## PHYTOPLANKTON BLOOM DYNAMICS IN COASTAL

ECOSYSTEMS' A REVIEW WITH SOME GENERAL LESSONS

FROM SUSTAINED INVESTIGATION OF SAN FRANCISCO 

# BAY, CALIFORNIA

James E. Cloern 

### U.S. GeologicalSurvey,Menlo Park, California



### Abstract. Phytoplankton bloomsare prominent features of biological

variability in shallow

coastalecosystems such as estuaries, lagoons,

bays, and tidal rivers. Long-term observation and research in San Francisco 

### Bay illustrates

some patterns of phytoplankton spatial and temporal

variability

and the underlying

mechanisms of this variability.

Blooms are events

of rapid production and accumulation

of phytoplankton

biomass that are usually responses

to changing

physical forcingsoriginat

### ing in the coastalocean (e.g., tides), the atmosphere (wind), or on the land surface (precipitation

and river runoff). These physical forcings havedifferent

timescales of variability,

so algalblooms

can be short-term

episodic events,recurrent seasonal phenomena,

or rare events associated

with exceptional

climatic or hydrologicconditions. The biogeochemical

role of phytoplankton

primary productionis to transformand incorporatereactive inorganicelements into organic forms, and these transformations

are rapid and lead to measurablegeochemical

changeduring blooms.Examplesinclude the 

### depletion

of inorganic

nutrients

(N, P, Si), supersaturation of oxygen

and removalof carbondioxide,shiftsin 

### the isotopic

composition

of reactiveelements

(C, N), production of climaticallyactive trace gases (methyl bromide, dimethylsulfide),

changes in the chemical

form and toxicity

of trace metals

(As, Cd, Ni, Zn), changes in the biochemical

composition

and reactivityof the suspended particulate

matter, and synthesis

of organic

matter requiredfor the reproduction and growthof heterotrophs, including bacteria, zooplankton, and benthic


### consumer

animals. Some classes

of phytoplankton

play specialroles in the cycling of elements

or synthesis

of 

### specific organic molecules,

butwe have

onlyrudimentary understanding

of the forces

that select

for and promote blooms of these species. Mounting evidence suggests that the natural cycles of bloom variability are being 

### altered on a global scaleby human activities including the input of toxic contaminants and nutrients,

manipulation of river flows, and translocation of species.

This hypothesis

will be a key component of our effort to understand

global change

at the land-seainterface. Pur

### suit of this hypothesis will require creative approaches for distinguishing

natural and anthropogenic sources of phytoplankton

population

variability,aswell as recognition that the modes of human disturbance of coastal bloom cycles

operate interactively

and cannot

be studied
as isolated processes.

INTRODUCTION

Earth science of the 1980s and 1990s has been moti

### vated partly by the challenge to understand global change, which in its broadest

sense includes the myriad 

### impacts of the human population on the Earth system. This problempersists

asa difficult

challenge

because the component

elementsof global change,such as the climate system,hydrologiccycle, and biological popula

### tions, all haveinherentlargenatural fluctuations.

Superimposed onto thesenatural changes are thosecaused

by 

### humandisturbance.

This scientific

challenge

persistsbecause human disturbance is often subtle, indirect, and sometimes

confoundedby natural changes that them

### selves are not well understood. This problem applies particularlyto ecosystems at the continental margins, where natural change originates

from processes

in the coastal ocean, in the atmosphere, and on the land surface, and where human disturbance is highly focused. Seventy-five

percent of the U.S. population will live 

### within 75 km of a coast by the year 2010 [Williams et al., 1991].As a resultof this dense human settlement

along the continental margins,coastal ecosystems are influenced by diverse

human activities,

including

agricultural practices

[Fleischer

et al., 1987; Nixon, 1995]; the dam

### ming of rivers

and manipulation

of their flows[Dynesius and Nilsson,1994]; inputsof wastes, including

nutrients 

### [Justif et al., 1995] and toxic contaminants [Windom, 1992];changing

land use [Cooper,

1995; Hopkinson

and Vallino, 1995]and habitat loss[Nichols et al., 1986];and disturbances

of biological

communities

through harvest 

### [Rothschild

et al., 1994]or introductions of exotic species

This paper is not subject to U.S. copyright.

Published

in 1996 by the AmericanGeophysical Union.

e127e Reviews of Geophysics,

34, 2 / May 1996
pages 127-168 Paper number 96RG00986128 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS

Table 1. Examples of Recent Ecological Change in Global Coastal Waters

Phenomenon Location (s) Reference (s)

Episodes

of anoxiaand associated mortalities Baltic Sea of fish and shellfish Adriatic Sea
Black Sea Harmful algal outbreaks global coastal waters Oysterpopulation

declines and disappearance Chesapeake Bay of vascular

plants Changes

in the community

composition

of phytoplankton Doubling of the biomass and shiftsin the communities of invertebrates Invasion by exoticinvertebrates and restructuring

of biological

communities Interannual fluctuations in abundance and species of macroalgae Mass mortalities of diverse marine biota Seabird mortality Episodes

of thickfoam accumulation on beaches Persistent closures of commercial shellfish harvest Increased

frequency

of red tides

and associated fish kills Rosenberg et al. [1990] Justi•et al. [1987] Mee [1992] Smayda [1989],Hallegraeff

[1993] Smith et al. [1992],Orth and Moore [1983]
Bay of Aratu Salvador, Brazil Dutch Wadden Sea Cowgill [1987]

Beukema[1991]

north San Francisco

Bay Alpine

and Cloem

[1992], Kimmerer

et al. [1994]

Peel-Harvey

estuary, Australia Lavery

et al. [1991]

Scandinavian coastal waters Monterey Bay southern North Sea Underdal et al. [1989] Walz et al. [1994] Btitje and Michaelis

[1986]

New Zealand

coastal waters Mackenzie

t al. [1995]

Tolo Harbor, Hong Kong SetoInland Sea,

Japan Hodgkiss and Yim [1995] Prakash [1987]



### [Carlton, 1985; Carltonand Geller, 1993]. Nearly a fifth of the total marine fish catch comes from these zones of 

### intensehuman activity [Pauly and Christensen,

1995].
In recent decades we have observed remarkable changes in coastal

watersof all the continents; examples

are listed in Table 1. Many of thesechanges are related either directly or indirectly to changes in the species 

### composition,

abundance,

or production

rate of the phytoplankton, so this one biologicalcommunity is central 

### to the problemof environmental change at the land-sea interface. This theme is prominent in the recent initia

### tives to understandmechanisms of change in coastal 

### ecosystems

(Table 2). One fundamental feature of phytoplankton dynamics

is the episodicrapid population increase as events that we traditionally refer to as 

### "blooms," presumablyin reference to Sch•itt's[1892] description

of the seasonal

plankton

cycles in Kiel Bight, 

### (translation

from Mills [1989,p. 125]): "and this play repeats itself year after year with the same regularityas every spring the trees turn green and in autumn lose their leaves;

withjust such

absolute certainty as the cherries bloom before the sunflowers, so Skeletonema arrives at their yearly peak earlier than Ceratium."


### My purpose here is to review some principles of phytoplankton

bloom dynamics

in their contextas features of change

in estuarine

and nearshore

coastalwaters.This reviewis organized to address

basic questions: What are phytoplankton blooms? What are their underlying mechanisms?

How are they related to changes in ecosystem

processes

and the geochemistry

of estuarine and coastal waters? The review is based around observations, models, and insights that have come from the 

### U.S. Geological

Survey(USGS) programof research focused on San Francisco

Bay. I begin with a general description and conceptual model of phytoplankton bloom dynamics

in shallow

coastal ecosystems.

Next is a

Table 2. Some Contemporary Research Initiatives to Describe and Explain Processes of Change in Coastal Ecosystems of North America and Europe

Program Sponsor(s) * Reference (s)

LMER (Land Margin Ecosystem Research) CoOP (Coastal

Ocean Processes) GLOBEC (GlobalOcean Ecosystems

Dynamics) NECOP (NutrientEnhanced Coastal Ocean Productivity) ECOHAB (Ecology

and Oceanography

of HarmfulAlgal Blooms) LOICZ (Land-Ocean

Interactions

in the Coastal

Zone) EROS (European

River Ocean

System) 2000 NSF

NSF, NOAA, ONR NSF, NOAA NOAA NSF, NOAA

ICSU CEC Boynton et al. [1992] Brinket al. [1992] U.S. GLOBEC [1995] Wenzel and Scavia

[1993],Atwood

et al. [1994] Anderson

[1995]
Holligan and de Boois

[1993] Martinand Barth [1989]

*Abbreviations

are NSF, U.S. National Science Foundation;

NOAA, U.S. National Oceanicand Atmospheric Administration;

ONR, U.S. Office of Naval Research; ICSU, International

Council for Scientific

Unions;CEC, Commission of the EuropeanCommunities.34, 2 / REVIEWS OF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 129



### ShallowCoastalEcosystem Local watershed

ß

.......... .. -..:..... ß Shallows ""

-.



### Processes of phytoplankton 

### population variability



### Lo n g i tu d inal"• i7 •'::. :. 

## .tr.•._..::•a..nsport:•.:..•

-' :-:?_:-_.- ß

.. '•.... • Zoca?•?us



## Za/era/ •ran•?orZc

'.i"

. /

Primary.production 

# '•:' ' "'•';• i"2i:'?•:i":' -::"

............ "'"• Turbulent

' •nputs [ 

# -i)/:::: -,- eel'2gic•

':":'" '"::':: 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) showing

the key processes

of phytoplankton population

variability

at the land-sea

interface.

Local processes

include primary production

(the source

of new phytoplankton

biomass),

consumption

by benthic

and pelagic

grazers, exchanges

between the sediment surface and water columnby sedimentation and resuspension,

and turbulent mixing.Horizontal transport processes

include exchanges

with the coastal

ocean, riverine inputs of phytoplankton,

and longitudinal

and lateraltransports

generated

by density-,

tide-, andwind-driven

circulation

and mixing.

The colortransition fromgreen

to blue represents

the salinity

gradient along the river-ocean

continuum.

Brightness

represents

the bathymetry,

and white shadings indicate the lateral

shallow domains common to coastal

plain estuaries and lagoons.



### detailedreview

of the approaches

usedin our analysis

of the long term observations in southSan Francisco Bay, with emphasis

on the search

for patterns and mecha

### nismsof phytoplankton population

variability.Then I describe the significance

of bloomsin the coastal zone, emphasizing

the role of phytoplankton productionas a mechanism

of geochemical

and ecological

change. I con

### clude with somethoughts on the compelling

questions 

### and hypotheses

that will guide research at the land-sea interface into the next century. 

### The USGS research

program in San Francisco Bay beganin 1968and continues asone of the few long-term efforts of combined observation and research in the U.S. coastal zone. Other aspects of this program are de

### scribed by Conomos

[1979b], Kockelman

et al. [1982], 

### Cloern and Nichols

[1985], Nichols et al. [1986],

Nichols and Pamatmat [1988], Peterson [1989], Cheng [1990], 

### Luoma et al. [1990],and Peterson et al. [1995]. THE GENERAL PROBLEM

Domains of Interest 

### San Francisco

Bay has been the focus of sustained investigation

becauseit has features common to many 

### shallow coastal ecosystems

(SCEs)that are influenced by natural and anthropogenic sources of variability.These SCEs include tidal rivers, estuaries, embayments,la

### goons,and coastal river plumes,which are distinctly differentecosystems

from the open ocean.The differences arise partly from the physical featuresillustrated in Plate 1, and they includethe following.
1. SCEs are transition zones at the land-sea inter

### face,sothey are influenced both by inputs

from the land surfaceand exchanges with the coastal

ocean. Connections to the land surfaceare made through rivers that 

### carryrunoff

from large-scale

catchments

or from smaller tributariesthat carry runoff from the local watershed130 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWSOF GEOPHYSICS



### (Plate 1). Riverine inputs are sources of fresh water, sediments,

and nutrientsthat together create a unique 

### habitat for phytoplankton population development. These habitatsare characterized by large spatial gradients along the river-ocean continuum.
2. The domains considered here are shallow. The



### mean depth of San FranciscoBay is less than 10 rn 

### [Conomos

et al., 1985], and maximum depth of the central channels

is of the order of 20-30 m. Exchanges 

### of materialsbetweenthe pelagicdomain (open water 

### column) and the benthos

(bottom sediments)

are rapid,

so strong

benthic-pelagic

coupling

is a defining

feature
of SCEs. 

### 3. River-influenced

SCEs are very different physical environments

from the open ocean.

For example,

turbulent mixingis a key physical process that determines

the vertical fluxes of heat, salt, nutrients, and plankton. 

### Vertical mixing in the open ocean is regulatedby the seasonal

cycle of heat input and thermal stratification 

### that retards mixing between surfaceand deep waters. However, in estuaries and other marine "regions of 

### freshwater

influence"

[Simpson

et al., 1991],

verticalmixing is regulatedby a larger and more variable source of buoyancy,

the riverine input of fresh water that actsto 

### stabilize the water column

through salinity stratification. 4. SCE's are particle-rich relativeto the open ocean. In San Francisco

Bay the near-surface

concentrations

of 

### suspended

particulate

matter (SPM) range

from <5 to 

### >300mg L-• [Conomos

etal., 1979];

at highestconcentrations the SPM is dominatedby mineral particlesde

### livered by river flow or resuspended off the bottom by tidal and wind wave currents.Suspended particlesabsorb and scatter light, so SCEs are turbid habitats in whichphytoplankton

growth can be limited by the avail

### abilityof sunlight

to sustain

photosynthesis

[Wofsy, 1983; Cloem, 1987]. 5. Many SCEs are nutrient-rich because of inputs from the land surface[Maloneet al., 1988;Nixon, 1995; 

### Justif et al., 1995] and geochemical and biological

processes that act as "filters" to retain nutrients within 

### estuaries

[Sharp et al., 1984].

In south SanFrancisco

Bay,

summerphosphate

concentrations

often exceed10 gM compared

with concentrations

of <0.5 gM in the adjacent Pacific

Ocean [Van Geen

and Luoma, 1993].

Similar enrichmentexists

for other nutrients such as nitrogen 

### (N) and silica (Si). Thereforethe potentialfor phytoplankton

production

canbe muchhigherin SCEs than in most regions

of the ocean,and the phytoplanktonpopulation fluctuations

in SCEs are highlyamplified.



### GeneralOverviewand Conceptual Model of Phytoplankton

Blooms in SCEs Shallow coastal ecosystems

maintain plankton populations distinct from those beyond the freshwater and oceanic interfaces.

Much of the biogeochemicalvariabil

### ity within theseSCEs originates with fluctuations

in the 

### phytoplankton

population,

andRiley[1967]provided the conceptual

framework

for understanding

thesefluctua

### tions.

The phytoplankton

(Table 3) include

5000marine species [Hallegraeff,

1993] of unicellularalgae havinga 

### broad diversity

of cell sizes

(mostly in the rangeof 1 to 100 txm), morphologies, physiologies,

and biochemical compositions

(Margalef

[1978], Soumia[1982],

and Fogg [1991]giveexcellent

reviews of the form and function of 

### the phytoplankton).

All phytoplankton

species are capable of photosynthesis, and many have the capacity for rapid cell division and population growth, up to four 

### doublings

per day [e.g., Fahnenstiel et al., 1995]. Population dynamics

of the phytoplankton

can be interpreted

as responses

to changesin individual processes that 

### regulate the biomass

(total quantity,

in measures

such as carbon, nitrogen,

or chlorophyll

concentration),

species composition,

and spatialdistribution of the phytoplank

### ton population.

These processes

includein situ (local) processes

that causepopulation change within a water 

### parcel, and horizontal transports that displace

or mix 

### water parcels

and their phytoplankton (Plate 1). In situprocesses

of population

change include (1) the productionof new biomass, which is controlledby the availability

of visible

light energy

required for photosynthesis and nutrient resources required for the biosynthe

### sis of newalgal

cells, (2) mortality,

including

that caused by parasites

or viruses,

(3) grazing

losses to pelagic

and 

### benthic consumer

animals, (4) turbulent

mixing by tideand wind-induced

motions in the water column, (5) sinking and deposition

of phytoplankton

biomass on the 

### bottom sediments,

and (6) resuspension

of bottom-deposited microalgae by tidal currents and wind waves. 

### Horizontal transports

follow water circulations that are driven by tidal currents, wind stresses on the water surface,and horizontal gradientsof water density [Fi

### scher et al., 1979].

Thesetransports

displacephytoplankton biomass

longitudinally

alongthe river-ocean

contin

### uum and laterally between shallowand deep domains, which are very different habitats for phytoplankton 

### growth [Cloem and Cheng, 1981; Malone et al., 1986]. Although techniques

existto measure

or estimateeach process shown in Plate 1, comprehensiveprocess-spe

### cific measurement

programs

are expensive,

logistically challenging,

and rarely done. Rather, phytoplanktondynamics in SCEsare often followedby measuring changes 

### in biomass

(usually as the concentration

of chlorophyll a, the photosynthetic pigment contained in all phyto

### plankton cells), species composition,

and photosynthesis

as an index of population growth rate. These measure

### ments are often done in conjunction with basichydro

### graphic measurements

(salinity, temperature,

tides) that

can be used to infer patterns of water circulation and 

### transports,

and surveys

of the pelagicand benthicherbivores that can used to estimate potential rates of grazing loss. 

### Phytoplanktonpopulations often exist in a static "quasi-equilibrium"

[Evans and Parslow,

1985] in which 

### the rate of biomass

production

(the primaryproductivity) is balanced

by the phytoplankton

losses and transports. Under this conditionthe net populationgrowth34, 2 / REVIEWS OF GEOPHYSICS Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 131

Table 3. Characteristics of the Primary Classesof Algae That Form Phytoplankton Blooms in Tidal Rivers, Estuaries, and Shallow Coastal Waters

Class Distinguishing Features Common Genera • Examples of Occurrence

Chlorophyceae forms includeunicells or multicelled Nannochloris (greenalgae) colonies or filaments;

cell walls contain cellulose; zero, two or four equal flagella;

storage productis Dunaliella starch; most species

are freshwater Chrysophyceae mostly smallunicells,

motile or Pseudopedinella (chrysophytes) nonmotile; some species with Aureococcus silicified or calcareous scales in the cell wall; either one or two (unequal) flagella; storage products are lipid (fat) small, flattened, motile cells;cell coverings

of minuteproteinaceous plates; two equal

flagella; ubiquitous but rarelydominate

bloombiomass nonmotile

cells shaped like discs,

needles, Chaetoceros

or multicelled colonies or chains;

cell Thalassiosira walls composed

of two organic

shells (frustules)

impregnated

with amorphous

silica; some species are capable of veryrapidcell division; Skeletonema oftenthe dominant

components

of spring blooms in temperate

coastal

waters Cryptophyceae Cryptomonas 

### (cryptophytes) Chroomonas

Diatomophyceae (diatoms)

Dinophyceae (dinoflagellates) (mostly) large, motileunicells; multilayered

cell covering,

formedinto distinct plates in the "armored" species; two unequal

flagella (one transverse,

one longitudinal);

some species capable of rapid swimming

and vertical migration;

responsible

for visible colored (red, green)

blooms; Rhizosolenia

Coscinodiscus Leptocylindricus Nitzschia Katodinium Gymnodinium

Alexand•um

Peridinium

many species are mixotrophic

(capable Dinophysis of both photosynthetic

and 

## heterotrophic nutrition) Prorocentrum Cyanophyceae

(blue- very

small, procaryotic

(bacteria-like) Microcystis green algae, or cells

with no defined

internal structures

Nodularia cyanobacteria) (e.g., no nucleus

or chloroplasts); unicells or multicelled colonies or 

## filaments; no flagella; gs vacuoles

Aphanizomenon allowbuoyancy

regulation

and dense 

### accumulations

atthe water surface; Synechococcus

some species fix N2 Prasinophyceae small, motilecells;

one,two,or four Pyramimonas flagella that are covered

with minute Micromonas scales or hairs; most species havecell coverings

with organic

scales Prymnesiophyceae most species are small,

motilecells,

but Phaeocystis

some form colonies

of nonmotile cells; cell coverings

include one or more layers of organic

scales or calcite

plates Emiliania (coccoliths);

oneor twoflagella,

with
some species also having a short Chrysochromulina appendage

(haptonema)

for attachment

o surfaces;

complex life cycles of alternating

cellformsand Prymnesium diverse modes of nutrition Calico Creek, North Carolina [Mallin, 1994]
lagoons of NE Spain [Comin, 1982]

Pamlico River estuary

[Mallin,1994] Long Island

embayments

[Cosper et al., 1989]; Narragansett

Bay [Smayda

and Villareal, 1989]
Rhode River estuary

[Gallegos,

1992]
NeuseRiver estuary

[Mallin, 1994];

San Francisco

Bay [Cloern

et al., 1985]
Bedford Basin, Canada [Kepkay et al., 1993] Auke Bay,

Alaska[Ziemann

et al., 1991]; Gulf of St. Lawrence

[Levasseur

et al., 1992]; Gulf of Naples,

Italy [Zingone

et al., 1995] Kinu-uraBay,Japan

[Hamaand Handa, 1994]; Fraser River plume [Harrison

et al., 1991]; Dutch coastal

waters [Brussaard

et al., 1995];

Scottish sealochs

[Tett et al., 1986]; Madras coast, India [Sivaswamy

and Prasad, 1990]; Patos Lagoon, Brazil [Abreu et al., 1995] French coastal waters [Sournia et al., 1987] Otsuchi Bay,Japan

[Nakaoka,

1992] GermanBight [Colijn

et al., 1990] Bay of Fundy,

Canada [Martin et al., 1990] Patuxent River estuary

[Sellner et al., 1991]
Tomales Bay [Cole,

1989]; Ria de Viso, Spain [Fraga et al., 1992]
Gulf of Maine [Franks

and Anderson,

1992]; Chinhae Bay, Korea [Han et al., 1992]
Baltic Sea [Heiskanen

and Kononen,

1994]
French Atlanticcoast

[Delmas et al., 1992] Chesapeake

Bay [Tyler

and Seliger,

1978]
Neuse River estuary

[Rudek et al., 1991] Baltic Sea [Wasmund,

1994]; Peel-Harvey estuary, Australia

[Lukatelich

and McComb,1986] BalticSea [Gran•li

et al., 1990] Changjiang

(Yangtse

River) plume,

China [Ning et al., 1988] TampaBay [Gardiner

and Dawes,

1987] Fraser River plume[Harrison

et al., 1991]; Sundays River estuary,

South Africa [Hilmer and Bate, 1991] Dutchcoastal

waters [Cad•e, 1990]; Narragansett

Bay [Verity

et al., 1988]

Black Sea [Sur et al., 1994]

Scandinavian

coastal waters [Maestrini

and Gran•li, 1991]
Norwegian

fjords [Kaartvedt

et al., 1991]132 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWSOF GEOPHYSICS

Table 3. (continued)

Class Distinguishing Features Common Genera Examples of Occurrence

Phototrophic chlorophyll-containing protozoans Mesodinium ciliates capable of rapid photosynthesis and population

growth; swimming structures

(cilia) allow rapidvertical migrations;

form intense

visible (nontoxic)

red tides;

a unique nonalgal

component

of the marine phytoplankton San Francisco Bay [Ctoern

et at., 1994]; PatosLagoon,Brazil [Abreu et at., 1994]; Sechelt Inlet, Canada [Haigh

et al., 1992];Southampton

Water, U.K. [Iriarte and Purdie, 1994];Strait of Georgia [Harrison

et al., 1983]

Based on the algal

taxonomy

of Chr•tiennot-Dinet

et al. [1993]and descriptions of Morals

[1967]and Sournia

[1982]. Algae are classified

on the basis

of their photosynthetic

pigments,

storage products (food reserves),

cell walls(external

coverings),

and number

and type of flagella (propulsive

organs).

rate is near zero and the biomass remains constant. 

### Phytoplankton

blooms are transient departuresfrom quasi-equilibrium

when the primaryproductivitytemporarily exceeds

the losses

and transports

and the population growsrapidly and reaches exceptionally

high bio

### mass [Paerl, 1988; Legendre, 1990]. Phytoplankton blooms usually are not single

discrete events but rather

are a series of fluctuations in which the biomass and the 

### species composition

(Table 3) of the phytoplanktonpopulation change

rapidly. We can very generally classifyblooms into three 

### types: (1) recurrent

seasonal events that usually

persist

over periodsof weeks,(2) aperiodic events that often persist for periods

of days[e.g., Takahashi et al., 1977], 

### and (3) exceptional

events that are typically

dominated by few species

(sometimes

noxious or toxicforms) and persist for months[e.g.,Nixon, 1989]. Seasonal blooms

can occurin spring[Malone et al., 1988;

Ziemannet al., 1991;Lignellet al., 1993],summer[Sinclair, 1978;Cole, 1989; Vant and Budd, 1993]; autumn [Zingone et al., 

### 1995], and winter [Hitchcock and Smayda,1977; MacKenzieand Gillespie,

1986; Sellner

et al., 1991]. These events are often dominated

by differentgroups

of species each season as the phytoplankton

community

adapts to changes

in resources

and the physical

environment 

### [Margalef,

1978;Smetacek

and Pollehne,

1986].A common annual

cycle begins with large

winter-spring

diatom blooms followedby summer

blooms of smallflagellates, dinoflagellates,

and diatoms and then autumn blooms 

### dominated

by dinoflagellates

[Smetacek,

1986; Tettet al., 1986; Mallin et al., 1991]. 

### The underlying

mechanisms

of phytoplankton

blooms

are diverse

and can be organized

with a simplepopulation budget

that describes

biomass fluctuations

at a fixed 

### geographic

reference,


### AB/At= -+(ix

- r) B - Gp- Gb-+E -+

X (1)

where AB is the change in phytoplankton

biomass over time increment At and terms on the right-hand side represent

the individual

process illustrated

in Plate 1: ix 

### is the growth rate, a function of light and nutrient 

### availability;

r is loss rate to respiration

(note that (ix - r) is the net growth

rate and (ix - r)B is the net rate of 

### biomass production);

Gpistheloss

rate to pelagic(zooplankton)

grazing; G b is the loss

rate to benthic

grazing; E represents

exchanges

of biomass

between the bottom 

### sediments

andoverlying

water column;

and X represents all horizontal

transports

by advective

and turbulent dif

### fusive processes.

Blooms are periods

in which AB/At is 

### large and positive,

so [from Legendre,

1990]


### (ix - r)B > > (Gp+ Gb+ E + X) (2)
Equation (2) can be satisfied under environmental conditions

in which the net growth

rate (ix - r) is large. When nutrients are abundant,the net growth rate is directly proportional

to light availability.

For example,

in 

### SanFrancisco

Bay, (ix - r) is correlated with the mean daily irradianceI to which phytoplankton cells are ex

### posed as they are movedwithin the water column by 

### turbulentmixing [Alpine and Cloern, 1988].The mean irradiancein a uniform mixed layer of thickness H is



### I • Io/(kH) (3)

whereI 0 is the dailyquantity of photosynthetically

active 

### radiation

penetrating

just below

the water surface

and k is the light attenuation

coefficient

hat defines

the exponential decay

of light with depth. 

### Equation(3) shows

that the depth-averaged quantity of light available

to sustain

phytoplankton

photosynthesisand growthis directlyproportional to surface

irradi

### ance I0 and inversely

proportional

to turbidity

k andthe depth scale

H. Bloomscan be triggeredby changes in each of these three quantities. The spring bloom in Swedish coastal waters beginswhen the daily surface irradianceI0 reaches

a threshold

value of about 30 E 

### m -2 d -1 [Bt•mstedt,

1985]. In Dutch coastal waters the spring bloom begins

first in offshore

regions where k is small and i reaches the threshold value earlier than in 

### the more turbid (high k) inshore regions [Gieskes and Kraay, 1975]. Short-term,aperiodic fluctuations

of phytoplanktonbiomass

can be caused

by wind events

that resuspend

fine bottom sediments and increase

k to the pointwhere meanI andthe net growth rate become

very small [Tett and Grenz, 1994]. Blooms often develop when the effective mixing34, 2 / REVIEWSOF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 133



### depthof thewater column (depthscale

H) is reduced

by verticalstratification.

If the water density

is uniform over 

### depth H, then wind and tidal stirringcan move phytoplankton cells rapidly betweenthe surface photic zone 

### (where sufficient

light exists

to sustain

photosynthesis and a positivenet growth rate) and the deeper aphotic



### zone (where light is absent and the net growth rate is negative). Surface heating and freshwater inputs are
sources of buoyancy

that can establish

vertical density 

### gradients

in the water column.

Strong verticalstratification can effectively

isolate phytoplankton in a shallow 

### (small H) surface

layerin which

the meanirradiance

I is much higherthan the irradianceaveraged over the full water columnheight.

As a result,the net growthrate of 

### phytoplankton

in the surfacelayer increases after the establishment of vertical stratification. Seasonal blooms



### can be triggered by seasonal fluctuations

in river flow 

### and the intensity of salinity stratification [Pennock, 1985]. At shorter timescales the intensity of vertical stratification

fluctuates

with changes

in the strength of 

### tidal stirring. Regular weekly fluctuationsof vertical stratification often coincide with the fortnightly neap

### spring tidal cycle,

with alternations

between well-mixed 

### (springtide) and stratified (neap tide) conditions. In many tidal SCEs the neap tide periods of enhanced stratification are periods of phytoplankton biomass growth,and the proximalagentof these weekly blooms is the increased

growth rate of phytoplankton confined in a shallow

surfacelayer [Winteret al., 1975; Sinclair, 1978;Haas et al., 1981;Cloern, 1984;de Madariagaet al., 

### 1989;Roden, 1994;Ragueneau et al., 1996]. The second critical resource for phytoplankton 

### growth is the pool of nutrientsrequiredfor the biosynthesis of new cells.The potential magnitude of phytoplankton blooms is set by the supplyrate of the least abundant nutrient elements. In addition, the growth 

### efficiency

of phytoplanktonin low-light habitats increases with nutrient availability [Cloern et al., 1995]. Therefore phytoplanktonblooms can be responses to seasonal

fluctuations

in the riverine inputs of nutrient 

### elements

such as N [Malone

et al., 1988]and P [McComb and Humphties, 1992]. Episodic blooms can follow 

### pulsedinputsof nutrients from runoff produced

in the local watershed during storms [Gallegos et al., 1992; 

### Hama and Handa, 1994], direct inputs of atmospheric nitrogen from rainfall [Paerl

et al., 1990],or the input of nutrients

from the coastal

ocean duringupwelling

events 

### [Lara-Lara et al., 1980]. 

### The necessary

condition

for bloom initiation (equation (2)) is that the primary productivity must be large relative to all mechanisms

of phytoplankton

loss,includ

### ing consumption

(grazing) by pelagicand benthic animals. Therefore blooms can develop through mechanisms that lead to reduced grazing loss. The spring 

### blooms in temperate and high-latitude coastalwaters begin when the zooplanktonbiomass and grazing rate


### are near their annualminima [B•mstedt, 1985]. Diatom bloomscan follow rapid declines in zooplankton

abundance

caused by episodes

of intense

predationon cope

### pods (small pelagic crustaceans

that feed on phytoplankton), so the timing and magnitudeof blooms can be regulated by top down processes originatingat higher trophic levels [Deason and Smayda,1982]. 

### In many SCEs the total biomass (and therefore potential grazing

rate) of the benthic

consumer

animals is muchhigher

than the biomass

of the copepods

and other 

### zooplankton [Cloern, 1982; Knox, 1986; Colijn et al., 1988].Suspension-feeding benthicinvertebrates,

such as 

### polychaete

worms andbivalve

mollusks (clams, mussels), actively removephytoplankton biomass from just above the sediment-water interface; other benthic animals con
### sume phytoplankton

biomass deposited

on the sediment surface. Therefore the rate of benthic grazing can be limited by the vertical flux of phytoplankton biomass
from the water column to the sediment-water interface 

### [Monismith

et al., 1990]. In south San FranciscoBay, blooms are controlled by the seasonal and weekly fluc

### tuationsin salinitystratification because strongstratification retardsthe turbulent diffusive flux of phytoplankton from the productive surface layer to the bottom zone 

### of active consumption

by benthicanimals.

Stratification acts to decouple

phytoplankton

from the bottom grazers 

### [Cloern, 1991b]. Therefore

stratification

promotes

blooms by (1) establishing

conditions

of rapid phytoplankton growthin the surface

layer and (2) slowing

the delivery of phytoplankton biomass to the benthic consumers [Koseff et al., 1993]. In some SCEs the rate of benthic grazingcontinually

overwhelms

phytoplankton

primary 

### production. This is the current situation in upper reaches of northern San Francisco Bay, where summer 

### blooms disappeared

after an exotic

clam(Potamocorbula amurensis)

became so abundant that its grazing rate balances

phytoplankton

productivity

[Alpine and Cloern, 

### 1992] (seeFigure

3b below).

Similar dramatic declines in phytoplankton

biomasshave been observedin other coastal systems after aquaculture

activities

increased

the abundance

of filter-feeding

mollusks

throughcultivation 

### [Motodaet al., 1987]. 

### The last term in (2) represents the horizontal

transports,which can also be mechanisms of bloom regulation. Plankton populations can be maintained in a coastal basinonlywhen the net rate of biomassproduc

### tion, (ix - r)B, exceeds the net rate of transport losses, X [Malone, 1977;

Kikuchiet al., 1992]. In SCEs coupled to large river systems, the hydraulic

residence

time can be shortrelativeto the phytoplankton population

growth 

### rate during periods of high discharge. Blooms can develop only when the river discharge falls to a level at which the residence

time within the SCE is longer than 

### the phytoplankton

population doubling

time [Cloern

et al., 1983;

Relexans et al., 1988].Horizontal transports can 

### be sourcesof phytoplanktonwhen coastal [Malone, 1977] or riverine [de Madariaga et al., 1992] blooms

are advected into coastal basins. Exceptional blooms can 

### follow exceptional

climate patterns

that cause

slowhor-134 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS



### izontal transportsand long hydraulic residencetime 

### within coastal

basins [Vieira and Chant, 1993]. 

### Other mechanisms

of water circulation

and mixing influence

plankton

dynamics.

The spring

bloomin Chesapeake Bay develops

when density-driven

circulations



### cause a landward

transport

and accumulat,

ion of phytoplankton biomass

in the upper estuary [Maloneet al., 1988].In south

San Francisco

Bay, localized

blooms that 

### develop over the lateral shallows are dissipated

quickly by strong

wind or river flow events that generate

pulses of enhanced

circulation

and rapid horizontal

transports 

### [Huzzey etal., 1990].

Red tide blooms

canbe triggered

by intrusions of coastal water that alter the vertical circu

### lationpattern

andcarry

dormant algal cells (cysts) from the sediments

to the water column,

where they seed

the 

### rapid population

growth of dinoflagellates

[Figueiras

and Pazos, 1991]. Sharp discontinuities between different 

### water masses

(fronts) can be sites of phytoplankton accumulation. Tidal fronts at the interface between shal

### low mixed

waters and deeperstratified

waters promote the growthand physical accumulation

of phytoplankton andcanbe zones

of intense

dinoflagellate

blooms[Simpsonand Hunter, 1974]. Buoyancy frontsbetween

a low

### salinity (low density)

and a high-salinity

water mass

can also be regions of active phytoplankton growth and accumulation

[Franks,1992]. 

### The conceptual

model outlined above placesgreat emphasis

on the changing

physical and chemical

environment as a mechanism of phytoplankton

population 

### change. However,it is important to remember

also that the plankton

species living in SCEshave

evolved in these habitats and acquired

behavioral,

biochemical,

and lifehistory adaptations

to the physical

and chemical

variabil

### ity characteristic

of coastalwaters. For example,the photosynthetic

ciliate Mesodinium

rubrum, which forms 

### visible red tides in SanFrancisco

Bay [Cloem

etal., 1994] and other temperate estuaries, has a behavioralmechanism that acts to retain this species within tidal SCEs: 

### active swimming

toward the surface

on incoming

flood tides, and then downward migrationto retard seaward 

### transports

by the ebb tides [Crawford and Purdie,1992]. Some dinoflagellates

[Horstmann,

1980]and other swim

### mingspecies

[Watanabe

et al., 1995]have

verticalmigrationscuedto the diurnal (daylight) cycle that allow for exploitation

of sunlight

at the surface

during the dayand nutrient resources

in the bottom watersat night. Other species produce restingcellsthat sink to the sediments when growth resources becomelimited; thesethen seed blooms when environmental conditions become favor

### able for populationgrowth [de Madariagaet al., 1989; 

### Figueiras

and Pazos, 1991]. Recent evidence suggests that overwintering

dormantstages

of somephytoplankton species

begin their developmentinto active cells 

### whenthe daylength

reaches about 13 hours

in spring,

so blooms of thesespecies

are life cycle

responses

cuedto 

### the annual photoperiodcycle [Eilertsen et al., 1995]. Therefore phytoplankton are not absolutely

passiveorganisms subjected

to the constraints

imposedby their 

### physical-chemical environment.

They havediverse

capabilities of adaptation.

THE SAN FRANCISCO BAY EXAMPLE



### A Representative

Shallow Coastal Ecosystem The sustained

investigation

of San FranciscoBay provides a case study to illustrate

the patterns

and mechanisms of phytoplankton

blooms in one shallow coastal ecosystem.

San Francisco

Bay is a useful site for comparativeestuarine

science because it comprises

two con

### nected,but distinct,

subsystems

(Figure 1). The north bay is the estuary

of the Sacramento

and San Joaquin 

### Rivers, which carry runoff rom a large (150,000 km 2)
watershed between the Sierra Nevada mountains and 

### the PacificOcean. The north bay has featurescharacteristic of partially mixedestuaries, including

large horizontalgradients

of salinity,

suspended

sediments,

nutrients,and biological

communities.

In contrast,

the south bay is a semienclosed basin with salinitythat is near

### oceanic during the low-flow seasons and is diluted by 

### freshwater

inputs during the high-flow winter-spring. The San Francisco Bay systemhas complex bottom topography

with broad shallow embayments that are incisedby a deeper channel,channel constrictionsbetween the embayments, and connection

to the Pacific 

### Oceanthrough

a deep (100 m), narrowentrance at the Golden Gate (Figure 1). The estuaryis nutrient-rich, with nutrient sources

dominated

by agricultural

inputs carried by river flow and sewage inputsfrom the local populationof 8 million. 

### Much of the phytoplankton population variability within San Francisco

Bay originates

with fluctuations

in 

### physical forcings at the oceanic,

atmospheric,

andwatershedinterfaces.

A primaryforcing

at the estuary-watershed interface is the input of fresh water, which has strong seasonal

and interannualvariability. Figure 2a shows fluctuations of the freshwater inflow to north San 

### Francisco

Bay during four of the years in which phytoplankton population variability has been measured. These records show that annual fluctuations in river flow



### are dominated

by a wet season

(from winter storms

and spring snowmelt)and a dry summer-autumn season when precipitation

stops. These records

also show

pronounced year-to-year fluctuation of river flow to San 

### Francisco

Bay: 1983

wasthe wettest

year of this century, 

### 1986 was dominatedby an extreme flood event (the highest recorded

flow of thiscentury),

andthe 1989and 1993 hydrographs

showseasonal

patternsof river flow during representative

dry and wet years, respectively. Freshwater inputs from the smaller local streamsare


### more immediately

responsive

to winter storms,

and local 

### streamflows

to the south

bay stopentirelyduringsum

### mer-autumn (Figure 2b). These seasonal and interannual fluctuations

in river flow are drivenby large-scale atmospheric

circulations

that control the strength and positionof the Pacifichigh-pressure system, which de-34 2 / REVIEWS OF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 135

122030 ' 122ø15;" 122000 ' 121"45'

37045 '

0 5 10 mi

0 5 10kin

Figure 1. Map of San Francisco Bay, a shallow

coastal ecosystem

influenced

by tides at the oceanic

boundary (the Golden Gate) and freshwater inflows at the watershed

boundaries.

Arrows show

sources and flows

of freshwater during periodsof high runoff. SFA is San Francisco InternationalAirport. The inset shows the drainage

basin and major tributaries

of the Sacramento-San JoaquinRiver system.



### flects moisture-bearing

storms to the north of California 

### [Peterson

et al., 1995]. Physical forcings at the estuary-atmosphere interface
include wind stress at the water surface that stirs the upper water column, resuspends bottom sediments,

and driveshorizontal circulations. In the San Francisco

Bay 

### region, windshave maximum

speeds in summer

(Figure 2c) associated

with the westerly

seabreeze [Conomos

et al., 1985]. Episodic

fluctuations

in wind stress

are associatedwith storms,

particularly

winter storms

that typically come from the southwest. Irradiance has regular seasonalperiodicity and daily fluctuations associated 

### with storms

and intrusions

of coastal

fog duringsummer 

### (Figure 2d). A primaryphysical

forcing at the estuary-ocean

interface is the tide, whichpropagates into San Francisco

Bay through the Golden Gate. In this regionof the northeast 

### Pacific, the tides have a strongsemidiurnal component with two unequal

flood and ebb cycles

every 24.84 hours. A second

important componentof the tide is the fort

### nightly neap-spring

cycle (Figure 2e) of two unequal spring and neap tides each lunar month (27.5 days).In the south bay the tidal amplitude (difference between water elevation

at high and low tide) is about 2 m, the tidal excursion

(horizontal

displacement

of a water parcel during a tidal cycle) ranges between7 km at neap tide and 13 km at spring tide, and maximum

tidal current 

### speed U is about 0.75 m s -• [Conomos,

1979a; Walters et al., 1985]. Therefore San Francisco Bay is a mesotidal SCE with tidal influence smaller than that in macrotidal 

### systems such as the English Channel and Bay of Fundy 

### (tidal amplitude > 10 m), but larger than in the microtidal Gulf of Mexico, Baltic Sea, and Mediterranean 

### Sea (tidal amplitude< 0.5 m).136 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS

150OO


# •10000

5000

z
o
300



## 200

lOO 

# -• o "*•i '•

15

• 10

-o 5 a

•, 6o

• 40

c: 20

0.7

0.5


### 0.4

1983 1986 1989 1993

Figure 2. Daily fluctuations of five physical forcings that influence

population

dynamics

of phytoplankton

in San Francisco Bay. Series are for four contrasting hydrologic

years (1983,1986,

1989, and 1993),

showing (a) netfreshwater

inflow from the Sacramento

and San JoaquinRivers (a calculated quantity, the Delta Outflow Index,from the CaliforniaDepartmentof Water Resources), (b) daily discharge

of a local stream (Patterson

Creek) that discharges into south San Francisco R•,x, (from 11R •oc•lc•glcml Suv:ey (L•, ni•_ trict), (c) meandaily

wind speed

at the San Francisco

airport (from the National Climatic Data Center, National Oceanic and Atmospheric

Administration),

(d) daily irradiance,

measured as quantum

flux of photosynthetically active radiation, and (e) m•imum dailytidal current speed in the channel

of south San Francisco

Bay, calculated

with harmonicconstants from long-term current measurements [Cheng and Ganner, 1985]. The Issue of Scale 

### Each of the physical

forcings illustrated

in Figure 2 contributes

to phytoplankton

population

variabilityby influencing

the ratesof verticalmixing, horizontal

transport, production,

or grazing.

Eachforcing

hascharacteristic timescales

of variability,

such asthe 12.42-hour

and 

### •-14-daytidal periods;

the diel (24 hours)light cycle; 2- to 5-daystorm

events of enhanced

streamflow

andwind stress; seasonal

cycles of irradiance and temperature; andthe pronounced

interannual

variability

of river flow. Therefore phytoplankton populations

in SCEs are ex

### posed to physical

forcings that have timescales

of variability ranging from hours to years: "a hierarchy of forcingfunctions

which drive the various biological

response mechanisms

at different

time and length scales" [Mackas etal., 1985,

p. 653]. Each of these

timescales

can be identified in the population fluctuations

of the phytoplankton. Biomass fluctuations at the short timescales can be
measured with moored fluorometers that detect and 

### record chlorophyll

fluorescence

at a fixed location.

A samplerecord in Figure 3a shows a 2-week series

of hourly measurements

in south San Francisco Bay. The first week of the record shows periodic fluctuations

in 

### chlorophyll

fluorescence

over the semidiurnal

tidal period, with chlorophyll

peaksat the two low slack tides each day. This high-frequency variability is caused

by tidal advection

as chlorophyll

spatialgradients

oscillate

over the sensor

with the tide [Cloemet al., 1989]. Spec

### tral analyses

of suchchlorophyll

series confirma high varianceat the tidal frequencies [Litaker et al., 1993]. Short-term

fluctuations

can result from other processes 

### such asdiel cycles

of chlorophyll

synthesis

andzooplankton grazing [Litakeret al., 1993] and wind-waveresus

### pension of algal cells off the bottom[Demers

et al., 1987; de Jonge

and van Beusekom,

1995]. The second

half of 

### the record in Figure 3a shows a 6-day period of expo

### nentialchlorophyll

increase.

Here the semidiurnal

tidal variability

is overwhelmed

by the rapid growth

of phyto

### plankton

biomass along the entire channel;

this period of the record illustrates daily-scale

variability during a 

### bloom event. Day-to-day fluctuations

in phytoplankton biomass or physiological

condition

are commonly

associated with hydrologic-meteorologic events, such asrainfall pulses,

wind events,

or periodsof abrupt warming 

### [C6t• and Platt, 1983], and with fluctuations in tidal mixing overthe neap-spring

period [Sinclair

et al., 1981; Cloem, 199

lb ]. Longer-termfluctuations of phytoplankton

biomass

are illustrated

in Figure 3b, a series

of monthlychloro

### phyll a measurements

in north San Francisco Bay from 1974 to 1995. Three scales of variability are evident in 

### this record: a seasonal cycle with peak biomass

during the low-flow summers,interannual variability with a 

### damped summer bloom during

yearsof extremely

high river flow and shortresidence time (e.g., 1983), and an apparent

permanent

change in the natureof the record, with the virtual disappearance of summer

blooms after34, 2 / REVIEWS OF GEOPHYSICS Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 137

40

•ø• 30

o (D oo 20

'• 10

0 

# Semi-diurnal

_ variability ' Y

1 2 4 5 7 8 i i i i i i 

## •--"•----'-----':•;%

daily variability F 

# • ' - ofa ,bo•t •,)• -

9 10 11 12 13 14 15

March, 1995

b 

# '• 4o,-- Seasonal

Interannual , ""'"':•:•:••

•"•'....'•• :• / I • variabili• variabili

• 30 -

o 20 

### • persistent

. -

e 10

o 1976 1978 198o 1982 1984 1986 1988 199o 1992 1994 1996

Figure 3. Some

timescales

of phytoplankton

biomass variability

in San Francisco

Bay. (a) A 14-day

record of hourlymeasurements with an in situfluorometer placed 2 m above

the bottomnear station 28 in south

San Francisco

Bay (Figure5); the fluorometer wascalibrated

with discrete

chlorophyll

a measurements

madeat the beginning

andendof the record

(fluorometer

data from D. A. Cacchione,

personal communication,

1995). (b) A 21-year

record of monthly

(or semimonthly)

measurements

of surface

chlorophyll

a concentration

ear station 5 in north San Francisco Bay (Figure 1); this recordincludes data from the CaliforniaDepartmentof Water Resources

(1974-1986) and USGS (1986-1995).



### the North Bay was colonizedin large numbers by the clam Potamocorbula

amurensis

in 1987.Jassby

and Pow

### ell [1994] examined

a period of this chlorophyll record and concluded

that most of the interannual variability is 

### driven by two hydrodynamic processes,

one associated 

### with fluctuations

in river flow (a natural source of variability), and one associated with managed

diversions

of fresh water from the upper estuary (an anthropogenic

source of variability). 

### Spatial variability

(patchiness)

is also observed

across
a spectrum

of scales [Mackas et al., 1985].Phytoplankton patchiness

can be measured

with continuous

profiles of chlorophyll

fluorescence

along horizontal

transects

[Wilson and Okubo, 1980; Childers et al., 1994;A.D. Jassby et al., Towards the design of sampling networks for 

### characterizing

water quality changes in estuaries,

submitted to Estuadne,Coastal,and Shelf Science, 1996]. Horizontal variability in south San Francisco Bay is illustratedin Figure 4, which shows the spatialstructure 

### of chlorophyll

fluorescence

alonga longitudinal

channel 

### transect (Figure 4a) and along a transverse transect between the channel

and adjacent

shallows (Figure 4b). The longitudinal profiles show measurements spaced every25 m, and variability is evidenteven at this small spatial scale. This small-scale

variability

is superimposed 

### onto larger-scale

patterns (mesoscale

variability) that often show trends of decreasing

chlorophyll

fluorescence 

### in the seaward

direction

(February

28, 1995;Figure 4a) and increasing

chlorophyll

across the shallows

(March 21, 1985; Figure 4b). Both small-scale and mesoscale patchiness

are influencedby hydrodynamic processes because the plankton are transported by their fluid environment [Mackaset al., 1985]. Therefore the spatial variability patterns,

both of chlorophyll

biomass and of individual

species [e.g.,Kononen

et al., 1992;Zingone

et al., 1995], are shaped

by the turbulent advectivetransportsof phytoplankton within a spatially

variablegrowth environment.

These featuresof spatial structure are not 

### stableor persistent.

The mesoscale

trendschange

from

season to season[Glibert et al., 1995] and day to day [Wilson and Okubo, 1980],

while the small-scale

variability changes

over the tidal period [Dustanand Pinckney, 1989]. 

### Figures3 and 4 show

that phytoplankton

biomass in shallow coastal ecosystems varies at timescales

from hours to decades and at spatial scalesfrom tens of metersto tens of kilometers. Levin [1992] suggests

that 

### the centralproblemin ecology is the problem

of pattern and scale,

where pattern is the description of spatial or 

### temporalvariabilityand the mechanisms of pattern formation are scale-dependent. Therefore studies

of populationfluctuations

such asphytoplankton

blooms require138 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS 34 2 / REVIEWS OF GEOPHYSICS



# • 50 A • "•B•-:•:•.•__•

• • • ]

,T 40



### '• 30

Fa 20

• •0



### 05 10 15 20 25 30 35 40 b 

# 50 • • • • D

40

30

20- -

10

c

o • • • i • o 2 4 6 8 lO 12

Distance (kin)



### Figure 4. Horizontal

variability

of phytoplankton

biomass from continuous

measures of chlorophyll

fuorescence along (a) longitudinal

transects and(b) a lateral

transect of south San Francisco

Bay. Near-surface waterwas pumped

to a shipboard

fluorometer

that wascalibrated

with 6-10 discrete

measurements

of chlorophyll

a concentration

taken along each transect. Inset maps show locations of the transects.



### explicit choices about the scales

at which population variability

can be observed

andexplained.

The long-term 

### observational

programin San Francisco Bay was designed to characterize

mesoscale

spatial variability

along the longitudinal

axis, at timescales

of weeksto years. 

### Eventhough

(large) population

variance exists at other scales, the data set described below is not appropriate 

### for analysis of the small-scale

fluctuations

illustrated

in Figures 3 and 4.



### The SouthSan Francisco Bay Data Set



### Patterns of Variability. South San Francisco Bay has been the site of focused research on phytoplankton

122030 '

.:.:.-......:• Central 

### Bay...._

37045 '

37o30 ' 122ø15; ' 122000 '

Figure 5. Map of south San Francisco

Bayshowing locations

of fixedsampling

stations along the longitudinal

channel.34, 2 / REVIEWSOF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 139

Table 4. Phytoplankton SpeciesCommonly Observed During Spring Blooms in South San Francisco Bay

Class Species

Diatomophyceae

Chlorophyceae

Chrysophyceae

Cryptophyceae

Dinophyceae

Prasinophyceae

Photosynthetic ciliates Diatoms

Chaetoceros debile Chaetoceros

decipiens Chaetoceros

didymus Chaetoceros

gracilis Chaetoceros socialis Chaetoceros vistulae Chaetoceros

wighami Coscinodiscus

curvatulus

(Actinocyclus curvatulus) Coscinodiscus

lineatus (Thalassiosira leptopus) Coscinodiscus radiatus Cyclotella

meneghiniana Cyclotella

sp. Cyclotella

striata Ditylum brightwelii Eucampia

zoodiacus Leptocylindrus

minimus Nitzschia

seriata (Pseudo-nitzschia

seriata) Paralia sulcata Rhizosolenia

setigera Skeletonema costatum Thalassiosira

decipiens

(Thalassiosira angulata) Thalassiosira rotula

Nondiatoms Chlorella marina Chlorella salina Monoraphidium

convolutum Nannochloris atomus Chromulina

sp. Kephyrion

sp. Ochromonas

sp. Chroomonas

acuta (Teleaulax

acuta ) Chroomonas

amphioxeia

(Teleaulax amphioxeia

) Chroomonas

alina (Rhodomonas

alina) Gonyaulax

tamarensis

(Alexandrium ostenfeldii) Heterocapsa

triquetra Katodinium rotundatum
Prorocentrum minimum Protoperidinium

claudicans Pyramimonas

micron(or P. orientalis) Tetraselmis

gracilis Mesodinium rubrum

From samples

taken during 1992-1995 and microscopicenumerations/identifications

of R. G. Dufford (personal communications, 1992-1995). Names in parentheses are revisions

basedon the taxonomy of Tomas[1993, 1996].

bloom dynamics

becauseit has a recurrent, somewhat 

### predictable

period of rapid biomass increase duringthe spring months.This lagoon-like basin has an irregular 

### bottom topography

with sharp bathymetric transitions between the 10- to 25-m-deep axial channel and the 

### lateral shallows

(Figure 5), and a large transverse shoal 

### (San Bruno) that slows horizontalexchanges

between the seaward and landward

estuary. Local streams

carry 

### runoff to the lower (landward)estuary. The open connection to the central bay allows fresh water from the 

### Sacramento

and San JoaquinRivers to intrude into the 

### southbay during periods of high river flow (Figure 1) and allowstidal exchange between the South Bay and 

### coastal ocean. The basin's

residual (tidally averaged) circulationis slow,with mean seaward flow along the eastern shallows

and landward flow along the channel [Chengand Gartner, 1985] and a hydraulic residence 

### time of several

months[Walters

et al., 1985].This weak

mean circulation

can be disrupted

by strong

wind events

or freshwater

inputs that alter the strength

and direction 

### of the residual

flows[Huzzey

et al., 1990].Water density is often vertically

uniform, indicating

rapid vertical mixing of the water column. The channelcan becomesalin

### ity stratified after periods of runoff that deliver lowdensity fresh water as a source of buoyancy, but 

### stratification

occursonly during neap tides when the tidal stirring is weak [Cloern, 1984]. Phytoplanktonprimary production

is the largest

source of organic

carbon to south San FranciscoBay [Jassby et al., 1993], and much of the total annual primary production occurs 

### duringthe spring[Coleet al., 1986]. The southSan Francisco Bay spring

bloom has been followed every year since 1978, and the patterns of variability within this series can be used to illustrate



### some generallessons

of phytoplankton

bloom dynamics in SCEs. The core measurement program.in south San 

### Francisco

Bay includes

vertical profilesof salinity,tem

### perature, chlorophyll

(by calibrated

fluorometry),and turbidity at sampling

stations (Figure 5) spaced

about every3-4 km alongthe channel(detailed methods are 

### given in annual

data reports

[e.g., Edmunds

etal., 1995]). Water samples

are alsotaken for microscopicexamina

### tion to determine

the abundance

of phytoplankton

spe

### cies presentduring the springblooms (Table 4). The sampling frequency in 1978-1979 was once monthly; 

### after 1979the sampling frequency

was increased

to once
or twiceweekly duringthe period of the springblooms. Bloom dynamics

are characterized

here with the chlorophyll measurements made along the channeltransect 

### (Figure 5). Near-surface chlorophyll

is used as a measure of biomass

in the photic

zone (i.e., the quantity

that contributes

to primary

production),

andvertical

variability is not considered

here. Lateral variability is also not considered,although there is coherence between the seasonal dynamics of phytoplankton biomass in the channeland adjacent

shallows

[Cloern and Cheng,1981; 

### Cloern et al., 1985; Vidergar

et al., 1993]. Plate 2 depicts the chlorophyll

fluctuations

in southSan Francisco Bay with color, and several prominent patternsof variability 

### stand out. First, the solid background shows that bio

### mass isusually less than 5 Ixg L- 1chlorophyll

a. Second,

a period of rapid biomassgrowth (a bloom) occurs duringthe spring

of every year. Third, bloom intensity is often greatest in the landward estuary,consistent with the trends in the high-resolution chlorophyll

transects.140 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS 34 2 / REVIEWS OF GEOPHYSICS



# Ba/• Bridge

78 

# San

Mateo Bri%ge Dumbarton Bridge

8O

82

84

• 86

88

9o

92

94

0 5 10 15 20 25 30 35

Distance along channel transect, in kilometers

....... I

.. I I I I I 5 10 15 20 25 30 35 40

Chlorophyll

a

Plate 2. Color representation of spatial-temporal

variability of phytoplanktonbiomass (chlorophyll a concentration)

in south San Francisco

Bay. Blooms

are shown

asdepartures

from the low background biomass (green), with bloomintensity

proportional

to color brightness.

The vertical

axis represents

time from January 1978 to July 1995, and the horizontal axis represents spatialvariability along the channeltransect from the seaward estuary (station 21) to the landward

estuary (station 32). Color contours

were produced

from a matrix of interpolated

valuesbased

on 4449 measurements of surface

chlorophyll

a concentration

on 417 dates.34, 2 / REVIEWS OF GEOPHYSICS Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 141

1.0

0.8

0.6

0.4

0.2

1.0

0.8

0.6

0.4

0.2 PC1 = 52% of Variance

21 22 23 24 25 26 27 Station PC2 = 35% of Variance

28 29 30 31 32 Figure 6. Coefficients (loadings)

of the first two principalcomponents, which account

for 87% of the chlorophyll variance along the south San Francisco Bay transect, for the period January 1978 to July 1995. Principal 

### component

analysis was done on•hecorrelation matrix, and results are varimax-rotated solutions

[Jassby and Powell,1990].

This analysissuggests

two independent

spatial modes of phytoplankton biomass variability: one (PC1) in the landward

estuarine

basinsouth of station 25, and a second(PC2) in the seaward estuarynorth of station 25.



### Finally, the nature of the springbloom changes from year to year. For example, the 1986 spring

bloomwas a monthlong

event of very high chlorophyll concentration 

### (maximum

>70 !xg L-•) along

theentire transect. The 1991 spring

bloom was a short-lived event confined

to the landward

estuary, where maximum

chlorophyll

con

### centration

was only 12 !xg L-•. Thepatterns

revealed in this image illustrate

two lessons

that apply generally

to 

### shallow coastal ecosystems:

(1) phytoplankfon

blooms

are spatiallyheterogeneous, and (2) the timing and magnitude

of the seasonal

blooms change from year to

year. 

### The patterns of populationvariability in time and spacecan be formalized with multivariate techniques 

### such as principal components analysis (PCA). If we consider measurements

at sampling

stations as variables, and sampling

dates as individual cases, then PCA can 

### reveal patterns of spatial coherencein the temporal fluctuations

of biomass

along a transect.

This PCA of the south San Francisco

Bay data set identifies

two principal 

### components

that togetheraccount

for 87% of the total chlorophyll variance. The first principal component 

### (PC1), whichaccounts

for 52% of the chlorophyllvariance, hassmallcoefficients

(or loadings)

at the seaward stations and progressively

largercoefficients

at the land

### ward stations

(Figure6). The second

component

(PC2), accounting

for an additional 35% of the variance, has largest coefficients

at the seawardstations. This PCA shows that most

of the phytoplankton

biomass variability in south San Francisco Bay can be explained

with only 

### two spatial modes (patterns): the first is expressed strongly in that regionof the estuary landwardof station 25, and the second

is expressed

strongly in the region of 

### the estuary

seaward of station

25 (Figure 6). This separation of the two spatialmodes at station

25 corresponds 

### to the location of the San Bruno Shoal (Figure 5), a topographiccontrol of horizontal mixing. The tidally averaged

circulationof south San Francisco Bay is char

### acterized

by a slowly

rotating gyre that acts to retain fluid 

### within the central basin of the estuary, below the San Bruno Shoal [Cheng

and Casulli,1982].The PCA result is consistent with this mean circulation that maintains 

### two spatialdomains

separated

by a topographic

control of mixing [Powellet al., 1986]. This lessonapplies to other coastal ecosystems where the mesoscale spatial variability

of plankton reflects

the water circulation

patten [Jouffre

et al., 1991] and where distinct spatial domains can have different temporal patterns of bloom 

### evolution [Therriault

and Levasseur,

1986; Kahru and Nbmmann, 1990; Glibertet al., 1995]. A second

result of PCA is the series of scalarampli

### tudes (or scores)

that express

the relativeimportance of eachprincipalcomponent over time [Jassby

and Powell, 

### 1990]. Figure 7 shows

the time series

of amplitudes

for PC1. This series is a representation of pattern in the 

### temporal variability of phytoplankton biomassin the landwardbasin.This temporal pattern is dominatedby 

### episodic spikes that occur

in the spring

of each year,with142 ß C!oern' COASTAL PHYTOPLANKTON BLOOMS 34, 2/REVIEWS OF GEOPHYSICS

'•' 30



## o•.•, :20 

# lO

I I I I I I I I I I I I

6

m

m

E 1--

0 m

_1 m

_2 /

78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 Year Figure7. (bottom) Time series

of amplitudes (scores) for the first principalcomponent of chlorophyll

variability in south San Francisco Bay. Large amplitudes correspond

to events

of high phytoplankton

biomass (blooms)in the landward

estuary. (top) Parallel

series of nearsurface salinity in the landward

estuary (mean of measurements

at stations

26-32), illustrating that blooms

occur during the wet season

of high river flow and annual salinity minima.



### prominent

year-to-year

fluctuation

in the timing, duration, and magnitudeof these spikes. 

### Mechanisms

of variability. The series of principal component

amplitudes

in Figure7 is consistent with the notion of phytoplankton blooms as departures from 

### population quasi-equilibrium. Blooms are population outbursts

that can appearand dissipate within a period of weeks.

What determines

the timing of these

outbursts, their duration, and their magnitude,and why do these features changefrom year to year? The two series in 

### Figure 7 show

that blooms

occurin south

San Francisco 

### Bay during the wet season, when surface salinity is 

### diluted by fresh water. This seasonal

coherence

between bloom developmentand low salinity results, in part, from the stabilization

of the water column

by the salinity 

### stratification induced by freshwater inflows [Cloern, 1991a, hi. The absence

of blooms

in summer-autumn

is 

### also a response

to the seasonal

cYCles of the benthic suspensiOn-feeding

animals, whose biomass and grazing rate are highest in summer. Therefore the seasonal 

### distribution

of blooms

in this particular

estuary appears

........ 1 • _•

_ •._

.... 

### to be a response

to seasonat

nuctuatlons

in nyurmogy 

### (riverflowandits influence on density

stratification)

and trophic interactions

(grazinglosses

to benthicconsumers). At shorter timescales, too, the timing of blooms is 

### regulatedby physical

processes

that influence

the balance between phytoplankton production and losses. Simulation experiments with numerical models show that this balance is sensitive

to the rate of vertical mixing 

### in the water column [Cloern, 1991b]. Vertical mixingis brought about bytidal stresses

applied at the bottom

and wind stresses

on the water surface

[Simpson

et al., 1991],
and in mesotidal SCEs the tidal stresses often dominate. 

### Weak tidal stirring

promotes

blooms by (1) slowing

the turbulent diffusive

lossof phytoplankton

biomass from 

### the photiczone [Koseff et al., 1993], (2) deepening the photic zone (growth habitat) as tidal resuspension of 

### bottom sediments

weakens [Schoellhamer,

1996], and(3) reducingthe vertical flux of phytoplankton to benthic



### consumer

animals [Cloern, 1991b]. Blooms developduring periods of weak tidal energy, and they dissipate during periods of strong tidal energy. This lesson is illustrated

in Figure 8, which shows the evolution

of the 

### 1985 spring

bloom and the simultaneous changes in the 

### dailytidal current

amplitude

U. Rapid biomass

(chloro

### phyll) growth occurredduring the neap tide in late March; this bloom dissipated soonafter the subsequent 

### spring tide in early

April. The association

between weekly-scalechlorophyll 

### vanatomy

andthe uuax

re -me •sa prominent

........ of phytoplankton

population

dynamics

in southSan Francisco Bay. This association is illustrated in Figure 9, which shows

a linear relationship

between the rate of biomass change and the antecedent

tidal current speeds 

### for all the large springbloomsobserved between 1978 and 1995.The rate of biomass change, R, wascalculated

as34, 2 / REVIEWSOF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 143

0.7

0.6

0.5

0.4
I I I I I I I

30 /

20•

10 /

.e'

I ' I 

### 79-,%b 10-/l•a

r I 

### 20-1•ar ' I 

### 30-graf

1985 I I



### 19-4,0 r Figure 8. The 1985 springbloom in south

San Francisco

Bay: (bottom) weeklyfluctuations of phytoplankton biomass in the landward estuary

(meanchlorophyll

a concentration at stations 26-32) and (top) daily fluctuations

in the tidal currentamplitude U. Current amplitudes were computed from tidal harmonicconstants derivedfrom longterm current measurements in the central south bay channel

[Cheng and Gartner,1985] (predicted U from J. W. Gartner (personal communication,

1995)). Biomassincreased rapidly after March 20, when U was less than 0.5 ms -•.

0.2 •

0.1 /

0.4 

## ß 'e89 4

95

0.5 0.6 

### Mean Current Amplitude U 7 (m/s) 0.7 Figure 9. Tidal forcing and phytoplankton blooms in south San Francisco

Bay.The net rate of biomass

change, R, was calculated from the week-to-week changesin mean chlorophyll

a concentration

in the landward estuary (stations 26-32). The tidal regimeis represented

by the 7-day mean current amplitude, U7. Points

represent

all the weeklyscale events of 1978-1995 in which the

meanchlorophyll

a concentration

fell below


### or increased

above 10 Ixg L- • (updated

and revised from Figure 4 of Cloern [1991b]). The dashed

line is the least squaresregression of R against

U7 (r = 0.66). Deviations around this regression in 1983, 1989, 1990, and 1995 are examined in Figures10-13 to illustrate other mechanisms of bloom variability.144 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS

Distance (km)

0 10 20 30 40

10 "•:•'

.......... .•i?.'ii•!,?,•i,•.

.... 

## 15 - .::

........... :?.-:-

20-

>26

5 - 24 22 20 18 16 14 <13

.. ::: !::!::•::-'::•!::•!:[i::!i!i::!!::i!::

............ •i•...•....•.•.•i[•[i[•:....•:....•...i!•!!•...•..•i•i•i;..•.•!i;..•i

i•ii!•:-:i --• 

## Salinity •i!',!!!?.'!:!:i!..:

........ ?'""•:'"'"•1
>28 27 25 

# i ...' ".'.:..:.::...::..:..::....:::•:. ß •

...... -: "-

..:--.......-•ii ::.-

....... •::-:: .;•-. :•:•: :: : :d: :•:::: -::. .:.

. .

.
ß 10- ;.



### i•i•!•:?•!•ii•i•i•:ii?•!•i•;

..... '

... 10

15 - 15

20 - 20 Distance (km)
O0 10 20 30 40 g'-.2j:•-•i!::iii•:'"----:-'---•::-.... "-'•il;-":g•i:•iiii?::::1111iii'#..

.";':'::!iii!::i::iii::i::i::::::i:" ".:i...:'•i•;;--':.-i•..

:ii!::i•i::i:;::i•!• ':• 

# !•;•i•.g•.:•i•:;..i.•.....•.•`..i•;•`..•.•.....?.`:.:..•i•i•i•i•i.•i;.....:4......•;;• ':":•1⁄2i•i•.' •:"•-"•:•i[?-::.-'i-'•.'.'• :':!•i•i![!•i•i!::i•i.:-::!..:-•:i•::::: !:•.•

....... - ...........

20

432<1 Mar-May River Flow (m3/s)

5000 3000 1000 0 

### i i i i 1978

1980

1982

1984

1986

1988

1990

1992

Figure 10. Sectional(vertical-longitudinal) contour plots of the (left) salinity and (right) chlorophyll a distributions

alongthe southSan Francisco Bay channel,

goingfrom the seaward (station21) to landward (station 32) estuary.

Top panels

show strong vertical gradients

in May 1983

following

a periodof exceptionally high river discharge.

Bottom panels showvertical homogeneity in May 1989 that is representative of the estuarine

condition

after periods

of lower river flow. The mean freshwater inflow to north San Francisco Bay (Delta Outflow Index, from the California Department of Water Resources) for the months

March-May is shown at far right. The springof 1983 was the wettest in this century.



### R = In [Bt+/,t/B

t]/At (4)

where n t+At is biomass(mean chlorophylla in the 

### landward estuary) at time t + At; Bt is biomass at previous time t; and R(1/d) is the specific rate of biomass change over time increment

At. The rate R represents the net result of all the processes of biomass change.This net rate is inverselyrelated to the tidal 

### current amplitudeaveraged over the previous

week, U7 

### (Figure9). The distribution of points

in Figure9 shows that the biomass

change R was always

positive (i.e., a 

### bloom developed)

when U7 was less than0.5 m s-•: phytoplankton

biomass increased

duringextremely

weak 

### neap tides. Conversely, R was always

negative when U7 

### exceeded 0.6m s-•: blooms

dissipated

during thehighly energeticspringtides. For tidal regimesbetween these extremes,

R was either positive

or negative:

bloomscan either grow or dissipate at intermediatetidal energies. The linear relation between R and U7 suggests that the timing of bloom inceptionis set by the astronomical tides. However, deviations around this linear relation



### are large, especially

at the intermediate tidal regimes 

### (Figure9), so other processes mustcomeinto play.The individual deviations around the linear relation between R and U7 can reveal some of theseother mechanisms of population variability. As an example, the rate of bio

### mass growthduringMay 1983 wasmuchlargerthan that 

### predicted from the tidal regime alone (see Figure 9). This positive

deviation

(+R) from the linear model can be explainedby the unusual hydrography of 1983: exceptionally

high river flow and strongsalinitystratifica

### tion that persisted

into May (Figure 10). The intense stratification

observed

in May of 1983 (but not other years)stimulated

rapid biomass

increases

in the surface layer.The combined

effects of large buoyancy

input plus weak tidal stirring created an unusually stable water 

### column and unusually

largeblooms

during 1983(Figure 7). Therefore the year-to-yearfluctuations in spring bloom magnitude

are determined partly by annual fluc

### tuationsin precipitation and river flow, with exception

### ally large blooms

(1982, 1983, 1986, 1995) during years of exceptionally

high river flow [Cloern

andJassby,

1995]. Climate can modulate the development of blooms in 

### otherways.

The positive

growthrate deviation

(+R) in 1990 occurredduring a period of unusually calm winds 

### in late March and early April (Figure 11), when the bloom magnitude

was amplified by the small inputs of mixingenergy

at the surface

[Koseff et al., 1993]. On the 

### other hand,the negative growth-rate

deviation

(-R) in 1989 followed an event of strong westerly winds that

--1 

### persisted

for severaldays.

Westerly winds of 10 rn s generate

a seaward

flow alongthe channel at speeds

up 

### to 10 km d

-1 [Walters,

1982; Cheng andCasulli,

1982].34, 2 / REVIEWS OF GEOPHYSICS Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 145

0.7

0.6

0.5

0.4 I I I I I

30

20 /

10•

o 

### 2o-•ar •o-•ar 9',q•r

1990 Figure 11. The 1990 spring bloom in south SanFrancisco

Bay.(bottom) Weekly changes

in chlorophyll

a concentration in the landward estuary (dashed line) and daily

fluctuations

in

mean wind speed (solid line). The horizontal line shows the long-term

mean wind speed for March-April 

### (5.6m s-•). (top)

The7-day

running

mean tidal current amplitude U?. A period of unusually

rapid biomass

increase (+R) occurred

in earlyApril, following2 weeksof unusually calm
winds.



### Therefore the negative deviation in early March 1989 

### (Figure 12) was probably the result of wind-driven pulsed flowsthat carried phytoplankton biomass away from the landwardestuary, coupled with the negative effects of rapidvertical

mixing by the surface

wind stress. 

### The negative

growth rate deviation(-R) in 1995 illustrates

another mechanism

of bloom regulation.

The 

### 1995 spring bloom began in late February, and high 

### biomass persisted

for over a month. This period of sustained

high biomass

led to a steady depletion of dissolved

inorganic

nitrogen(Figure 13) as the phytoplankton assimilated

nutrients faster than they were replaced by inputsand regeneration. By late March the 

### initial high stock of dissolved inorganicnitrogenwas exhausted,

and the potential rate of further biomass production

became limited by the availability of N. As a 

### result, the phytoplankton biomass declinedrapidly in earlyApril. This example illustrates

that phytoplankton biomass production

can be episodically

nutrient limited,

even in SCEsthat receivelarge inputs of nutrients.



### A Synthetic

Picture of BloomMechanisms This detailed analysis of chlorophyll

variability in 

### south San Francisco

Bay leadsto a generalpicture of how the timing and magnitudeof the spring bloom change fromyearto year.

The proximal

agents of blooms

are changes

in the physical

stateof the estuary

as deter

### mined by inputs of energy at the interfaces with the 

### coastal

ocean,rivers,and the atmosphere (Figure 14). Tidesoriginate

in the ocean,

propagate

into the estuary, and influence

turbidity and light availability for photosynthesis

(through tidal resuspension of bottom sedi

### ments), the intensity

of turbulentmixing,and the patterns of horizontalcirculation. The strength

of the tidal 

### forcing fluctuates,

and episodes

of minimaltidal energy 

### occur within each neap-spring

and lunar monthly period. The monthly

minimum

tidescreatea physical

condition that promotes

bloom development

hrough severaldifferent mechanisms,

and these periods of weak tides 

### providewindows

of opportunity

for the phytoplankton population

to grow. The timingof potential bloom development is set by the astronomical tides and is therefore 

### predictable

in estuaries

uch assouth SanFrancisco

Bay. The degree

to which phytoplankton populations

can respond to the tidal windowsis determinedby hydrol

### ogy, weather, nutrient availability, and the activity of

consumer

organisms.

River flow delivers

freshwater that 

### establishes

density-driven

circulations,

and it is a source 

### of buoyancy

to stratify the water column and inhibit vertical mixing.If freshwater buoyancy

inputsare large 

### enough to offsetthe effects

of tidal and wind stirring, then the water column remains stratified for a suffi

### ciently longperiod

that phytoplankton

biomass cangrow and reach high levels.

Other sources

of buoyancy,

such



### as rapid heatingof the surface layer during periods

of calm, stable weather, can have the same effect. Winds146 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS

0.7

0.6

0.5

0.4

3o

2o

lO



## 9"c'eb 19.F.eb •9.F.eb 10.•ar •O'•a r 30'•ar

1989 12

lO•

8 _m.

6 •

4• Figure 12. The 1989 spring bloom in south SanFrancisco

Bay. (bottom) Weekly changes

in chlorophyll

a concentration in the landward estuary (dashed line) and daily

fluctuations

in

mean wind speed (solid line). The horizontal line shows the long-term

mean wind speed for March-April 

### (5.6m s-•). (top)

The 7-day

running

mean tidal current amplitude U7. The rapid biomass

decline (-R) in early March followed a storm when daily wind speeds exceeded 12 m s-•.



### further influence

the development

of blooms

by altering the circulation

patterns and transport

of phytoplankton, 

### turbidity and the light climate

(through wind-wave

resuspension of bottom

sediments),

and the breakdown

of strat

### ification andenhancement

of vertical

mixing (Figure 14). The magnitude of the spring bloom in south San Francisco Bay is set by the initial stocksof nutrients 

### required for biomass

production,

the water circulation pattern as it determines phytoplankton

residence

time within the estuarine

basin, the potentiallosses

to pelagic and benthic grazers,

and the particular combination of climatic-hydrologic

onditions

duringthe tidal windows

30--

20--

_

lO--



### 9-F'eb 19.F.eb

'•9.F.eb 

## 6-6

10-•a r •O-•a r 30-•a r 9-•i1• r 1995 -- 5O

40 ---• Z

o 

### •30•

o 20:3

• 10 Figure 13. The 1995 spring bloom

in south San Francisco Bay. The dashed line shows

the weekly fluctuationsin mean chlorophyll a concentration in the landward estuary(stations 26-32); the solid line shows parallel changes

in the concentration of dissolved

inorganic

nitrogen (DIN

= nitrate + nitrite + ammonium). The eventof unusually rapid biomass decline (-R) in_ earl_y April occurred after the large initial stock of inorganicnitrogenbecame depleted.Nutrient datafrom S.W. Hager (personal communication,

1995).34, 2 / REVIEWS OF GEOPHYSICS Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 147

River Inflows

...

Figure 14. Cartoon diagrams of three physical

forcings that operate at the interfacebetween SCEs and the coastal ocean (tides), watershed

(river inflow),and atmosphere (wind). Each physical

forcing influences

the 

### growth rateof the resident

phytoplankton

population

through, for example,

its influence

on thedistribution of suspended

sediments

and turbidity.

Each forcing

alsoinfluences

the rate of verticalmixing, with riverine inputs of fresh water as a source

of buoyancy

to stratify

the water column

and the tide andwind as sources of kinetic energyto mix the water column. Each forcing is also a mechanism of water circulation

that transports

phytoplankton

horizontally.

Much of thevariability

of phytoplankton

biomass during blooms can be understood

as responses

to fluctuations

in theseinterfacial

forcings.148 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS

OCEAN RIVER

ß Small pelagic Reactive heterotrophs 

### inorganic

..... Inver/ebrate Metazoan 

## substances ,.,,.•a,•c•..,. Consumpt,o_•=,•

larvae. copepods. food
"'•

............. rotifers etc 

## CO 2, NH 3, I Uptake

, .... ••""•"•' ,' ' chan 

# uo.Po.. I ; I I•hytøp

'anktøn r•:cretio, Si04, S04, [ Regenemt•oon

] [ •,LVsis

. . ,. I Bacieria Fe, Cd, etc I'•'"- I I nl--• Upt_akel •, I

.......... 

### ' ' I I I

..... •'--•1 Fla•ellateslfood • Consumption Sedimentation I 

### 34,2 / REVIEWS OFGEOPHYSICS

Figure 15. Schematic illustrating the central role of phytoplankton as agents 

### of biogeochemical

hange in shallow coastal ecosystems.

Phytoplankton assimilate reactive inorganic substances and incorporate

these into particulate 

### (POM) and dissolved

organic matter (DOM) which

supi•ort theproduction

of pelagic and benthic heterotrophs.Arrows indicate some of the material fluxes 

### between these different compartments.

of potential

population

growth. Blooms are biological responses

to physical

variability

[Paerl, 1988], where the timescales

of bloomvariability

are set by the timescales 

### of the prominent

physical forcings [Legendre

and Demers, 1984]:semidiurnal, daily, and weeklytidal fluctuations; seasonal,

episodic, and interannual

fluctuations

in river flow; and seasonal and event-scale

fluctuations in
wind stress.



### LINKAGES

OF PHYTOPLANKTON TO THE

BIOGEOCHEMICAL SYSTEM



### The preceding

sectionpresented

the patterns and mechanisms

of phytoplankton

bloom variabilityin San 

### Fi'ancisco

Bay to illustrate

the strong

linkages between the climate

System, hydrologic

cycle, and biological

populations in the coastal zone. Here we explorethe geo

### chemical and ecological implications

of these phyto

### plankton population fluctuations.Geochemists and ecologists

use mass

balances to describe

the dynamical natureof the systems

theystudy.

Figure 15 is an example 

### showing some of the linkages

between the phytoplank

### ton and other components

of estuarine-coastal

ecosystems. This diagram

shows exchanges

between five pools of matter: reactive

inorganic

substances

(RIS; see

Table 

### 5) that are transformed

by biogeochemicai

processes; particulate

organic matter (POM), which includesphytoplankton, detritus, and organic matter sorbed onto 

### suspended

sediments;

dissolved

organic matter (DOM) including

metabolites

produced

by phytoplankton

and releasedinto the water; and populations of the pelagic 

### andbenthic

consumer

organisms

(heterotrophs)

that u•e phytoplankton-derived organic matter for their nutrition. 

### Phytoplankton

arelinked to thepool

of reactive

inorganic substances

through their uptake and assimilation of C02 and the other raw materialsrequired for 

### photosynthesis

and the biosynthesis

of newphytoplankton biomass.

Heterotrophs

are linkedto the phytoplankton either through their directconsumption of live algal biomass or their consumption/assimilation of algal-derived detritus

or DOM. Phytoplankton consumption

occurs in the water column,

by pelagic

heterotrophs,

and in 

### the sediments,

by benthic

heterotrophs

(Figure 15). The heterotrophs

are not perfectlyefficient at transforming food into new biomass, so their feeding and metabolic 

### activities

return a portion of the ingested organic matter back to the RIS or DOM pools (the process of regeneration or remineralization). Although the pools of reactive materials and their

Table 5. Frequently Used Acronyms and Abbreviations

Abbreviation Definition

DIC

DIN

DOC
DOM
DRP DSi •13C

813C POM

•15N

PCA P'C1, PC2
PC. PC:PN

PN POM
PP PUFA RIS SCE SPM
U dissolved inorganic

carbon(all species

of CO2), mM dissolved

inorganic

nitrogen (total of NO•-, NO•-, NH•-), • dissolved

organiccarbon dissolved

organicmatter dissolved

reactive phosphorus,

IdF/ dissolved

silicate, I•M
measure of the ratio •3C: •2C relative to a Standard,%o
measure of the ratio 13C: 12C in the particulate

organic matter, %0
measure of the ratio 15N: •4N relative to a standard, %o principal

Component

analysis first and second

principal components 

### particulate

carbon, pog L-• ratio of particulatecarbonto particulate 

### nitrogen, mol mol-• 

### particulate

nitrogen, •g L-• particulate

organic matter particulate

phosphorus polyunsaturated

fatty acids reactiveinorganic

substances shallowcoastal

ecosystem 

### suspended

particulate

matter, mgL- • tidal current speed amplitude,

m s -•34, 2 / REVIEWS OF GEOPHYSICS Cloern' COASTAL PHYTOPLANKTON BLOOMS ß 149

linkages are more complexthan is suggested in Figure 

### 15, this diagram illustrates how phytoplankton

primary productionactsto transform inorganicsubstances into organic matter. This newly produced organic matter exists in forms that are readily available to consumer 

### organisms.

Thus phytoplankton

primary production

is a key process

in both the cycling

of reactive

elements

and 

### in trophicdynamics

(the transfers

of matter and chemical energybetweenorganisms). These transformation processes

operate continuously,

but they are not easily observed

when the rates of RIS uptake and regeneration, or the ratesof phytoplankton production

and consumption,are balanced. These balances

are disrupted 

## during phytoplankton

blooms, when the rate ofprimary production temporarily exceeds the rate of consump

### tion. Blooms

ar• biological

events that cause

largegeochemical

changes (transformations

of RIS into POM or DOM), followed by accelerated consumption

and metabolism

of organicmatter by the heterotrophs.Therefore all the roles played by phytoplankton in element cycling and trophic dynamics are amplified during blooms. This central role of the phytoplankton can be illustrated with some geochemicaland biological re

### sponses to the spring blooms observedin south San Francisco

Bay. Phytoplankton

biomass in southSan Francisco Bay is 

### low exceptduring the springblooms, when chlorophyll 

### concentrations

exceed 10 Ixg L-• and reach peaks in the 

### range of 50-70 IxgL-• (Figure 16a).Phytoplankton primary productivity

is typically

<0.5 g C m

-2 d -1, exceptduring the springblooms when the rate of pro

### duction can exceed 1 gC m -2 d- 1 and reach peaks ofthe 

### order of 2-3 g C m

-2 d -• (Figure

16b). Primaryproductivity is a measure of the rate at which new organic matter is produced and made availableto the hetero

### trophs, and ratesof other biological processes

(in composite, the system

metabolism)

accelerate

as a response to these new inputs of food. This response is seen,for 

### example, in the production rate of pelagic bacteria, 

### which peaksduring March-April (Figure 16c). Pelagic 

### respiration

(measured

as oxygen consumption),

an index of total microbial metabolismin the oxygenated water 

### column, alsopeaks

in spring

(Figure 16d). Theseaccel

### eratedrates

of biological

activity are general

responses to phytoplankton

blooms:pelagic respiration is corre

### lated with phytoplankton biomass and primary productivity [L. M. Jensen

et al., 1990;Iriarte et al., 1991], and bacterialand primary productivity are tightlycoupled

in coastal ecosystems

where phytoplankton

are the dominant source

of labile organic

matter [Lancelot

and Billen, 1984;Billen and Fontigny, 1987; Cole et al., 1988; Lignell 

### et al., 1993]. One consequence

of the shallow

water depth of SCEs 

### is a close linkage betweenthe pelagic and benthic domains.Food deliveryto the benthos is enhanced

during blooms, eitherby the active

particle capture of suspension

### feedingmacrofauna

(e.g., bivalvemollusks, polychaete 60

'• 30

,- 20
o
lO a. Chlorophyll

Biomass 

## oO • 3


# :. • 2 

# ß



# •11

_ 0j
FMAMJ J ASOND b. Daily Primary Productivity

,,



### , ,-,*•

.... • ,**,

',.

FMAM J J A$OND

Years 1990-1994 Years 1980,1991

and 1993

c. Bacterial

Productivity 

# 400 ' '

-q,, ~ 1990

bloom



### --- 300


# • 200Iß

I •'1 ee ß

. .., ..,,•. 

### 0j i•M A M ,•j A S (•1• D 800

600 

# •400
200

0j d. Pelagic Respiration



### , , •
1993 bloom

ß

Years 1988-1991 Year 1993

Figure 16. Seasonal

distributions

of phytoplankton

biomass (as chlorophyll

a) and three indices

of system

metabolism

in southSan Francisco

Bay: (a) near-surface

chlorophyll

a concentrations

(measurements

between USGS stations

29 and 33 for the years 1990-1994; data from Wienke et al. [1991, 1992, 1993], Caffrey

et al. [1994], and Edmunds et al. [1995]), (b) primary productivity

(between

USGS stations

27 and 32 for the years 1980, 1991, and 1993;data from Coleand Cloern[1984, 1987] and B. E. Cole (personal communication,

1993)), (c) pelagic bacterial

productivity

(betweenUSGS stations 21 and 36 for the years 1988-1991; data from Hollibaugh and Wong [1996]), and (d) pelagicrespiration measured

as oxygen

consumption

during24-hour incubations of sample

water in dark bottles (USGS stations27 and 32 during 1993; data from Rudek and Cloern[1996]).



### worms, and crustaceans) or through the deposition of phytoplankton-derived POM onto the sediment surface.
Blooms can terminate as mass sedimentation events 

### triggered by resourcedepletion [Bienfang et al., 1982; 

### Smetacek,

1985; Waite et al., 1992]

or by the formation

of densealgal aggregates [Riebesell

1991a, b; Jackson

and 

### Lochmann,1992], leading to pulsedinputsof POM to the sediments [Riebesell, 1989; Lignell et al., 1993]. Benthic microbial and animal communitiesrespond quickly to these events of enhanced

food supply,

leading to rapid acceleration

of oxygenconsumption and CO2 

### andNH•- release

fromthe sediments

[Kelly andNixon, 1984; Hansen and Blackburn, 1992; Conleyand Johnstone,1995]. This direct couplingbetween benthic metabolism and phytoplanktondynamics gives rise to a general correlationbetween phytoplankton productivity 

### and the rate of oxygen consumption

in coastalmarine 

### sediments

[Nixon, 1981;Dollar et al., 1991].
Much of the POM delivered to sediments is consumed through anaerobic pathways of metabolism,in

### cluding those coupled to the bacterial respiration of

### 150 ß Cloern: COASTAL

PHYTOPLANKTON

BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS

a. Dissolved

Oxygen i i I •i i i i i i i i i 

# .-. 14 I •;ø -

-- • 10



### •" •

/ I I I I I I I J F M A M J J A S O N D b. Dissolved Inorganic Carbon, DIC

i i i i i i i i i i

- •

øi

990 bloom c. Nitrate

Years 1993-1994 Years 1990-1992 Years 1990-1994

d. Ammonium

i i i i i i i i i i i

I ß 

# "i ' ; :

. :, 

# .j.:l" ß !, t 'j ! i!1 I i

D

Years 1990-1994 e.Silicate f. Phosphate



### •0 i ß ß 

# ß ßß 

# : :.:.* i:- * , ß ß 

### ß , '- I * :*;,:** 

### I , ß • : : 

### I0 :o •* • _1 • 10 *

I I I I I I J J A S ON D Oj FM A M J J A S ON D

Years 1990-1994 Years 1990-1994 

### Figure 17. Seasonal

distributions

of some reactive inorganic substances

in south SanFrancisco

Bay: near-surface

oncentrations

of (a) dissolved

oxygen (between USGS stations 29and 33 forthe years 1993 and 

### 1994; data from Caffrey et al. [1994] and Edmunds et al. [1995]),

(b)dissolved

inorganic carbon (between USGS 

### stations 29 and 33 for the years 1990-1992;

data from M. Huebner

(personal communication,

1992)), and (c) NO•-, (d) NH•-,(e) DSi,

and (f) DRP(between

USGS stations 27and 33 for the years 1990-1994;

data from Hager [1993, 1994, also S.W. Hager,

personal communication,

1995]).



### sulfate (the process

of sulfate

reduction,

producing

S-- from SO•--) or nitrate(denitrification, which produces gaseous N20 and N 2 from NO•-). Total benthicmetab

### olism (combined

anaerobic

plus aerobic processes)

can be measured

as biogenic

heat production

in the sedi

### ments, and this index also accelerates in response

to 

### inputs of POM from

phytoplankton

blooms [Graf, 1992]. The geochemical

implications

of this benthic-pelagic coupling are that rates

andpathways

of element

cycling in shallow

coastal environments

are strongly

influenced by seasonal

phytoplankton

blooms. The rate of sulfate 

### reduction

in coastal

sediments

increases

with phyto

### plankton primary productivity

[IndrebO etal., 1979].

Sedimentation

of diatom-derived

POM leads

to rapid in
### creases in the flux of NH•- from sediments to the overlying water and a shift from net release to net 

### consumption

of NO•- in the sediments, becausenitriffU,,,XIU•tLIUII 

### k,;i::l, tlUJl [,Hllf,.;I UUli::tl of tO U 3 minD]lea iN INI-14 is 

### while denitrification

is stimulated

by oxygen

reductions 

### that follow inputs

of labile organic

substrates

[M. H. Jensen et al., 1990].

Similar linkages between N cycling and blooms have been established in south San Fran

### cisco Bay, where the production

of NH•- in sediment porewaters

increases

more than tenfold duringspring [Caffrey, 1995]. Dissolved Substances 

### Even before

Redfield's

[1958] seminal paper,ocean

### ographers

recognized

the importance

of biological

processes in changing

the chemical

composition

of seawa

### ter. A key biological

process of geochemical

change is 

### phytoplankton

primary production

(Figure 15),and the impactof this process

is evident

duringblooms,

when primary productivity

exceeds the rates of remineraliza

### tion processes.

In south San Francisco

Baythe concen

### tration ofdissolved

oxygen is usually below 8 mg L- • and it is undersaturated

with respect

to atmospheric

oxygen 

### (Figure 17a).Exceptions

occur in the spring,

when the rateof photosynthetic

oxygen production

byphytoplankton exceeds

losses from respiration

and atmospheric 

### exchange.

Duringthe spring

blooms, dissolved oxygen becomes

supersaturated

in the water and reachescon

### centrations

50-60% higherthan those at equilibrium with atmospheric

02. The CO

2 content

of seawater

Is 

### largerelative

to the photosynthetic

demand of phytoplankton, but sustained bloom events

can lead to mea

### surable decreases

of dissolved

inorganic arbon (DIC) [Nakatsuka

et al., 1992].

In south San Francisco

Bay the DIC concentration

is usually

in the range2-2.2 mM, 

### except during blooms, whenphotosynthetic

uptakede

### presses DIC to about 1.85 mM (Figure 17b).This re-34, 2 / REVIEWS OF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 151

moval of CO2 leads to pH increases in the water, and seasonal

fluctuations

of pH are common responses to 

### seasonal fluctuations in phytoplankton productivity [Hinga, 1992]. These large fluctuations in the inorganiccarbon and 

### oxygen content of the water are indications that the net 

### ecosystem

metabolism

(balance between total photosynthesis by all primary producers and total community respiration)

changes duringphytoplankton

blooms.Depletion of DIC and supersaturation of 02 indicatethat community

photosynthesis

exceeds community

respira

### tion (the ecosystem

is net autotrophic).

Conversely,

undersaturation

of 02 and excess

CO2 indicate that respi

### ration exceedsphotosynthesis (the ecosystem

is net 

### heterotrophic).

The net metabolism

is usedas an integrative descriptor

of coastal

ecosystems

as tranformers of reactive materials as they are carried from the land 

### surfaceto the coastal ocean [Smith et al., 1991]. Although most assessments of systemmetabolism have 

### been made as annual averages [Smithand Hollibaugh, 1993],phytoplankton

blooms can lead to large, episodic shifts from net system

heterotrophy

to net autotrophy [Relexans

et al., 1988]. These episodic shiftsin trophic
state must be considered in the calculation of annual 

### budgets of reactiveelements

such as C and 02. Phytoplankton

blooms alsogive rise to large changes in the concentrations of dissolved

inorganic nutrients. 

### South San FranciscoBay receives continual inputs of nitrogen, phosphorus, and silica from treated sewage [Hager and Schemel, 1996], so the concentrations of 

### dissolved

inorganicnitrogen (DIN), dissolved reactive 

### phosphorus

(DRP), and dissolved

silicate (DSi) are very high. In the landward estuary, nutrient concentrations during winter months

usually fall in the following

ranges: 

### NO•- = 40-80 gM, NH•- = 10-15 gM, DSi = 70-130 gM, and DRP = 5-10 gM. These concentrations are 

### muchhigher

than those

typically seen in the open ocean, but they are representative of nutrient concentrations observedin estuariesand bays influenced by agricultural, riverine, and municipal inputs.The variability of inorganic

nutrient concentrations in south San Francisco 

### Bay is highestin spring(Figures 17c to 17f), and this nutrient variabilityis a result of the fluctuating uptake and assimilation

of reactiveinorganic

substances

around 

### the timing of the spring blooms. As phytoplankton

biomass increases,

the winter stock of DIN can be almost 

### completely

depleted.

Phytoplankton

blooms also change the isotopic

composition

of the DIN because

algal up

### take ofthe light nitrogen isotope (14N) is faster than 15N uptake. As nitrate assimilationacceleratesduring a 

### bloom,the residual

pool of nitrate becomes enriched

in 

### lSN by this biological fractionation,

especially in estuaries where phytoplankton uptake is the dominant NO•- 

### sink [Horrigan

et al., 1990]. Seasonal

depletions

of DSi reflect the springbloom dominance by silica-requiring 

### diatoms(Figure 17e), and although DRP is not com

### pletely depleted,

minimum

concentrations

(• 1 g3//) occur during peaks of phytoplankton biomass.Nutrient 

### concentrations (DIN, DRP, DSi) progressively increase duringsummer

months, when phytoplankton

productivity decreases

and nutrient uptake rates becomesmaller 

### than the nutrient sources (Figures 17c to 17f). These seasonal-scale

connections

between phytoplankton

photosynthesis

and the distributions

of 02, CO2, and nutrients are well-characterized features of estuarine variabil

### ity that include oxygen supersaturation

[Gr•eti• et al., 1991; Ragueneau

et al., 1994] and depletionsof DIN, DRP, and DSi during blooms [Peterson et al., 1985; Froelichet al., 1985; Robertet al., 1987; Meybeck et al., 1988;Jordan

et al., 1991a, b; Conley and Malone, 1992; Wetsteyn

and Kromkamp, 1994; Pennock and Sharp, 1994]. Recent improvementsin analytical precision have given us new tools to explore phytoplankton-mediated transformations of trace substances such as dissolved 

### metals.The traditional conceptual model of metal dynamics in estuariesplaced emphasis on geochemical processes

uch asexchange

reactions

on particlesurfaces



### or complexation

reactions.

However,phytoplanktonuptake and biochemical

transformations

can also play important roles in the cycling of some trace elements 

### [Froelich et al., 1985;Sanders

and Riedel, 1993],perhaps through pathways

analogous

to those of nutrient cycling. In south San FranciscoBay the concentrations of dissolved cadmium, zinc, and nickel decreasedfrom 0.8 to 

### 0.4 nM, 20 to 3 nM, and 40 to 30 nM, respectively, 

### duringthe 1994 spring bloom (A. Van Geen and $. N. Luoma, manuscript

in preparation,

1996).Similardepletions of dissolved

zinc [Reynolds

and Hamilton-Taylor, 1992], aluminum [Moran and Moore, 1988], and cadmium [Gonzalez

et al., 1991] havebeen observed during blooms, when phytoplankton

removethesemetalsfrom solution and transform them into particulate forms. 

### High concentrations

of reduced iron Fe(II) occur in surfacewaters during blooms, when algal metabolites 

### (hydroxycarboxylic

acids) facilitate the photoreduction 

### of the low-solubility

form Fe(III) [Kuma et al., 1992]. The biological

availability

of some metals,such

as cop

### per, fluctuates

in response

to the extracellular

production of organic ligands(complexing agents)by phytoplankton[Zhouand Wangersky, 1989; Shine and Wallace, 1995]. Phytoplankton

can reduce

and methylate

arsenic, increasing

its toxicity to animals [Sanders and Riedel, 1993]; rates of these biotransformations are propor

### tional to primary productivity [Sanders,

1983]. Because of these observations, the contemporary conceptual 

### model of metal cycling includes algal uptake and biotransformation

amongthe key processes that influence 

### the chemical

form, toxicity,and incorporation of some trace metals into estuarine food webs,

with the recognition that theseaspects

of metal geochemistry

can change 

### rapidly during blooms. 

### Parallel revisionsare occurring in the conceptual models of estuarineorganic geochemistry. The largest 

### pool of organic

matter is the dissolved pool, and distributions of dissolved

organic carbon(DOC) within estu-152 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWSOF GEOPHYSICS

5000

• 4000

.o 3000

• 2000

o 1000

0 b. Ratio f Chlorophyll

a. Particulate

Carbon to Particulate Carbon
i i I el i I , i i i i i i i , {• i i i i , i I i

ß



# [,.i.", 1⁄2

J FMAMJ J ASOND

Years 1980,1990

and 1991 • 0.03



### • 0.02

..

o • O.Ol

o

Years

1980,1990 and 1991

c, Particulate

Carbon: Particulate Nitrogen



# ii

J FMAMJ J ASOND

Years1990-1992 d. 13C: 12C Ratio f POM



### = / 1990 bloom ! -

ß ß -

ß



## . : .-

ß

, , , , i i i i i i i J FMAMJ JASOND

Years 1976-1977and

1990-1992

Figure 18. Seasonaldistributions of four characteristics of the suspended

particulate matter in near-surface waters of south San Francisco

Bay:(a) concentration

of particulate

carbon and (b) ratio of chlorophyll a to particulate

carbon(between USGS stations

21 and 32 for the years 1980 and 1990- 1991; data from Wienke and Cloern [1987] and Cloernet al. [1993]), (c) ratio of particulate carbon to particulate

nitrogen (betweenUSGS stations 21 and 34 for the years 1990-1992; 

### datafrom Cloern

et al. [1993]),

and (d) •3C:•2C

ratio,expressed as g•3C (between USGSstations

27 and32 for the years 1976-1977 [Spiker and Schemel,

1979] and 1990-1992 [Cloern et al., 1993]).



### aries often follow conservative patterns of mixing between high-DOC fresh water and low-DOC seawater. These distributions are consistent with the traditional 

### viewthat estuarine

DOC is refractory

(resistant

o rapid microbial degradation) and originates

primarily from riverine inputs of terrestrial material. However, recent observations

indicate that the estuarine DOC pool is reactive and altered by internal sinks and sources,in

### cluding the synthesis

and release of algal metabolites 

### [Peterson et al., 1994].

The mechanisms

of DOC release by phytoplankton

are not well understood, but algal cells excrete low-molecular-weight

compounds

such as amino 

### acids [Pouletet al., 1985; Fuhrman, 1990], and when blooms are terminated by nutrient limitation [l/an 

### Boekel et al., 1992] or viral infection [Suttle et al., 1990; Bratbak et al., 1993], algal cellscan rupture and release their dissolved

contents

into the water. Changes in the DOC pool duringbloomsincluderapid increases in the 

### extracellular

release of organic

carbon [Baines and Pace, 1991]; the bulk DOC concentration [e.g., Norrman

et al., 1995]; the low-molecular-weight components

[Kepkay et 

### al., 1993], including

volatile hydrocarbons

[Milne et al., 1995]; the turnover

rate of labile compounds [Kirchman 

### et al., 1991]; aliphatic hydrocarbons associated

with rapid algal cell division (e.g., heneicosahexaene[Oster

### roht et al., 1983]); and aldehydes produced

from algal fatty acids

[Jalliffier-Merlon

et al., 1991]. Coastal phytoplankton blooms also play important roles in the production and release

of chemically

active 

### trace gases

to the atmosphere.

An example

is dimethylsulfide [Stefels et al., 1995],

whichis oxidized

to sulfate

in the atmosphere

and then contributes

to the acidity of rainfall [Turner et al., 1988] and climate modulation [Charlson

et al., 1987]. Coastal phytoplanktonproduction is alsoa globally

significant

source of ozone-deplet

### ing halocarbons,

suchas methyl bromide [Lobert et al., 1995].



### Particulate

OrganicMatter As phytoplankton

transform

inorganic

materials

into particulateorganicmatter during blooms(Figure 15), theychange

the abundance

and chemical

composition

of the particles suspended in water. These changes are sometimes obscured because the total concentration of 

### suspended

particulate matter (SPM) can be high in shallowcoastal

waters [Ward and Twilley, 1986]. The SPM of estuaries

is often dominated by mineral parti

### cles, and the small organic fraction is composedof 

### complex moleculesthat are difficult to characterize chemically

[Fichez et al., 1993].The suspended POM of estuaries

originates

from many sources,

including

river

### ine inputs

derived from freshwater

or terrestrial

plants, sewage, detritus from surrounding marshes, marine plankton,or primary production by vascular

plantsand algae. During bloomsthe phytoplankton production

of POM can dominate the other sources, and the SPM 

### becomes

more biogenic

in character

(the labile, or utilizable, components

become important relative to the 

### refractory

components).

Thesechanges

in the SPM are reflected in the quantity of specific classes of organic 

### compounds

such as lipids [Kattner and Brockmann, 1990], proteins [Billen and Fontigny,

1987], and carbohydrates [Fichezet al., 1993]. One geochemicalconsequence of the algal assimilation of reactive elements, suchas C, N, P, Si, is a large shift in elementalcompo

### sition (or "repackaging") [Leboand Sharp, 1992] from dissolved

inorganicforms to particulate organic forms 

### [Ward and Twilley,

1986; Zwolsman,

1994].In south

San Francisco Bay, concentrationsof particulate carbon 

### (PC) vary over nearly2 orders of magnitude,

with maximum concentrations

of biogenic

PC during

spring when 

### phytoplankton

biomass is high (Figure 18a).A common feature of bloomsis a rapid increase in the concentra

### tions of particulate

carbonand nitrogen [Nakatsuka et ai., i992], particulate phosphorus [Sakamoto and Tanaka, 1989], and biogenic silica [Ragueneau et al., 1994]. Geochemists

use a variety of measurements to infer the origin, reactivity, and biochemical composition

of the complex mixture of organic substances in coastal
waters. These measurements can be sensitive indicators 

### of the changing

phytoplankton

component

of the POM34, 2 / REVIEWSOF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 153



### during blooms. One simple indicator of the biogenic fraction of SPM is the ratio of particulate carbon to 

### SPM. This ratio is commonly •0.05 [Zwolsman,

1994], but it can reachvaluesas high as 0.35 during periodsof 

### high primary productivity[Cauwet,1991]. A simple in

### dicator of the phytoplankton fraction of POM is the 

### ratio of chlorophyll

a to PC [Jordan

et al., 1991a;Cifuentes et al., 1988]. In south San Francisco Bay this index ranges

from 0.001 to 0.03 (Figure 18b). Although the ratio of phytoplankton chlorophyll

to carbon

varies 

### with growth conditions [Cloem et al., 1995], the maximum chlorophyll:PC ratio of 0.03 observed in springis close to the ratio expected

in a suspension

of pure algal biomass.

The minimum chlorophyll:PC ratio of 0.001 indicates that most of the POM was then associated with 

### components

other than living phytoplankton biomass. 

### Canuel et al. [1995] usedanalyses of lipid biomarkers

to confirm that phytoplankton

biomass constitutes

mostof the particulate carbon in San Francisco Bay during blooms but less than 20% of the particulate carbon during nonbloomconditions. A related index is based on the "standard" elemental 

### composition of healthy phytoplankton, C:N:P = 

### 106:16:1 [Redfield,

1958]. If phytoplankton

composition followsthis Redfield ratio, then pure algal suspensions 

### should have molar ratiosof particulate carbon to partic

### ulate nitrogen (PC:PN) of 6.6 and ratios of PC to particulatephosphorus (PC:PP) of about 106. Departures from these ratios indicatethat the POM might be 

### composed

of organicmatter other than phytoplankton. In southSan Francisco Bay the PC:PN ratio is typically 

### greater than 8-9 except

during spring, when it canfall to 

### values below 7 (Figure 18c).In many other estuaries

the PC:PN ratio lies in the range 6-8 during algal blooms 

### but is >10 when the POM is dominatedby nonphyto

### plankton

components

[Ward and Twilley,

1986; Jordan et al., 1991a].

Similar fluctuations

in the PC:PP ratio occur 

### in coastal

waters, with highest

ratios (230) during nonbloom periods and lowest ratios (96) during blooms [Sakamoto

and Tanaka, 1989]. 

### Differentsources

of estuarine

organic matter (anthropogenic, terrestrial,and marine) have differentcompositions of stable isotopes

of elements

suchas C and N. These differences

have been the basis

for using isotope ratios of the POM to infer the relative importance of 

### these different sources. The approachis based on the 

### assumption

that isotopic

composition

of estuarine

POM is controlled by mixing between end-membersources. However, we now recognizethat biogeochemicalpro

### cesses, including

primary production,

alter the isotopic 

### composition

of POM. In south San Francisco Bay the 

### ratio of •3C to •2C in the POM (expressed

as •3C, the deviation of the measured 13C:12Cratio from that in a 

### carbonate

standard[Fry and Wainright, 1991]) usually falls in the range - 27 to - 23 %o (Figure 18d). However, this ratio changes

during spring blooms,when phyto

### plankton constitute the bulk of the POM and

the•3C POM increases

to -18 to -17%o (indicatingenrich

### ment in •3C). Comparable

(orlarger)

shifts inthe carbon isotopic composition

of the POM have been observed in 

### other estuaries

[Fogel et al., 1992]. Fast growing coastal 

### diatoms become particularly

enriched in •3C (with •3C up to -13%o [Fry and Wainright, 1991]), and during diatom blooms the •3C POM can increasefrom -21 to 

### -16%o in less than 1 week [Nakatsuka et al., 1992]. Although there is uncertainty about the biochemical mechanisms behind the variable discrimination of C isotopes by photosynthesis [Fry and Wainright, 1991; 

### Fogel et al., 1992], it is clear now that phytoplankton primaryproduction

can alter the isotopic

composition

of particulate carbon. Similarly, phytoplankton primary 

### production

alters the N isotopic

composition

of POM, 

### with rapidshifts

of •5N from +9 to + 1%o during blooms as algae preferentially

assimilate

•4NO• and produce POM thatisenriched

in •4N [Nakatsuka

etal., 1992]. Interpretation of the variability of C and N isotopes in estuaries

requires consideration of these biogeochemical

transformations

that become pronounced 

### duringblooms

[Pennock

et al., 1996]. Another emerging

technique

for characterizing

POM is based on analyses

for biomarkers,organic molecules 

### that can be traced to specific groups of organisms 

### [Mayzaud

et al., 1989].The lipid components of POM, particularly

sterols and fatty acids,

can give clues

about the relative importance of algal, bacterial, or vascular plant sources

of POM because

eachgroup of organisms synthesizes

a characteristic

set of lipid molecules

[Scribe et al., 1991]. For example,14- and 16-carbon fatty acids

are the most commonfatty acidssynthesized by algae, and these moleculesare used as indicators of phyto

### plankton activity[Hama, 1991]. In southSan Francisco Bay the lipid composition of the POM changes

during the spring bloom, with large increases in the relative 

### abundance

of 14:0, 16:0,and 16:1co7c fatty acids

[Canuel et al., 1995]. These same changes have been followed closely during the exponential growth phase of other 

### coastaldiatom blooms [Kattner and Brockmann,1990]. The specificmolecular composition of lipids can give information about the community compositionof the 

### phytoplankton

because differentclasses

of algaesynthe

### size different signaturemolecules[Fraser et al., 1989; Mayzaud et al., 1989]. In south San Francisco Bay the abundanceof 24-methylenecholesterol increases

mark

### edly during

the spring

bloom [Canuel

et al., 1995;

Canuel and Cloem, 1996], and this sterol is a major component 

### of marine diatoms

of the genus

Thalassiosira

(common members

of the spring

bloom community

in this estuary;


### seeTable 4).



### Responses

of the Heterotroph

Populations The complex

suite of geochemical

changes caused by algal blooms is an important mechanism of habitat change for consumer

organisms.

Some of thesechanges

are beneficial because most of the DOM and POM 

### produced

duringblooms

can be usedas a food resource154 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS

a. Bacterial

Biomass 1õ0

............

125

lOO ßß

_ _ ß
ß ß ß e•e -

ß ße e 

# ,• ø."1•.• ø ø o [ -

I I I I I I 

### J F I• A M • J • • •) N D b. Tintinnopsis sp. c. Acartia c,lausi na,uplii

i I ! i i i I i i ! i i i i i i i I i I



# t" ß 100 ;ßß


## •" • L. q ,' ß

ß - lO •, :."•;
ß ßi I



## ... . :- 

# ß ! f oo

ß

Years 1988-1991 Years 1978-1981 Years 1978-1981

d. Spionid Polychaete Larvae

i i I I i I i I i i i

_ -16



### • -18

- •. 

# •' .20

.22

-24 e. l•C: 12C

Ratio of Clam Tissues

i i i I i i i i i i !
ß 1990 ß bloom ./

ß f. Lipid Biomarkers in Clams

I I I I I I I I I I I

ß 

# ß/1990 bloom

ß .tt ,o ß

i i i i i i i i i i i J FMAMJJA$0ND

Years 1978-1981 Years 1990-1991 Years 1990-1991

Figure 19. Seasonal

changes in the abundance

or biochemical

composition

of heterotrophs

in southSan Francisco

Bay:(a) pelagic

bacterial biomass (between

USGS stations

21 and32 for theyears

1988-1991;

data from Hollibaugh

and Wong[1996]); abundances of (b) the tintinnid ciliate protozoan Tintinnopsis

p., (c) nauplii of the copepod

Acartia clausi,

and (d) larvaeof spionid polychaete

worms (from near-surface

pump samples at USGS stations

30 and32 for theyears

1978-1981;

data fromHutchinson

[1981, 1982]); and(e) ratio 

### of •3C: •2C, expressed as •3C, and (f) concentration

of thebiomarker

fatty acid 20:5o•3 in tissues of the clam Potarnocorbula

arnurensis

(between

USGS stations

28 and33 for theyears

1990-1991;

datafrom Cloern

et al. [19931).



### by bacteria, protozoans, and invertebrates.

There are two different pathways through which phytoplanktonderived organic matter canbe assimilated and converted 

### into new biomass

(production)

of heterotrophs

(Figure 15). The microbial

food chainis based

on the assimilation of DOM by bacterioplankton; it directly supports 

### the production of protozoan communities [e.g., Van 

### Boekel et al., 1992].

The metazoan

(multicellular

animal) food chain is based

on the consumption

of phytoplankton and organisms

of the microbialfood chain. Both pathways

are important,and investigations of the past 

### decade haveshown

that much(up to 60%) of the phytoplankton

primaryproduction

passes through the bacterial trophic level [Fuhrman, 1990] or is consumed 

### directly by protozoans [McManus and EderingtonCantrell,1992].

•1-•1_

_ 1•'__1

..... 11 _J I 1, 1 1 

### z nc nnAagc

is nowwen estaonsnea between the production of algal metabolites

and the rapid utilizationof these as substrates

to support bacterial productionin 

### coastal waters [Larsson

and Hagstr6rn,

1982; Lancelot and Billen, 1984]. As the rate of bacterial production increases

in response

to the enhanced

primary productivity of blooms,we would then expect corresponding increases in the abundance or biomass of the bacterio

### plankton. This population

response

is well documented 

### in mesocosm

(large enclosure)

experiments

[Painting et al., 1989;

Riemann

et al., 1990;

Norrman

et al., 1995]and in somecoastal

waters [Billenand Fontigny, 1987; Van 

### Boekel et al., 1992]and sediments [Yap, 1991].

However, strong correlationsbetween bacterial abundanceand 

### phytoplankton

primary productivity

are not always

observedin nature because bacterioplankton

populations



### are influenced

by losses

to microzooplankton

(protozo

### an) grazers

or bacterial

viruses [Bratbak et al., 1990]. Bacteriallosses

to the microzooplankton can equalthe rate of bacterial production [Coffin and Sharp, 1987]. This means that the rate of energy flow through the 

### microbial

food chain can increase in proportion

to primary productivity,

evenwhen the total biomass of bacteria changes

little. This mayexplain

whythe biomass

of bacteriopiankton

in south San FranciscoBay •s most 

### variable during spring months (Figure 19a), because rapid increases

in bacterialbiomass

are often followed by increased

abundance

of bacterial consumers [Van 

### Boekelet al., 1992]. The degree of couplingbetween bacterial and primary productivityis temperature-de

### pendent [Coffin

and Sharp,1987;Pomeroy et al., 1991], and it can be damped

by the input of terrestrial sources34, 2 / REVIEWS OF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 155



### of DOM that can also support bacterial production 

### [Ducklow

and Kirchman, 1983;Kirchman et al., 1989]. Other populations

of the pelagic

foodweb respond

to the productionof high-qualityorganic matter during blooms, because the heterotrophs

are often food-limited 

### [Durbin et al., 1983]. In southSan Francisco Bay, some 

### species of tintinnid ciliates

(protozoans

that build pro

### tectiveshells)

are present

only in spring

(Figure 19b). Sudden largepopulation

outbreaks

of these protozoans

are common in coastal waters, and these events are 

### closely linkedto seasonal

changes in phytoplankton

primary productivity.

Tintinnid ciliates

produce cysts when food availability

is low; the cysts

sink to the sediments and remain dormant until food availability increases. The development

of cysts into active

cellsis triggered

by 

### dissolved

organic substances

produced by the phyto

### plankton [Kamiyama,

1994], and this adaptive response allows the tintinnidsto exploit conditions of high food 

### availability

during blooms. Some species

of copepods

also have dormant stages 

### that are producedand hatch in response to changing 

### foodavailability.

Thisexplains

whynauplii

(larvalstages) of the copepod

Acartia clausi

are most abundant

in south 

### San Francisco

Bay during spring

(Figure 19c). Nauplii develop from resting

eggs in the sediments

(a function

of temperature

[Sullivan

and McManus, 1986]) and from the eggs produced

by the existing

adult stock.

For estuarine-coastal

copepods

such asCalanus

pacificus,

Acartia 

### tonsa, and Acartia hudsonica

the rate of eggproduction is highlyinfluenced

by the abundance

and composition of the phytoplankton

[Durbin et al., 1983; Runge, 1985; Beckman and Peterson, 1986; Sullivan and McManus, 

### 1986]. These copepods have a common response of negligible

egg production at chlorophyll a concentra

### tions of 1-2 •g L-• [Durbin

et al., 1983] and maximal egg production

rates when chlorophyll a concentration

ex

### ceeds about 10•g L-•. These

zooplankton

species store only smallfood reserves, so the population

growth rate of copepods

is sensitive

to fluctuations

in phytoplankton 

### biomass in the range of 1-10 •g L-• chlorophyll

a. This couplingbetween zooplankton productionand phytoplanktonblooms

may propagate

to higher levelsof the food web because

strong coherence

has been observed 

### between larval fish abundanceand spring plankton blooms in somecoastal

waters [Townsend,

1984]. Benthic and pelagic

heterotrophs

share the same

food

resourcein shallow coastal waters, so population responses of the benthicanimals are alsocoupled

to phytoplankton

dynamics.

Biologists

have long recognized

a close timing between the onset of reproduction of 

### benthic invertebrates

and phytoplankton

blooms [Starr et al., 1990].In southSan Francisco Bay the pelagic

larval stagesof some polychaeteworms are most abundant 

### during the spring (Figure 19d), and reproduction of other species

such asmussels,

urchins [Starr et al., 1990], 

### barnacles

[Starr et al., 1991], and oysters [Ruiz et al., 1992]is coupled

to the timingof phytoplankton blooms. 

### This synchrony provides the Obvious advantage ofensuring an abundant food supply

for larvaeas

theydevelop

in variable environments.

The mechanism

of thissynchrony is the induction of spawning by metabolitesproduced 

### and released

into the water by the phytoplankton [Starr et al., 1990]. A secondresponse

of benthic invertebrates is their seasonal growthcycle.

The cosmopolitan

estuarine

clam 

### Macomabalthica

has monthly fluctuations

of growth

rate in San FranciscoBay that are coherent with monthly 

### fluctuations

in phytoplankton

biomass:

the growth period coincides

with the seasonal

phytoplankton

blooms, and the growth rate changes from year to year in re

### sponse to the magnitude

of the annual phytoplankton 

### bloom [Thompson

and Nichols,

1988]. Comparable

studies with other species in other estuaries,

such as the 

### mussel Mytilus edulis [Smaal and van Stralen,

1990],the clam Yoldia notabilis[Nakaoka, 1992], and the oyster Ostrea edulis [Ruiz et al., 1992],

show that the growth

rate 

### of benthic suspension feeders is often near zero (or negative)

exceptduring episodes of rapid growth supported by the enhanced food availability

during phyto

### plankton

blooms. Interannual

fluctuations

in the population growth of benthic invertebratesare caused by year-to-year

fluctuations

in the abundance

of the phyto

### plankton

food resource

during the growing

season[Beu

### kemaand Cadde,

1991; Powell et al., 1995]. The biochemical

composition

of the benthic inverte

### brateschanges

as animals

grow and accumulate

storage products,

suchas lipids and carbohydrates, during peri

### odsof high phytoplankton biomass [Wenne and Styczynska-Jurewicz,

1985; Ruiz et al., 1992]. These changes in the biochemical

composition

of consumer

organisms

can 

### be linked directlyto fluctuations in phytoplankton

biomass with the same biomarker analyses usedto charac

### terize POM. The approach is based on observations

that 

### the biochemical

composition

of animals,including

the 

### 13C' 12C ratio oftheir tissues, reflects the composition

of their food resources

[DeNiro andEpstein,

1978]. In south San Francisco

Bay the carbon isotopic composition

of the clam Potamocorbula amurensis

has a seasonal

cycle 

### very similar to theseasonal

fluctuations

in g•3C POM. Carbon in the tissues of P. amurensis

has an isotopic 

### signature indicative of nondiatom

food sources (g•3C of -25 to -22%0) during winter and early spring (Figure 

### 19e). However, theg•3C of P. amurensis

increasesrapidly during springand reaches an annual maximum of 

### -17%o in April,

similar to theg•3C

of the POMwhen phytoplankton

biomass constitutes

most of the POM. This coherence

between the seasonal

fluctuations

of •3C
enrichment in both the food source and P. amurensis 

### shows that the growth

of this filter feederis supported by the assimilation

of phytoplankton

producedduring the 

### spring bloom. Fry and Wainright [1991] also interpreted 

### seasonal enrichments

of zooplankton

•3C as evidence that •3C-rich diatom carbon is transferred to the zoo

### planktontrophic level. Molecular biomarkers

provideconfirmatory

evidence 

### that algal biomass

is directlyincorporated into the pro-156 ß Cloern: COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS



### duction of organisms

at higher

trophiclevels.

Fatty acids

are useful biomarkers becausesome polyunsaturated 

### fatty acids

(PUFA) are essential

dietary factors for animalsthat can only be synthesized by algae.

An example is the 20-carbon fatty acid 20:5o03, one of the major 

### PUFAs produced by diatoms [Fraser et al., 1989]. In south San FranciscoBay the concentration of this fatty acid in the tissues of the clam Potamocorbula amurensis increased

by a factor of 10-30 within weeks after the 

### springdiatom bloom in 1990 (Figure 19f). Mesocosm experimentshave also been used to demonstratethe 

### enhanced transfer of dietary fatty acids from phytoplankton to zooplankton and then to larval fish during phytoplankton

blooms[Fraser

et al., 1989].



### The Importance

of AlgalSpecies

Composition
We conclude this section with a reminder that not all 

### phytoplankton

species are equal. The rapid production of dimethylsulfide

in coastalwaters is associated with 

### blooms of only somephytoplankton species (Emiliania huxleyi [Wolfe et al., 1994];

Gyrodinium

aureolum

[Turner 

### et al., 1988];

Phaeocystis

sp.[Stefels

et al., 1995]).

The flux of this climatically

activetrace gas

to the atmosphere

is therefore a function of the phytoplanktoncommunity 

### composition

as well as biomass

and productivity.

Only

somespecies

of cyanobact•ria

fix atmospheric

nitrogen 

### [Carpenter

et al., 1992],onlythe diatoms and silicoflagel

### lates influence

the cycling

of silica[Tr•guer

et al., 1995], and the methylated forms of arsenic produced during 

### blooms are species-dependent [Froelich et al., 1985]. 

### Nondiatoms

appear to fractionate

inorganic

carbon [Fry and Wainright, 1991] and nitrogen [Montoyaand Mc

### Carthy,1995] isotopes

less than diatoms.

The fate of phytoplankton

(e.g., grazing

versus sedimentation)

depends on the sizeand sinking rate of the cells

produced during blooms [Fahnenstiel et al., 1995]. Therefore the rates and pathways

through which blooms

act as agents of geochemicalchange are highly dependent on the species composition

of the bloom communities. 

### This same comment appliesto the linkage between algal blooms and other trophic levels, becausephytoplankton communities include a diverse array of cell 

### sizes, morphologies, and biochemical compositions. Within this diversity

of forms is a broad range of suit

### ability asfood resources for consumer

organisms.

Copepodscan select

among food items,and estuarine-coastal 

### species appear to have a preference

for dinoflagellates and microzooplankton over diatoms [Kleppel et al., 1991]. The production of viable eggsby the copepod Temorastylifera

is 4-6 times faster on a diet of Proro

### cenrrwn tninitnurn

(a dinolqagellate)

compared

with the diatom Thalassiosira

rotula [Ianora and Poulet, 1993]. This may be partly a response to the higher nutritional 

### quality of the dinofiagellate

species, although

the diatom 

### T. rotula produces

a powerful inhibitor of cell division that can block

the development

of copepod

eggs [Poulet et al., 1994]. Other species, such asthe prymnesiophyte Phaeocystis

pouchetii,can suppress feeding [Bautista

et al., 1992]

and egg production

[Van Rijswijk

et al., 1989]

of copepods.

Among the dinoflagellates, somespecies

are 

### poor food resources

for copepods

[Huntley et al., 1986], 

### andothers

(e.g., Dinophysis

acuminata)

synthesize

toxins that repel copepod

grazers [Carlsson

et al., 1995].

Therefore species

composition

of the phytoplankton

community ultimately

affects zooplankton

production

by changing the feeding and reproduction rate of copepods 

### [Pouletet al., 1994]. This appearsto be true for the benthic fauna as well [Beukema and Cad•e, 1991]. Although phytoplankton primary production is a 

### prominent

source of organic

matter to support

production at higher trophic levels,exceptional bloomsdominated by one or several species can cause

major ecolog

### ical disturbance,

sometimes

leading to large economic losses. Blooms of the red tide flagellate Olisthodiscus 

### luteus disrupt plankton food webs by inhibiting the growthof microzooplankton [Verity and Stoecker,

1982]. Dense, persistent

bloomsof species

suchas the chryso

### phyte Aureococcus

anorexefferens

[Cosper et al., 1987; Tracey, 1988] or the red tide dinoflagellate Ptychodiscus brevis [Summerson

and Peterson,

1990] can cause

reproductive failure and mortalityof shellfish such as mussels and bay scallops.

Toxin-producing

species can cause mortality at higher levelsof the food web: the prymnesiophyteChrysochromulina polylepsis

produces

a toxin that can cause

mass mortalities

of fish [Estep

and MacIntyre, 1989], the newly discovered "phantom" dinoflagellate Pfiesteria

piscicida causes

fish kills in the Pamlico 

### and Neuse estuaries

[Burkholder

et al., 1992], and diatomsof the genus

Pseudonitzschia

produce domoic acid, which is toxic to vertebrates and has caused mortalities 

### of pelicans

and cormorants

[Walz e! al., 1994]. Because of these strongspecies-specific attributes

of the phytoplankton, the linkagesbetween algal bloom dynamics and the biogeochemical system are best established throughprograms

that includemeasures

of phytoplankton community composition to identify the occurrence 

### of species

that play particular roles in the cyclingof elements

and production

of heterotrophs.

SOME LESSONS

AND QUESTIONS TO GUIDE
FUTURE RESEARCH



### My primary objective in this review was to present phytoplankton ecology as an example of multidisciplinaryscience.

The problemof coastal bloom dynamics requires consideration

of the linkages

between the geo

### logic,hydrod•amic, climatic, hydrologic,

geochemical, and biological

components

of the Earth system.

Results from sustained

investigation

of San Francisco

Bay illus

### trate some general lessons about these linkages.

They alsohelp to identifythe large gaps in our understanding of these linkages,

and I conclude

with three questions that will persist

as central elements

of coastal

ecosystem 

### research

into the next century.34, 2 / REVIEWS OF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 157

Some lessons 1. Phytoplankton blooms are key agents of geochemical variability in coastal ecosystems. A biogeo

### chemical

functionof phytoplankton primary production is the transformation of reactive inorganic substances into organic matter. During blooms these transformations are rapid and give rise to measurable changes in oxygen concentration;

CO2 and p H; dissolved nutrients such as nitrate, phosphate, and silicate;speciation and form of reactive trace metals such as cadmium, zinc, and arsenic; production

of climatically

active trace gases

such



### as dimethylsulfide;

and isotopic fractionation of elements such as C and N. 2. The rapid production of fresh organic matter 

### during bloomstriggers a complex

suite of responses

at other trophic

levels. Theseresponses

include stimulation 

### of bacterial productivity, growth of microzooplankton, and reproduction

and growth

of consumer

animals(zooplankton,mollusks,

worms, and crustaceans). 3. Phytoplankton

bloomscan be understood in the context of a simple

population

budget that expresses

rate 

### of population

change as the sum of local (in situ) processes plus transport processes. Both sets of processes 

### respond to fluctuations

in physical

forcings that originate 

### in the ocean,

atmosphere,

andwatefshed.

As an example, vertical mixing is a key determinant of phytoplank

### ton population

growth rate; mixing

is influenced

by tidal 

### (oceanic)current stresses at the bottom, wind (atmospheric) stresses on the water surface,

and riverine(watershed)inputs

of freshwater. 4. Phytoplankton

biomass varies at all spatial and temporal scales

at which we make measurements, and blooms do not necessarily develop uniformly within an estuarine basin. Temporal and spatial variability are 

### coupled; small-scale

patchiness

is ephemeral, but the mesoscale

patterns of variability can persist for daysor 

### weeks. Mesoscale

patchiness

is shaped

by the basin-scale water circulation

and mixing,and it can be altered rapidly by events that disrupt the mean circulation. The 

### timescales

of phytoplankton

biomass variability are determined by the timescales of the physicalsources of 

### biomass change, such as the semidiurnal and neapspring tidal fluctuations,

seasonal

and interannual

fluctuations of river flow, and episodic and seasonal

fluctuations of the wind forcing. 5. In southSan Francisco Bay the timing of blooms 

### is set partly by the tides,which fluctuate and establish windowsof opportunityfor phytoplankton population growth as periods of low tidal energy and slowvertical 

### mixing.The magnitudeof the springblooms is set, at least in part, each

year by the particular hydrologic and weather conditions operating during these tidal win

### dows. Therefore the timing of blooms (from an astronomical forcing) is predictable, but the magnitudeof blooms is determined

by aperiodic

forcings and is therefore unpredictable.

This observation

could be the basis for a framework of estuarine comparison, organized around the hypothesis that strongly tidal SCEs have strongly periodicvariability,whereas weakly tidal SCEs



### are characterized

by aperiodicfluctuations around the seasonal

cycles. 6. Although SCEs have recurrent annual cycles of phytoplankton

blooms, the timing, magnitude, and species composition

of these blooms all change

from year to year. Large departuresfrom the mean annual pattern



### are caused

by exceptional

climatic or hydrologicconditions, suchas events

of extreme precipitation and river discharge

or anomalous

regional wind forcings. 7. Colonization of SCEs by exotic species can lead 

### to major (sometimes

permanent)

disturbance

at the ecosystem level. The invasionof northern San Francisco Bay by the clam Potamocorbula amurensis

has caused

a fivefold reduction in annual primary production, near 

### completedisappearance of the summerdiatom bloom, and diverse

changes in the pelagic

heterotroph

community. Coastal ecosystems are particularlysusceptible to 

### this mode of global

change, and our conceptual

models 

### of coastal

ecosystems

must include recognition

thatthe 

## ecosystems we are currently studying can be profoundly altered in the future by the introduction of exotic species that disrupt trophic interactions. 8. Shallow coastal waters are nutrient-rich, turbid, 

### characterized

by largevariabilityat shorttimescales and small spatial scales,

and highly influencedby the rapid exchanges of materials with the bottom sediments. 

### Therefore the traditional conceptual modelsof pelagic oceanography

do not work as a framework for understanding

phytoplankton

bloom dynamics

in the shallow
coastal zone.



### Question

1: What Determines

Species Composition

of Blooms?
The lessons noted above come from a search for 

### patterns,

mechanisms,

and ecosystem-level

responses

to phytoplankton blooms as revealed through measurements made at one set of scales. Emphasis

is placed on 

### chlorophyll

variability as an index of the phytoplankton populationresponse

to physical

variability.

These kinds of lessons

can be used as a first step in the process of understanding

coastalblooms as features of the Earth system that are subject

to change

aswe alter the climate system and hydrologic

cycle, aswe alter the water chemistry through inputs of contaminants and nutrients,and



### as we continue

to translocate

species. However,thisfirst step is based on a narrow perspective that does not considerthe rich details of phytoplankton population variability at the species level. Smetacek

and Pollehne [1986, p. 404] call thesedetailsa "source of irritation to modernempiricalecologists." Hopefully it is clear at this point why the details are important. The recent discov

### ery of Poulet et al. [1994] that some diatom species produce a potent chemical

inhibitor of eggdevelopment is a compelling

exampleof why we need to understand the processes

that determine speciescomposition of 

### phytoplankton

blooms. If we want to fully understand 

### population

fluctuations

of copepods,

seaurchins,

or fish,158 ß Cloern' COASTAL PHYTOPLANKTON BLOOMS 34, 2 / REVIEWS OF GEOPHYSICS

then we need to understand the forces that select for 

### thosealgal species

that play critical roles in the production of food and in the synthesis of molecules that 

### interfere with population recruitment at these higher trophiclevels.

Similarly,

geochemists

needto understand 

### population variability of those phytoplankton species that are active in the production of trace gases, the 

### isotopic fractionation

of C and N, the biochemicaltransformations

of trace metals,and the cycling of nutrients. Smetacek

and Pollehne[1986] suggest hat our inability to understand

or predict bloom dynamics at the species level is the result of a conceptual framework

that over

### emphasizes

the "physicochemical

paradigm."

Smetacek [1986] suggests

the need for an "ecosystem paradigm" based on a natural history

orientationto understand life 

### history cycles, with recognition

that phytoplankton

species distributionsreflect not only adaptations to the 

### immediate environment during the growth (bloom) phase of population

cycles, but alsolife cycle

strategies, such as production

of resting

stages, that ensure

persistence of the population throughthe nongrowth phases. Work towardan ecosystem paradigm

should be based on 

### Margalef's [1978] reminder (cited by Legendre et al. [1984, p. 629]) that "Organisms are not only carriers

of molecules,

but they are subject

to natural selection."



### Question2' How Do Toxic Contaminants Alter 

### Blooms and Their Biogeochemical Functions? The urgency

of thisquestion

comes from the certainty that coastal

ecosystems

in the developed

world are contaminated with toxic substances such as heavy metals, chlorinated hydrocarbons, and petrochemicals

and the 

### likelihood that SCEs in the developing world will become progressively

more contaminated in the future [Windom, 1992;Nixon, 1995]. It is now well established that phytoplankton

blooms can change

the concentra

### tion andgeochemical

form of some

tracemetals

[Slauenwhite and Wangersky,

1991]. However,there is muchless certainty about the impacts of toxic contaminants on 

### phytoplanktoncommunity composition, primary production, and population

growth. The limited experimen

### tal work suggests

that chroniclow level inputsof toxic elements

can alter the evolution of phytoplankton

com

### munities by eliminatingsensitive species (e.g., dinoflagellates

[Brandet al., 1986]) and selecting for more tolerantforms[Sanders and Cibik, 1988;

Kuwabara

et al., 1989]. A second aspect of this question comes from the likelihood that interactions between toxic substances 

### and phytoplankton

bloomsproduce effects that propa

### rvrat-a LIUI.

JIIII•, IK,,V•.,13. UIIK;; 111UklK;; k, kJUlkl be '•-

..... s,•,- to upper *•""•':• •

.... • r•

...... •

..... • tmougn 

### phytoplankton

uptake of trace metals(or organiccontaminants

suchas PCBs and DDT [Mailhot, 1987] and subsequent

transfer of these toxicsubstances

to animals that ingest

and assimilate

phytoplankton.

It appears

that the transfer efficiency

of metalsfrom phytoplankton to
consumers

depends

on the degree to which algae can 

### assimilate

and sequester

the different elementsinside their cell membranes [Reinfelderand Fisher, 1991]. Therefore ecosystem-level effects of toxic contaminants 

### may be set, in part, by the efficiency with which phytoplankton can act as agents of bioaccumulation

and trophic transfer. Ecosystems scientists

are beginningto 

### recognize

that toxic contaminants are human forces

of change just aspotentasglobal

warming,

habitatdestruction, and introductions of exoticspecies.

As we pursue this hypothesis,

one focus

should be directed

to under-

, 

### standing

the role of blooms as events that move toxic
substances into the food resource of animals and to 

### thosesubstances

for which phytoplankton are especially efficient at assimilation

and trophic transfer.



### Question

3: How Is Nutrient Enrichment Changing Coastal Ecosystems? This question is motivated by concern about the harmful effectsof nutrient enrichment causedby the application

of fertilizersin river basins, the discharge

of urban wastes, andthe combustion

of fossil fuels [Justid

et 

### al., 1995]. A simplistic answer to this question

is that 

### nutrientenrichment

stimulates

primaryproduction

(the process of eutrophication

[Nixon, 1995]), leading

to accumulations

of phytoplankton

biomass,

episodes of nox

### ious blooms, depletions of dissolved oxygen as the blooms decay, and mortality of fish or shellfish.Al

### though this sequence of acute responses

to nutrient enrichmenthas been observed [Justid, 1987; Rosenberg and Loo, 1988], responses to chronic nutrient enrichment in most coastal ecosystems are probably more subtle, are more difficult to detect or measure, and 

### follow a sequence

of stages

leadingtoward these acute symptoms.

There is considerable

evidence that increased nutrient concentrations in coastal waters have led to 

### biological

changein recent decades; compelling

exam

### ples come from long-term observations in the Baltic [Rosenberg

et al., 1990; Gran•li et al., 1990], German Bight [Radach

et al., 1990], Chesapeake Bay [Harding, 1994; Cooper, 1995], and southernNorth Sea [Cad•e, 1986;Cadreand Hegeman, 1991]. However,there is also considerable

uncertainty

about how nutrient enrichment 

### leads to ecosystem

changein the coastal

zone. As we 

### work to answer

this question,

our broad goal should

be

a global conceptual

modelof how coastal

eutrophication works. This conceptual

model should

recognize

the following: 

### 1. Eutrophication is an ecologicalprocess, so it shouldbe studiedfrom an ecosystem perspective

that 

### considers

all the interacting

physical,

chemical,

trophic, and life history processes of phytoplankton

population fluctuation[Hecky

and Miham, 1988].•ative applications of this perspective will also be requiredto resolve the relative importance of natural processes such as 

### climate anomalies [e.g., Vieira and Chant, 1993] and anthropogenic

nutrient enrichment

as mechanisms

that 

### triggerexceptional

blooms of harmful algal species. 2. Ecosystem

responses

to chronicnutrient enrich

### ment might occuras a sequence of successional

stages,34, 2 / REVIEWSOF GEOPHYSICS Cloern: COASTAL PHYTOPLANKTON BLOOMS ß 159



### andthe earlyresponses mightbe subtle

community

shifts 

### in the phytoplankton, benthic invertebrates

[Elmgren, 1989], attached algae[McComb

and Lukatelich,

1995], or rooted plants [Orth and Moore, 1983]. 

### 3. Changing

nutrient ratiosis an important element of coastal

eutrophication

that appears

to selectively

promote blooms

of nondiatom

species [Conley et al., 1993]

as human activities

increase the availability

of N and P 

### relative to Si [Justif

et al., 1995]. 4. A conceptual

framework is neededto explain the 

### great rangeof sensitivity to nutrient enrichment among 

### different coastal water bodies.

It is not clearat thispoint why some SCEs, such as San Francisco Bay, do not exhibit obvious

symptoms

of nutrient enrichment.The 

### strong couplings

between primaryproduction

and benthicconsumption

may be a partial explanation[Cloern, 1982; Herman and Scholten, 1990; Hily, 1991]. 

### Coastalecosystems

with a short retentiontime [Balls et 

### al., 1995] or strong

tidal mixing [Tr•guer

and Qu•guiner, 1989;Monbet, 1992] appear to be more resilientto the acute effectsof nutrient enrichmentthan weakly tidal 

### systems with slow

circulation.

Thereforethis global

conceptual model should incorporate both the trophic in

### teractions

and the physical

processes

that influence

the pathways

throughwhich nutrient enrichmentcan alter 

### phytoplankton

populations. These three research

questions

are closely

intercon

### nected,so they should be pursued

togetheras componentsof integrated

programs

to identifythe patterns of ecosystem

change in the coastal zone, the underlying mechanisms

of those changes,

and the interactions

between thesedifferent mechanisms of change.

ACKNOWLEDGMENTS. The San Francisco Bay program of the United States Geological

Survey wasconceived

by David Peterson, T. John Conomos, Fred Nichols, and David McCulloch,

who introduced

me to the complexities of estuarine ecosystems.

This program has continued for nearly 3 decades because the science

leadership

of John Bredehoeft, Roger Wolff, and Robert Hirsch included a commitment to sustained

programs

of fundamental

research as integral components of the USGS mandate as the nation's Earth science agency. My own commitmentto estuarinescience has been sustained

for 2 decades

by the boundless

energyand enthusiasm of my dear friends Brian Cole and Andrea Alpine. The interdisciplinary

nature of this review comes from USGS and academic

colleagues

who continue

to broaden

my perspectives of geochemistry,

microbiology,

benthicecology,

fluid mechanics, and approaches

for data synthesis:

Sam Luoma, Ron Oremland, Ralph Cheng, Jan Thompson, Steve Hager, Fred Nichols, Tim Hollibaugh,

Alan Jassby,

Elizabeth Canuel,Jane Caffrey,Jeff Koseff, StephenMonismith, Linda Huzzey, and Joe Rudek. Illustrations in this review

were designed

by Jeanne DiLeo and David Jones. Alan Chave, Brian Cole, Christian Grenz, Debbie Hutchinson,Alan Jassby, Steven Lohrenzen, Lisa Lucas-Vidergar,

Jon Pennock,

and Tom Torgersen

gave thoughtful

suggestions

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