970
1975
1980
1985
1990
1995
2000
c)
4
3
2
1
mean = 971
0
0
1955
1960
1965
1970
00
1975
1980
37
1985
0 0
1990
1995
2000
Figure 3.
38
Figure 4
Land
POM
Dissolved Nutrients
Predators
Predators
(Large Fish, Mammals)
(Fish, Mammals)
Kelp Forest
Herbivores/Detritivores
Predators
(Sea Urchins, Snails,)
(Small Fish, Mobile Invertebrates)
Macroalgae
POM
Sessile Filter Feeders
Zooplankton
POM
Open Ocean
Dissolved Nutrients
Phytoplankton
39
Figure 5.
16
15N (o/oo)
14
barnacle
12
sea urchin
tunicate
10
giant kelp
8
coralline
algae
stream
POM
ocean
POM
6
4
2
-30
-20
-25
13C (o/oo)
40
-15
-10
Figure 6.
30
a)
-1
NO3 (mol L )
25
20
15
10
5
0
J
F
M
A
M
J
J
A
S
O
N
2002
8
b)
-1
NO3 (mol L )
6
4
2
0
26 Jun 02
28 Jun 02
41
30 Jun 02
D
Figure 7.
6000
a)
moles NO3 h-1
5000
4000
3000
2000
1000
0
Oct
Feb
Jun
2003
2002
6000
Oct
b)
moles NO3 h-1
5000
4000
3000
2000
1000
0
00:00
12:00
00:00
15 Mar 2003
12:00
16 Mar 2003
42
00:00
Figure 8.
NO3 (umol L-1)
2000
Baseflow
Stormflow
1500
1000
500
0
Fra Ca
S
A
M
A
R
rpi anta rroy issio rroy attle
nk
nte
o
oH
lin
sn
ria Mon Bur n
o
nd ake
ro
ica
o
High
Anthropogenic influence
43
Low
Figure 9.
a) El Niño year
?
Oct
Dec
Feb
Apr
Jun
Aug
b) La Niña year
?
Oct
Dec
Beach pore water
Feb
Apr
Runoff
Upwelling
44
Jun
Aug
Internal waves