J A S ON D. Oj FM A M J J A S ON D. Years 1990-1994. Years 1990-1994 ...... Striven and Fyne, Proc. R. Soc. Edinburgh, Sect. B, 90,. 223-238, 1986. Therriault ...
PHYTOPLANKTON ECOSYSTEMS' FROM
BLOOM A REVIEW
SUSTAINED
DYNAMICS
WITH
SOME
INVESTIGATION
IN COASTAL GENERAL
OF SAN
LESSONS
FRANCISCO
BAY, CALIFORNIA James E. Cloern
U.S. GeologicalSurvey,Menlo Park, California
Abstract. Phytoplanktonbloomsare prominent features of biologicalvariability in shallowcoastalecosystems such as estuaries,lagoons,bays, and tidal rivers. Long-term observationand researchin San Francisco Bay illustratessome patterns of phytoplanktonspatial and temporalvariabilityand the underlyingmechanisms of thisvariability.Bloomsare eventsof rapid production and accumulationof phytoplanktonbiomassthat are usuallyresponsesto changingphysicalforcingsoriginating in the coastalocean (e.g., tides), the atmosphere (wind), or on the land surface(precipitationand river runoff).Thesephysicalforcingshavedifferenttimescales of variability,so algalbloomscanbe short-termepisodic events,recurrent seasonalphenomena,or rare events associatedwith exceptionalclimatic or hydrologicconditions.The biogeochemicalrole of phytoplanktonprimary productionis to transformand incorporatereactive inorganic elementsinto organic forms, and these transformationsare rapid and lead to measurablegeochemicalchangeduring blooms.Examplesinclude the depletionof inorganicnutrients(N, P, Si), supersaturation of oxygenand removal of carbondioxide,shiftsin the isotopiccompositionof reactiveelements(C, N), production of climaticallyactive trace gases (methyl
bromide,dimethylsulfide), changesin the chemicalform and toxicityof trace metals(As, Cd, Ni, Zn), changesin the biochemicalcompositionand reactivityof the suspendedparticulatematter, and synthesis of organicmatter requiredfor the reproductionand growthof heterotrophs, including bacteria, zooplankton, and benthic consumeranimals.Some classesof phytoplanktonplay specialroles in the cyclingof elementsor synthesisof specificorganicmolecules,but we haveonlyrudimentary understandingof the forcesthat selectfor and promote blooms of these species.Mounting evidence suggests that the natural cyclesof bloom variability are being altered on a global scaleby human activitiesincluding the input of toxic contaminantsand nutrients,manipulation of river flows, and translocationof species.This hypothesiswill be a key component of our effort to understandglobal changeat the land-seainterface. Pursuit of this hypothesiswill require creative approaches for distinguishing natural and anthropogenicsourcesof phytoplanktonpopulationvariability,aswell as recogni-
INTRODUCTION
where natural changeoriginatesfrom processesin the coastalocean,in the atmosphere,and on the land surface, and where human disturbanceis highly focused. Seventy-fivepercent of the U.S. population will live within 75 km of a coastby the year 2010 [Williamset al., 1991].As a resultof this densehuman settlementalong the continental margins,coastal ecosystemsare influencedby diversehuman activities,includingagricultural practices[Fleischeret al., 1987;Nixon, 1995]; the damming of riversand manipulationof their flows[Dynesius and Nilsson,1994];inputsof wastes,includingnutrients [Justif et al., 1995] and toxic contaminants[Windom, 1992];changingland use [Cooper,1995;Hopkinsonand Vallino, 1995] and habitatloss[Nicholset al., 1986];and disturbancesof biologicalcommunitiesthrough harvest [Rothschild et al., 1994]or introductionsof exoticspecies
Earth
science of the 1980s and 1990s has been moti-
vated partly by the challenge to understand global change,which in its broadestsenseincludesthe myriad impactsof the human populationon the Earth system. This problempersistsasa difficultchallengebecausethe componentelementsof global change,such as the climate system,hydrologiccycle, and biological populations,all haveinherentlargenaturalfluctuations.Superimposedonto thesenatural changesare thosecausedby humandisturbance.This scientificchallengepersistsbecause human disturbance is often subtle, indirect, and
sometimesconfoundedby natural changesthat themselvesare not well understood.This problem applies particularly to ecosystemsat the continental margins,
This paper is not subjectto U.S. copyright.
tion that
the modes
of human
disturbance
of coastal
bloom cyclesoperateinteractivelyand cannotbe studied as isolatedprocesses.
Reviewsof Geophysics,34, 2 / May 1996 pages 127-168
Publishedin 1996 by the AmericanGeophysicalUnion.
Paper number 96RG00986 e127e
128 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS Table 1.
34, 2 / REVIEWS OF GEOPHYSICS
Examples of Recent Ecological Change in Global Coastal Waters Phenomenon
Location(s)
Episodesof anoxiaand associatedmortalities Baltic Sea of fish and shellfish
Adriatic Black
Sea
Sea
Harmful algal outbreaks global coastalwaters Oysterpopulationdeclinesand disappearance ChesapeakeBay of vascularplants Changesin the communitycompositionof Bay of Aratu Salvador, Brazil phytoplankton Dutch Wadden Sea Doubling of the biomassand shiftsin the communities
Reference (s)
Rosenberg et al. [1990] Justi•et al. [1987] Mee [1992] Smayda[1989],Hallegraeff[1993] Smithet al. [1992],Orth and Moore [1983] Cowgill[1987] Beukema[1991]
of invertebrates
Invasionby exoticinvertebratesand restructuringof biologicalcommunities
north San FranciscoBay
Interannual
Peel-Harveyestuary,Australia Laveryet al. [1991]
fluctuations in abundance and
Alpineand Cloem[1992],Kimmereret al. [1994]
speciesof macroalgae Mass mortalities
of diverse marine biota
Seabirdmortality Episodesof thickfoam accumulation on
Scandinavian coastal waters
Monterey Bay southern North
Sea
Underdalet al. [1989] Walzet al. [1994] BtitjeandMichaelis[1986]
beaches
Persistent closures of commercial harvest
shellfish
New Zealandcoastalwaters
Increasedfrequencyof red tidesand associated Tolo Harbor, Hong Kong fish kills SetoInland Sea,Japan
[Carlton, 1985; Carltonand Geller, 1993]. Nearly a fifth of the total marine
fish catch comes from these zones of
intensehuman activity[Paulyand Christensen, 1995]. In
recent
decades
we
have
observed
remarkable
changesin coastalwatersof all the continents;examples are listed in Table 1. Many of thesechangesare related either directly or indirectly to changesin the species composition,abundance,or productionrate of the phytoplankton, so this one biologicalcommunityis central to the problemof environmentalchangeat the land-sea interface. This theme is prominent in the recent initiatives to understandmechanismsof change in coastal ecosystems (Table 2). One fundamentalfeature of phytoplankton dynamicsis the episodicrapid population increase as events that we traditionally refer to as "blooms," presumablyin reference to Sch•itt's[1892] descriptionof the seasonalplanktoncyclesin Kiel Bight, (translationfrom Mills [1989,p. 125]):
Mackenzie et al. [1995] Hodgkiss and Yim [1995] Prakash[1987]
"and this play repeats itself year after year with the same regularityas every springthe trees turn green and in autumn losetheir leaves;withjust suchabsolutecertaintyasthe cherries bloom before the sunflowers, so Skeletonema arrives at their
yearly peak earlier than Ceratium."
My purpose here is to review some principles of phytoplanktonbloom dynamicsin their contextas features of changein estuarineand nearshorecoastalwaters.This reviewis organizedto addressbasicquestions: What are phytoplanktonblooms?What are their underlying mechanisms?How are they related to changesin ecosystemprocessesand the geochemistryof estuarine and coastal waters? The review is based around
obser-
vations,models, and insightsthat have come from the U.S. GeologicalSurvey(USGS) programof research focusedon San FranciscoBay. I begin with a general description and conceptual model of phytoplankton bloom dynamicsin shallowcoastalecosystems. Next is a
Table 2. Some Contemporary Research Initiatives to Describe and Explain Processesof Change in Coastal Ecosystemsof North America and Europe Program
Sponsor(s) *
NSF LMER (Land Margin EcosystemResearch) NSF, NOAA, ONR CoOP (CoastalOceanProcesses) NSF, NOAA GLOBEC (GlobalOceanEcosystems Dynamics) NECOP (NutrientEnhancedCoastalOceanProductivity) NOAA ECOHAB (Ecologyand Oceanography of HarmfulAlgal NSF, NOAA Blooms) ICSU LOICZ (Land-OceanInteractions in the CoastalZone) CEC EROS (EuropeanRiver OceanSystem)2000
Reference (s)
Boyntonet al. [1992] Brinket al. [1992] U.S. GLOBEC [1995] Wenzeland Scavia[1993],Atwood et al. [1994] Anderson[1995] Holliganand de Boois[1993] MartinandBarth[1989]
*Abbreviationsare NSF, U.S. National ScienceFoundation;NOAA, U.S. National Oceanicand AtmosphericAdministration;ONR, U.S. Office of Naval Research;ICSU, InternationalCouncilfor ScientificUnions;CEC, Commissionof the EuropeanCommunities.
34, 2 / REVIEWSOF GEOPHYSICS
Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 129
ShallowCoastalEcosystem Local watershed ß..........
.. -..:.....ß
Shallows "" -.
Processesof phytoplankton population variability
ß.. '•....
•Zoca?•?us
Za/era/ •ran•?orZc '.i" ./
Longitudinal"• i7•'::. :.
Primary.production
.tr.•._..::•a..nsport:•.:..• -':-:?_:-_.-
'•:' -i)/:::: ':"'•:';• -,i-"2i:'?•:i":' -::" ............ eel'2gic• "'"• ':":'" Turbulent '"::':: ' •nputs [ ß"...Resusp,e.i•Sion •i•' • ,&_grazing mixing ... ß . ::'.•!•:..i,: Sedir•entation '....•.•"i•.'-'::.. -'-":I:'--')'" ":! -': '!i • -'-•-_d• Benthic grazing
Plate 1. An idealized shallowcoastal ecosystem(SCE) showingthe key processesof phytoplankton populationvariabilityat the land-seainterface.Localprocesses includeprimaryproduction(the sourceof new phytoplanktonbiomass),consumptionby benthicand pelagicgrazers,exchanges betweenthe sediment surfaceand water columnby sedimentationand resuspension, and turbulentmixing.Horizontal transport processes includeexchanges with the coastalocean,riverineinputsof phytoplankton, and longitudinaland lateral transportsgeneratedby density-,tide-, and wind-drivencirculationand mixing.The colortransition fromgreento bluerepresents the salinitygradientalongthe river-oceancontinuum.Brightness represents the bathymetry, andwhiteshadings indicatethelateralshallowdomainscommonto coastalplainestuaries andlagoons.
detailedreviewof the approachesusedin our analysisof the long term observationsin southSan FranciscoBay, with emphasison the searchfor patterns and mechanismsof phytoplanktonpopulationvariability.Then I describethe significanceof bloomsin the coastalzone, emphasizingthe role of phytoplanktonproductionas a mechanismof geochemicaland ecologicalchange.I conclude with some thoughtson the compellingquestions and hypothesesthat will guide researchat the land-sea interface into the next century. The USGS researchprogram in San FranciscoBay beganin 1968and continuesasone of the few long-term efforts of combined observation
and research in the U.S.
coastal zone. Other aspectsof this program are describedby Conomos[1979b],Kockelmanet al. [1982], Cloernand Nichols[1985],Nicholset al. [1986],Nichols and Pamatmat [1988], Peterson[1989], Cheng [1990], Luoma et al. [1990], and Petersonet al. [1995].
THE
GENERAL
PROBLEM
Domains of Interest
San FranciscoBay has been the focus of sustained investigationbecauseit has features common to many shallowcoastalecosystems (SCEs)that are influencedby natural and anthropogenicsourcesof variability.These SCEs include tidal rivers, estuaries, embayments,lagoons,and coastalriver plumes,which are distinctly different ecosystems from the open ocean.The differencesarise partly from the physicalfeaturesillustrated in Plate 1, and they includethe following. 1.
SCEs are transition
zones at the land-sea
inter-
face,sothey are influencedboth by inputsfrom the land surfaceand exchangeswith the coastalocean. Connections to the land surfaceare made through rivers that carryrunofffrom large-scalecatchmentsor from smaller tributariesthat carry runoff from the local watershed
130 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS
34, 2 / REVIEWSOF GEOPHYSICS
tions.The phytoplankton(Table 3) include5000marine species[Hallegraeff,1993] of unicellularalgae havinga broad diversityof cell sizes(mostlyin the rangeof 1 to 100 txm), morphologies,physiologies, and biochemical compositions (Margalef[1978],Soumia[1982],andFogg 2. The domains considered here are shallow. The [1991]giveexcellentreviewsof the form and functionof mean depth of San FranciscoBay is less than 10 rn the phytoplankton).All phytoplanktonspeciesare capaand many have the capacityfor [Conomoset al., 1985], and maximum depth of the ble of photosynthesis, central channelsis of the order of 20-30 m. Exchanges rapid cell division and population growth, up to four of materialsbetweenthe pelagicdomain (open water doublingsper day [e.g.,Fahnenstielet al., 1995]. Popucolumn)and the benthos(bottomsediments)are rapid, lation dynamicsof the phytoplanktoncanbe interpreted so strongbenthic-pelagiccouplingis a definingfeature as responsesto changesin individual processesthat of SCEs. regulatethe biomass(total quantity,in measuressuchas 3. River-influencedSCEs are very differentphysical carbon,nitrogen,or chlorophyllconcentration),species environmentsfrom the open ocean.For example,turbu- composition,and spatialdistributionof the phytoplanklent mixingis a key physicalprocessthat determinesthe ton population.These processes includein situ (local) vertical fluxes of heat, salt, nutrients, and plankton. processesthat causepopulation changewithin a water Vertical mixing in the open ocean is regulatedby the parcel, and horizontal transportsthat displaceor mix seasonalcycle of heat input and thermal stratification water parcelsand their phytoplankton(Plate 1). that retards mixing between surfaceand deep waters. In situprocesses of populationchangeinclude(1) the However, in estuaries and other marine "regions of productionof new biomass,which is controlledby the freshwaterinfluence"[Simpsonet al., 1991],verticalmix- availabilityof visiblelight energyrequiredfor photosyning is regulatedby a larger and more variable sourceof thesisand nutrient resourcesrequiredfor the biosynthebuoyancy,the riverine input of fresh water that acts to sisof newalgalcells,(2) mortality,includingthat caused stabilizethe water columnthroughsalinitystratification. by parasitesor viruses,(3) grazinglossesto pelagicand 4. SCE's are particle-richrelativeto the open ocean. benthicconsumeranimals,(4) turbulentmixingby tideIn San FranciscoBay the near-surfaceconcentrationsof and wind-inducedmotions in the water column, (5) suspended particulatematter (SPM) rangefrom 300mgL-• [Conomos etal., 1979];at highest concen- bottom sediments,and (6) resuspension of bottom-detrations the SPM is dominatedby mineral particlesde- posited microalgaeby tidal currents and wind waves. livered by river flow or resuspendedoff the bottom by Horizontal transportsfollow water circulationsthat are tidal and wind wave currents.Suspendedparticles ab- driven by tidal currents, wind stresseson the water sorb and scatter light, so SCEs are turbid habitats in surface,and horizontal gradientsof water density [Fiwhichphytoplanktongrowthcan be limited by the avail- scheret al., 1979].Thesetransportsdisplacephytoplankabilityof sunlightto sustainphotosynthesis [Wofsy,1983; ton biomasslongitudinallyalong the river-oceancontinuum and laterally between shallowand deep domains, Cloem, 1987]. 5. Many SCEs are nutrient-rich becauseof inputs which are very different habitats for phytoplankton from the land surface[Maloneet al., 1988;Nixon, 1995; growth [Cloem and Cheng,1981; Malone et al., 1986]. Justif et al., 1995] and geochemicaland biologicalpro- Although techniquesexist to measureor estimateeach cesses that act as "filters" to retain nutrients within processshown in Plate 1, comprehensiveprocess-speestuaries[Sharpet al., 1984].In southSanFranciscoBay, cific measurementprogramsare expensive,logistically summerphosphateconcentrationsoften exceed10 gM challenging,and rarely done.Rather, phytoplanktondycomparedwith concentrationsof 10 m), but larger than in the micface is the tide, whichpropagatesinto San FranciscoBay rotidal Gulf of Mexico, Baltic Sea, and Mediterranean throughthe Golden Gate. In this regionof the northeast Sea (tidal amplitude< 0.5 m).
136 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS
34, 2 / REVIEWS OF GEOPHYSICS The Issue of Scale
150OO a
•10000 5000
z
o 300
200 lOO
-• o "*•i '• 15
Each of the physicalforcingsillustratedin Figure 2 contributesto phytoplanktonpopulationvariabilityby influencingthe ratesof verticalmixing,horizontaltransport, production,or grazing.Each forcinghascharacteristictimescalesof variability,suchas the 12.42-hourand •-14-daytidal periods;the diel (24 hours)light cycle;2to 5-daystormeventsof enhancedstreamflowandwind stress;seasonalcyclesof irradiance and temperature; and the pronouncedinterannualvariabilityof river flow. Therefore phytoplanktonpopulationsin SCEs are exposedto physicalforcingsthat have timescalesof variability ranging from hours to years: "a hierarchy of forcingfunctionswhich drive the variousbiologicalresponsemechanismsat differenttime and length scales" [Mackasetal., 1985,p. 653].Each of thesetimescales can be identified in the populationfluctuationsof the phytoplankton. Biomass fluctuations
• -o
10
measured
5
•, 6o •
40
c:
20
0.7
0.5
0.4 1983
1986
1989
1993
Figure 2. Daily fluctuations of five physical forcings that influencepopulationdynamicsof phytoplanktonin San Francisco Bay. Series are for four contrastinghydrologicyears
(1983,1986,1989,and 1993),showing(a) net freshwaterinflow from the Sacramentoand San JoaquinRivers (a calculated quantity,the Delta Outflow Index, from the CaliforniaDepartmentof Water Resources), (b) dailydischarge of a localstream (PattersonCreek) that dischargesinto south San Francisco R•,x,(from 11R •oc•lc•glcml Suv:ey (L•, ni•_ trict), (c) meandailywind speedat the SanFranciscoairport (from the National Climatic Data Center, National Oceanic and AtmosphericAdministration),(d) daily irradiance,measured as quantumflux of photosynthetically activeradiation, and (e) m•imum daily tidal currentspeedin the channelof south San FranciscoBay, calculatedwith harmonicconstants from long-term current measurements[Chengand Ganner, 1985].
with
moored
at the short timescales fluorometers
that
can be
detect
and
record chlorophyllfluorescenceat a fixed location.A samplerecord in Figure 3a showsa 2-week seriesof hourly measurementsin south San FranciscoBay. The first week of the record showsperiodic fluctuationsin chlorophyllfluorescenceover the semidiurnaltidal period, with chlorophyllpeaksat the two low slacktides each day. This high-frequencyvariabilityis causedby tidal advectionas chlorophyllspatialgradientsoscillate over the sensorwith the tide [Cloemet al., 1989]. Spectral analysesof suchchlorophyllseriesconfirma high varianceat the tidal frequencies[Litaker et al., 1993]. Short-termfluctuationscan result from other processes suchasdiel cyclesof chlorophyllsynthesis andzooplankton grazing[Litakeret al., 1993] and wind-waveresuspensionof algalcellsoff the bottom[Demerset al., 1987; de Jongeand van Beusekom,1995]. The secondhalf of the record in Figure 3a showsa 6-day period of exponentialchlorophyllincrease.Here the semidiurnaltidal variabilityis overwhelmedby the rapid growthof phytoplanktonbiomassalongthe entire channel;this period of the record illustratesdaily-scalevariability during a bloom event. Day-to-dayfluctuationsin phytoplankton biomassor physiologicalconditionare commonlyassociatedwith hydrologic-meteorologic events,suchasrainfall pulses,wind events,or periodsof abrupt warming [C6t• and Platt, 1983], and with fluctuationsin tidal mixingoverthe neap-springperiod [Sinclairet al., 1981; Cloem, 199lb ]. Longer-termfluctuationsof phytoplanktonbiomass are illustratedin Figure 3b, a seriesof monthlychlorophyll a measurements in north San FranciscoBay from 1974 to 1995. Three scalesof variability are evident in this record: a seasonalcyclewith peak biomassduring the low-flow summers,interannual variability with a dampedsummerbloom duringyearsof extremelyhigh river flow and shortresidencetime (e.g., 1983), and an apparentpermanentchangein the natureof the record, with the virtual disappearanceof summerbloomsafter
34, 2 / REVIEWSOF GEOPHYSICS
Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 137
40
•ø• o
i
Semi-diurnal
30 _
variability
'
Y
•
(D
oo
20
'•
10 0
1
2
4
5
7
i
i
i
i
i
•--"•----'-----':•;% daily variabilityF
' - ofa ,bo•t•,)•9
8
10
11
12
13
14
15
March,1995
b
'• 4o,-• /
•
30
o
20
e
10
•
Seasonal Interannual , ""'"':•:•:•• •"•'....'•• .:.• variabili I
variabili•
-
persistent .
-
o
1976
1978
198o
1982
1984
1986
1988
199o
1992
1994
1996
Figure3. Sometimescales of phytoplankton biomassvariabilityin SanFranciscoBay. (a) A 14-dayrecord of hourlymeasurements with an in situfluorometerplaced2 m abovethe bottomnear station28 in southSan FranciscoBay (Figure5); the fluorometerwascalibratedwith discretechlorophylla measurements made at the beginningandendof the record(fluorometerdatafrom D. A. Cacchione,personalcommunication, 1995). (b) A 21-yearrecordof monthly(or semimonthly) measurements of surfacechlorophylla concentration near station5 in north SanFranciscoBay (Figure 1); this recordincludesdata from the CaliforniaDepartmentof Water Resources(1974-1986) and USGS (1986-1995).
the North Bay was colonizedin large numbersby the clam Potamocorbulaamurensisin 1987.Jassbyand Powell [1994] examineda period of this chlorophyllrecord and concludedthat most of the interannualvariability is driven by two hydrodynamicprocesses,one associated with fluctuationsin river flow (a natural sourceof variability), and one associated with manageddiversionsof fresh water from the upper estuary(an anthropogenic sourceof variability). Spatialvariability(patchiness) is alsoobservedacross a spectrumof scales[Mackaset al., 1985].Phytoplankton patchinesscan be measuredwith continuousprofilesof chlorophyllfluorescence alonghorizontaltransects[Wilson and Okubo, 1980; Childerset al., 1994;A.D. Jassby et al., Towards the design of sampling networks for characterizingwater quality changesin estuaries,submitted to Estuadne,Coastal,and Shelf Science,1996]. Horizontal variability in south San Francisco Bay is illustratedin Figure 4, which showsthe spatialstructure of chlorophyllfluorescencealonga longitudinalchannel transect (Figure 4a) and along a transversetransect betweenthe channeland adjacentshallows(Figure 4b). The longitudinal profiles show measurementsspaced every 25 m, and variabilityis evidenteven at this small spatialscale.This small-scalevariabilityis superimposed onto larger-scalepatterns (mesoscalevariability) that
often showtrendsof decreasingchlorophyllfluorescence in the seawarddirection(February28, 1995;Figure 4a) and increasingchlorophyllacrossthe shallows(March 21, 1985; Figure 4b). Both small-scaleand mesoscale patchinessare influencedby hydrodynamicprocesses becausethe plankton are transportedby their fluid environment [Mackaset al., 1985]. Therefore the spatial variability patterns,both of chlorophyllbiomassand of individualspecies[e.g.,Kononenet al., 1992;Zingoneet al., 1995], are shapedby the turbulent advectivetransportsof phytoplanktonwithin a spatiallyvariablegrowth environment.These featuresof spatial structureare not stableor persistent.The mesoscaletrendschangefrom seasonto season[Glibert et al., 1995] and day to day [Wilsonand Okubo, 1980],while the small-scalevariability changesover the tidal period [Dustanand Pinckney, 1989]. Figures3 and 4 showthat phytoplanktonbiomassin shallow coastal ecosystemsvaries at timescalesfrom hours to decades and at spatial scalesfrom tens of meters to tens of kilometers.Levin [1992] suggeststhat the centralproblemin ecologyis the problemof pattern and scale,where pattern is the descriptionof spatial or temporalvariabilityand the mechanismsof pattern formation are scale-dependent. Therefore studiesof population fluctuationssuchasphytoplanktonbloomsrequire
138 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS
34 2 / REVIEWS OF GEOPHYSICS b
• 50 A• ,T
"•B•-:•:•.•__• • • •
]
40
50
•
•
•
• D
40
'• 30
30
Fa 20
20-
•
10
•0
-
c
05
10
15
20
25
30
35
40
o
o
•
2
•
4
•
6
i
8
•
lO
12
Distance (kin)
Figure4. Horizontalvariabilityof phytoplankton biomass from continuous measures of chlorophyll fluorescence along(a) longitudinal transects and(b) a lateraltransectof southSanFrancisco Bay.Near-surface waterwaspumpedto a shipboardfluorometerthat wascalibratedwith 6-10 discretemeasurements of chlorophyll a concentration takenalongeachtransect.Insetmapsshowlocations of the transects.
explicitchoicesabout the scalesat whichpopulation variabilitycanbe observedandexplained.The long-term observationalprogramin San FranciscoBay was designedto characterize mesoscale spatialvariabilityalong the longitudinalaxis, at timescalesof weeks to years. Even though(large)populationvarianceexistsat other scales,the data set describedbelow is not appropriate 122ø15; '
122030 '
for analysisof the small-scalefluctuationsillustratedin Figures3 and 4. The SouthSan FranciscoBay Data Set
Patternsof Variability. South San FranciscoBay hasbeen the site of focusedresearchon phytoplankton 122000 '
.:.:.-......:•
Central
Bay...._
37045 '
Figure 5. Map of southSanFranciscoBayshowing locationsof fixedsamplingstationsalongthe longitudinalchannel.
37o30 '
34, 2 / REVIEWSOF GEOPHYSICS Table 4. Phytoplankton SpeciesCommonly Observed During Spring Blooms in South San Francisco Bay
Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 139
the seawardand landwardestuary.Local streamscarry runoff to the lower (landward)estuary.The open connection to the central bay allows fresh water from the Class Species Sacramentoand San JoaquinRivers to intrude into the southbay during periodsof high river flow (Figure 1) Diatoms and allowstidal exchangebetween the South Bay and Diatomophyceae Chaetoceros debile Chaetoceros decipiens coastalocean. The basin'sresidual (tidally averaged) Chaetoceros didymus circulationis slow,with mean seawardflow along the Chaetoceros gracilis eastern shallowsand landward flow along the channel Chaetoceros socialis [Chengand Gartner, 1985] and a hydraulic residence Chaetoceros vistulae time of severalmonths[Walterset al., 1985]. This weak Chaetoceros wighami Coscinodiscus curvatulus(Actinocyclus mean circulationcanbe disruptedby strongwind events curvatulus) or freshwaterinputsthat alter the strengthand direction Coscinodiscus lineatus(Thalassiosira of the residualflows[Huzzeyet al., 1990].Water density leptopus) is often verticallyuniform, indicatingrapid verticalmixCoscinodiscus radiatus ing of the water column.The channelcan becomesalinCyclotellameneghiniana Cyclotellasp. ity stratified after periods of runoff that deliver lowCyclotellastriata density fresh water as a source of buoyancy, but Ditylum brightwelii stratificationoccursonly during neap tides when the Eucampiazoodiacus tidal stirringis weak [Cloern,1984]. PhytoplanktonpriLeptocylindrus minimus Nitzschiaseriata(Pseudo-nitzschia seriata) mary productionis the largestsourceof organiccarbon Paralia sulcata to south San FranciscoBay [Jassbyet al., 1993], and Rhizosoleniasetigera much of the total annual primary production occurs Skeletonema costatum during the spring[Coleet al., 1986]. Thalassiosira decipiens(Thalassiosira The southSan FranciscoBay springbloom has been angulata) Thalassiosira rotula followed every year since 1978, and the patterns of variability within this series can be used to illustrate Nondiatoms somegenerallessonsof phytoplanktonbloom dynamics Chlorella marina Chlorophyceae Chlorella salina in SCEs. The core measurementprogram.in south San Monoraphidiumconvolutum FranciscoBay includesvertical profilesof salinity,temNannochloris atomus perature, chlorophyll(by calibratedfluorometry),and Chrysophyceae Chromulinasp. turbidity at samplingstations(Figure 5) spacedabout Kephyrionsp. every3-4 km along the channel(detailed methodsare Ochromonassp. givenin annualdatareports[e.g.,Edmundsetal., 1995]). Cryptophyceae Chroomonas acuta ( Teleaulaxacuta) Chroomonas amphioxeia(Teleaulax Water samplesare also taken for microscopicexaminaamphioxeia ) tion to determinethe abundanceof phytoplanktonspeChroomonas salina (Rhodomonas salina) cies present during the springblooms (Table 4). The Dinophyceae Gonyaulaxtamarensis(Alexandrium sampling frequency in 1978-1979 was once monthly; ostenfeldii) after 1979the samplingfrequencywasincreasedto once Heterocapsatriquetra Katodinium rotundatum or twice weekly during the period of the springblooms. Prorocentrum minimum Bloom dynamicsare characterizedhere with the chloProtoperidiniumclaudicans rophyll measurementsmade along the channeltransect Prasinophyceae Pyramimonas micron(or P. orientalis) (Figure 5). Near-surfacechlorophyllis used as a meaTetraselmis gracilis Mesodinium rubrum sureof biomassin the photiczone (i.e., the quantitythat Photosynthetic ciliates contributesto primaryproduction),andverticalvariabilFrom samplestaken during 1992-1995 and microscopicenumera- ity is not consideredhere. Lateral variability is also not tions/identifications of R. G. Dufford (personal communications, considered,although there is coherence between the 1992-1995). Names in parenthesesare revisionsbasedon the taxon- seasonal dynamics of phytoplankton biomass in the omy of Tomas[1993, 1996]. channeland adjacentshallows[Cloernand Cheng,1981; Cloernet al., 1985; Vidergaret al., 1993]. Plate 2 depicts the chlorophyllfluctuationsin southSan FranciscoBay bloom dynamicsbecauseit has a recurrent, somewhat with color, and severalprominent patternsof variability predictableperiod of rapid biomassincreaseduringthe stand out. First, the solid backgroundshowsthat biospringmonths. This lagoon-likebasin has an irregular mass isusually lessthan5 IxgL- 1chlorophyll a. Second, bottom topographywith sharpbathymetrictransitions a period of rapid biomassgrowth (a bloom) occurs between the 10- to 25-m-deep axial channel and the duringthe springof everyyear. Third, bloom intensityis lateral shallows(Figure 5), and a large transverseshoal often greatest in the landward estuary,consistentwith (San Bruno) that slowshorizontalexchangesbetween the trends in the high-resolutionchlorophylltransects.
140 ß Cloern' COASTAL PHYTOPLANKTON
BLOOMS
34 2 / REVIEWS OF GEOPHYSICS
San Mateo Bri%ge Dumbarton Bridge
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Distance along channel transect, in kilometers
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Chlorophylla Plate 2. Color representationof spatial-temporalvariability of phytoplanktonbiomass (chlorophyll a concentration)in southSanFranciscoBay.Bloomsare shownasdeparturesfrom the low backgroundbiomass (green),with bloomintensityproportionalto color brightness. The verticalaxisrepresentstime from January 1978 to July 1995, and the horizontal axis representsspatialvariability along the channeltransectfrom the seawardestuary(station21) to the landwardestuary(station32). Color contourswere producedfrom a matrix of interpolatedvaluesbasedon 4449 measurementsof surfacechlorophylla concentrationon 417 dates.
34, 2 / REVIEWSOF GEOPHYSICS
Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 141
1.0
PC1 = 52% of Variance 0.8
0.6
Figure 6. Coefficients(loadings)of the first two principalcomponents,which accountfor 87% of the chlorophyllvariance along the south San Francisco Bay transect, for the period January1978 to July 1995. Principal
0.4
0.2
component analysis wasdoneon •hecorrela-
1.0
tion matrix, and results are varimax-rotated
solutions[Jassby and Powell,1990].This analysissuggests two independentspatialmodes of phytoplankton biomass variability: one (PC1) in the landwardestuarinebasinsouth of station 25, and a second(PC2) in the seawardestuarynorth of station 25.
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Finally, the nature of the springbloom changesfrom in south San FranciscoBay can be explainedwith only year to year. For example,the 1986 springbloomwas a two spatial modes (patterns): the first is expressed monthlongevent of very high chlorophyllconcentration stronglyin that region of the estuarylandwardof station (maximum >70 !xgL-•) alongtheentiretransect. The 25, and the secondis expressedstronglyin the region of 1991 springbloom was a short-livedevent confinedto the estuaryseawardof station25 (Figure 6). This sepathe landwardestuary,where maximumchlorophyllcon- ration of the two spatialmodesat station25 corresponds centration wasonly12!xgL-•. Thepatterns revealed in to the location of the San Bruno Shoal (Figure 5), a this image illustratetwo lessonsthat apply generallyto topographiccontrol of horizontal mixing. The tidally shallowcoastalecosystems: (1) phytoplankfon blooms averagedcirculationof southSan FranciscoBay is charare spatiallyheterogeneous,and (2) the timing and acterizedby a slowlyrotatinggyrethat actsto retain fluid magnitudeof the seasonalbloomschangefrom year to within the central basin of the estuary,below the San Bruno Shoal [Chengand Casulli,1982].The PCA result year. The patterns of population variability in time and is consistent with this mean circulation that maintains spacecan be formalized with multivariate techniques two spatialdomainsseparatedby a topographiccontrol such as principal componentsanalysis(PCA). If we of mixing [Powellet al., 1986]. This lessonapplies to considermeasurements at samplingstationsasvariables, other coastal ecosystemswhere the mesoscalespatial and samplingdates as individual cases,then PCA can variabilityof planktonreflectsthe water circulationpatreveal patterns of spatial coherencein the temporal ten [Jouffreet al., 1991] and where distinct spatial dofluctuationsof biomassalonga transect.This PCA of the mains can have different temporal patterns of bloom southSanFranciscoBay data setidentifiestwo principal evolution [Therriaultand Levasseur,1986; Kahru and componentsthat togetheraccountfor 87% of the total Nbmmann, 1990; Glibertet al., 1995]. A secondresult of PCA is the seriesof scalaramplichlorophyll variance. The first principal component (PC1), whichaccountsfor 52% of the chlorophyllvari- tudes(or scores)that expressthe relativeimportanceof and Powell, ance,hassmallcoefficients (or loadings)at the seaward eachprincipalcomponentover time [Jassby stationsand progressively largercoefficientsat the land- 1990].Figure 7 showsthe time seriesof amplitudesfor ward stations(Figure6). The secondcomponent(PC2), PC1. This series is a representationof pattern in the accountingfor an additional 35% of the variance,has temporal variability of phytoplanktonbiomassin the largest coefficientsat the seawardstations.This PCA landwardbasin.This temporal pattern is dominatedby showsthat mostof the phytoplanktonbiomassvariability episodicspikesthat occurin the springof eachyear,with
142 ß C!oern' COASTAL PHYTOPLANKTON BLOOMS
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34, 2/REVIEWS OF GEOPHYSICS
30
o•.•,:20 lO I
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Figure7. (bottom)Time seriesof amplitudes (scores)for the first principalcomponentof chlorophyllvariability in south San Francisco Bay. Large amplitudescorrespondto eventsof high phytoplanktonbiomass(blooms)in the landwardestuary.(top) Parallelseriesof nearsurfacesalinityin the landwardestuary(mean of measurementsat stations26-32), illustrating that bloomsoccurduringthe wet seasonof high river flow and annualsalinityminima.
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Year
prominentyear-to-yearfluctuationin the timing, duration, and magnitudeof these spikes. Mechanismsof variability. The seriesof principal componentamplitudesin Figure7 is consistent with the notion of phytoplanktonblooms as departures from population quasi-equilibrium.Blooms are population outburststhat can appear and dissipatewithin a period of weeks.What determinesthe timing of theseoutbursts, their duration, and their magnitude,and why do these features change from year to year? The two series in Figure 7 showthat bloomsoccurin southSan Francisco Bay during the wet season,when surface salinity is dilutedby freshwater.This seasonal coherencebetween bloom developmentand low salinity results, in part, from the stabilizationof the water columnby the salinity stratification induced by freshwater inflows [Cloern, 1991a,hi. The absenceof bloomsin summer-autumnis
that thisbalanceis sensitiveto the rate of verticalmixing in the water column[Cloern,1991b].Vertical mixingis broughtaboutby tidal stresses appliedat the bottomand wind stresses on the water surface[Simpsonet al., 1991], and in mesotidal
SCEs the tidal stresses often dominate.
Weak tidal stirringpromotesbloomsby (1) slowingthe turbulent diffusivelossof phytoplanktonbiomassfrom the photiczone [Koseffet al., 1993], (2) deepeningthe photic zone (growth habitat) as tidal resuspension of bottomsediments weakens[Schoellhamer, 1996],and(3) reducingthe vertical flux of phytoplanktonto benthic consumeranimals[Cloern,1991b].Bloomsdevelopduring periods of weak tidal energy, and they dissipate during periods of strong tidal energy. This lessonis illustratedin Figure 8, which showsthe evolutionof the 1985 springbloom and the simultaneouschangesin the dailytidal currentamplitudeU. Rapid biomass(chloroalso a responseto the seasonalcYCles of the benthic phyll) growth occurredduring the neap tide in late suspensiOn-feeding animals,whosebiomassand grazing March; this bloom dissipatedsoonafter the subsequent rate are highest in summer. Therefore the seasonal springtide in earlyApril. distribution of bloomsin thisparticularestuaryappears The associationbetween weekly-scalechlorophyll vanatomyand the uuaxre -me•s a prominent........ of to be a responseto seasonatnuctuatlonsin nyurmogy (riverflowandits influenceon densitystratification)and phytoplanktonpopulationdynamicsin southSan Frantrophic interactions(grazinglossesto benthicconsum- cisco Bay. This associationis illustrated in Figure 9, which showsa linear relationshipbetween the rate of ers). At shorter timescales,too, the timing of blooms is biomasschangeand the antecedenttidal current speeds regulatedby physicalprocessesthat influencethe bal- for all the large springbloomsobservedbetween 1978 ance between phytoplankton production and losses. and 1995.The rate of biomasschange,R, wascalculated Simulation experimentswith numerical models show as ........
1
•
_•
_ •._
....
34, 2 / REVIEWSOF GEOPHYSICS
Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 143
0.7 0.6 0.5 0.4 I
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Figure 8. The 1985 springbloom in south San FranciscoBay: (bottom) weeklyfluctuations of phytoplanktonbiomassin the landward estuary(meanchlorophylla concentration at stations 26-32) and (top) daily fluctuationsin the tidal currentamplitudeU. Current amplitudes were computed from tidal harmonicconstantsderived from long-
30 /
20•
term
current
measurements
in the central
southbay channel[Chengand Gartner,1985] (predictedU from J. W. Gartner (personal communication,1995)). Biomassincreased rapidly after March 20, when U waslessthan
10 /
0.5 ms -•. .e'
I
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79-,%b 10-/l•a r 20-1•ar30-graf
19-4,0 r
1985
0.2
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•
Figure 9. Tidal forcingand phytoplankton bloomsin southSanFranciscoBay. The net rate of biomasschange,R, was calculated from the week-to-week changesin mean chlorophylla concentrationin the landward estuary(stations26-32). The tidal regimeis representedby the 7-day mean current amplitude, U7. Pointsrepresentall the weekly-
/
scale events
of
1978-1995
in which
the
meanchlorophylla concentrationfell below
ß
or increased above10IxgL- • (updated and
'e-
89
revisedfrom Figure 4 of Cloern [1991b]). The dashedline is the least squaresregressionof R againstU7 (r = 0.66). Deviations around this regressionin 1983, 1989, 1990, and 1995 are examinedin Figures10-13 to illustrate
4
ability.
95
0.4
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MeanCurrent Amplitude U7 (m/s)
0.7
other mechanisms
of bloom vari-
144 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS
34, 2 / REVIEWS OF GEOPHYSICS
Distance (km) 0
10
Distance (km)
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O0
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g'-.2j:•-•i!::iii•:'"----:-'---•::-.... "-'•il;-":g•i:•iiii?::::1111iii'#.. .";':'::!iii!::i::iii::i::i::::::i:" ".:i...:'•i•;;--':.-i•.. :ii!::i•i::i:;::i•!• ':•
40
!•;•i•.g•.:•i•:;..i.•.....•.•`..i•;•`..•.•.....?.`:.:..•i•i• ':":•½i•i•.' •:"•-"•:•i[?-::.-'i-'•.'.'• :':!•i•i