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The Modification of an Estuary
Author(s): Frederic H. Nichols, James E. Cloern, Samuel N. Luoma, David H. Peterson
Source:
Science,
New Series, Vol. 231, No. 4738 (Feb. 7, 1986), pp. 567-573
Published by: American Association for the Advancement of Science
Stable URL: http://www.jstor.org/stable/1696456
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The
Modification
of
an
Estuary
FREDERIC H.
NICHOLS,
JAMES
E.
CLOERN,
SAMUEL
N.
LUOMA,
DAVID
H.
PETERSON
The San Francisco
Bay estuary
has been
rapidly
modified
by
human
activity.
Diking
and
filling
of
most of
its
wetlands
have
eliminated habitats for
fish
and
waterfowl;
the
introduction of exotic
species
has
transformed
the
composition
of its
aquatic
communities;
reduction
of
freshwater
inflow
by
more than
half has
changed
the
dynamics
of
its
plant
and animal
communities;
and
wastes
have contaminated its
sediments
and
organisms.
Contin-
ued
disposal
of
toxic
wastes,
the
probable
further reduc-
tion in
freshwater
inflow,
and the
possible
synergy
be-
tween the two
provide
the
potential
for further
alteration
of the
estuary's
water
quality
and biotic
communities.
STUARIES HAVE
LONG BEEN A FOCUS OF HUMAN
SETTLE-
ment and
activity
because
of
their wide
array
of
living
and
nonliving
resources.
They
have
also
been
susceptible
to
change:
their
tributary
rivers
have
been
dammed
and
diverted,
shorelines
modified,
fish
populations
reduced or
eliminated,
and
water
quality
altered
by
wastes
(1).
The
San Francisco
Bay
estuary
is
no
exception.
San
Francisco
Bay
is
located
at the mouth of the
Sacramento-San
Joaquin
river
system,
which carries runofffrom 40
percent
(153,000
km2)
of
California's
surface area
(Fig.
1).
Spanish
soldiers
and
missionaries,
first
arriving
in
1769,
found here a
complex
of
bays
and marshes where an estimated
10,000
to
20,000
aboriginals
lived
and harvested food
(2,
3).
The
Spanish
settlement
(now
San
Francisco)
remained an isolated
trading outpost
until
gold
was
discovered in
the Sierra Nevada
foothills
(Fig.
1)
in
1848. Within
2
years,
San Francisco's
population
grew
from
400 to
25,000,
begin-
ning
the
California
population
boom.
The
estuary
changed
as
well.
By
1900
the
surface area and
depth
of the
bay
had
decreased,
marshes were
nearly
gone,
fresh water
was
being
diverted
for
irrigation,
many
exotic
plants
and
animals
(including pest
species)
had been
introduced,
and
the effects of
sewage
were
already apparent.
With
respect
to
diversity
of
change,
San Francisco
Bay
is
today
considered the
major
estuary
in
the
United States most
modified
by
human
activity
(4).
In this
article we describe
some
of
the human activities
occurring
in the San Francisco
Bay estuary
and its
watershed since
1850 that
have resulted
in
physical,
chemical,
and
biological changes.
Early
Ecological
Changes
Fish
and
wildlife.
The
best documented
change
that
occurred
in
San
Francisco
Bay
after the
Gold Rush was a
decline in
fish
abundances
(5).
Early
immigrants exploited
the
waterfowl, fish,
and
shellfish
of the
bay
and the
Delta-the
low-lying region
of
marshes,
7
FEBRUARY
1986
islands,
and channels
surrounding
the confluence
of the
Sacramento
and
San
Joaquin
rivers
(Figs.
1 and
2).
Commercial
fisheries
in
salmon,
sturgeon,
sardines, flatfish, crabs,
and
shrimp
were
quickly
established.
However,
by
1900 catches
of
larger, longer
lived
species
at
upper trophic
levels,
such as
salmon,
sturgeon,
and the
introduced
striped
bass,
had
declined;
gradually,
these
commercial
fisheries
were halted to
protect
the
stocks
for
sports
fishing
(5).
Declining
abundance
of
the
Dungeness
crab
(Cancer
magister)
in
the
bay
forced that
fishery
to
move
offshore
in
the
1880's,
although
the
bay
remained a
nursery
ground
until
the
1960's,
when
the
nearby
offshore
fishery
collapsed
(6).
Today's
commercial
fishing
is
restricted to
herring
and
anchovies
(7, 8),
species
representative
of the
smaller,
more
rapid
reproducers
at
lower
trophic
levels that
dominate the
fisheries
of
disturbed
environ-
ments
elsewhere
(9).
The
shifts
in
San
Francisco
Bay
fisheries
presumably
have
resulted
from
a
combination of
overfishing,
elimi-
nation of
essential
habitats,
and
changes
in
water
quality
(5),
whereas the
decline of the
offshore
crab
fishery
since
1960
is
attributed
variously
to
increased
ocean
temperature, predation by
hatchery-reared
salmon,
and
pollution
(6).
The
specific
contribution
of
any
of
these factors to
the decline of
individual
species
has not
been
quantitatively
determined.
Introduced
species.
A less
obvious but
equally
important change
occurred within the
communities of
plants
and animals
representing
the
lower
levels
of the
estuarine food
web.
Upon
completion
of the
transcontinental railroad in
1869,
large quantities
(up
to 100
carloads
per year)
of
live
eastern
oysters
(Crassostrea
virginica)
were
shipped
from the
East
Coast to
California
for
maturing
on
coastal
bay
mud flats.
By
the
late
1890's the
imported oyster
was
Califor-
nia's most
valuable
fishery product
(10).
Although
the
eastern
oyster
never
became
naturalized
in
San
Francisco
Bay (transplanted
adults
failed to
produce
young),
other
East Coast
invertebrates,
unintentionally shipped
with
the
oyster,
became
fully
established
(Fig.
3).
Additional
species
that
had'bored
into
ship
hulls or were
carried in
ship
ballast
were
also
released
into
the
bay
(7).
In
total,
approximately
100 invertebrate
species
were
introduced,
including
the
only
two
mollusk
species
in
today's bay
sports
fishery
[the
eastern
soft-shelled
clam
(Mya
arenaria)
and the
Japanese
little-neck clam
(Tapes
japonica)]
and
pest
species
[such
as
the
oyster
drill
(Urosalpinx
cinerea)
and
the
shipworm
(Teredo
navalis),
the latter
causing
large-scale
destruction of
piers
and
bridges
soon
after its
introduction
(11)].
Now,
nearly
all
common
macroinvertebrates
present
on
the inner
shallows of the
bay,
and
some
planktonic
invertebrates
and
algae,
are
introduced
species
(7,
12,
13).
The
remarkable
success of the
introduced
invertebrates has
been
attributed to
(i)
the lack
of a
diverse native
fauna
because of the
estuary's
geologic
youth
and
geographic
isolation
(7)
and
(ii)
the
The
authors are research scientists with the U.S.
Geological Survey,
345
Middlefield
Road
(MS-999),
Menlo
Park,
CA
94025.
ARTICLES
567
m
opportunistic
characteristics
of
many
of the
introduced
species
that
made them well
suited to
rapidly
colonize the
bay's
underexploited
habitats
(12).
Fish
species
were
intentionally
introduced
beginning
in
the
1870's
(5).
Of the 42
fish
species
now
inhabiting
the
sloughs
of
Suisun
Bay
marshes
(Fig.
2),
for
example,
20 are
introduced
(14).
The
striped
bass
(Morone
saxatilis),
introduced
from the
East
Coast
in
1879,
yielded
annual
catches
exceeding
450 tons
between
1889
and
1915. Catches
declined
thereafter,
and
commercial
fishing
was
prohibited
in
1935.
The
striped
bass
remains the
primary
sports
fishery
in
San Francisco
Bay
(5,
7).
CenSan
F
ran
r
alley
Poject-
':
'
:
'~
oville
I
\
Auburn
. i!
\
(u.c.)
-
-
San
Francisco
iaClramento
San
Francisco
ay
Kesterson
eroir
\
(
\
'i~.:
ii
Central
!3
Project
^
^Prject
e
\
Water
Project
)
?:i~i::~iiiii[:i
i
,
uisDra4
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"
Drainage
divide
Fig.
1.
Major
features of
California's
natural and
man-made
water
systems,
including
the
drainage
basin and
major
tributaries
(fine lines)
of the
Sacramento and San
Joaquin
river
system,
major
storage
reservoirs
(black
areas),
aqueducts
(bold lines),
the
Central
Valley
(shaded
area),
the
Delta,
and the San Francisco
Bay estuary.
568
t
Physiographic
Alterations
The
character
of
the
central
California
landscape
changed
during
the late
1800's
as
a
result
of the
gold
mining,
farming,
and land
F
development
that
accompanied
the
explosive growth
of
population
centers.
Hydraulic
gold
mining
and
land
reclamation
resulted in
t
particularly
marked
physical
changes
to
San
Francisco
Bay.
Hydraulic
mining
debris.
Hydraulic
mining
(the
use of water
under
high pressure
to
expose
ore
deposits,
employed
from
1853
to
1884)
greatly
accelerated
the
recovery
of
gold
from
the
Sierra
Nevada.
In
the
process,
tens
of
millions of
cubic
meters
of
rock
and
earth
were
excavated
annually.
This
debris
choked
creeks
and
rivers,
silted
or
blocked
salmon
spawning
streams,
and
obstructed
navigation
throughout
the
drainage
basin
(15).
The
obstructed river
channels
could
not
contain
winter
and
spring
runoff,
and
periodic
massive
flooding
resulted
(15,
16).
Hydraulic
mining
was
stopped by
court
injunction
in
1884,
but
decades
of
winter
floods
and
dredging
were
required
to
flush
the
sediments
from
the
river
channels.
The
Sacramento
River
channel
did
not
return
to
its
pre-mining depths
until
the late
1920's
(11).
Although
most
damage
from
hydraulic
mining
debris
occurred
in
the
drainage
basin of
the Sacramento
and San
Joaquin
rivers,
much
of
the
mud
and
sand
reached
San Francisco
Bay. By
the end
of
the
19th
century,
1.0, 0.75,
and 0.25
m of sediment
was
deposited
in
Suisun,
San
Pablo,
and central
San Francisco
bays
(Fig.
2),
respec-
tively
(15).
Acceleration
of
the
natural
sedimentation
process
con-
tributed
to
both
a
permanent
reduction
in the
open-water
area
of
the
bay
through
shoaling
and
an
expansion
of marshland
across
some
of the
newly
formed
mudflats
(7).
The reformed
bottom
topography
reduced
the water volume
of the
bay
and altered
tidal
circulation
patterns
(15).
No
record exists of
short- or
long-term
effects of
these
changes
on the
bay's
biological
communities,
although oyster
beds
were
reported
to have been
harmed
by
heavy
siltation
during
the
mining period
(10).
Land
reclamation.
Before
1850,
1400
km2
of freshwater
marsh
surrounded
the confluence
of the
Sacramento
and
San
Joaquin
rivers,
and another
800
km2 of saltwater
marsh
fringed
the
bay's
shores
(Fig.
2)
(15).
As
population
increased,
tidal
marshes
were
diked to
create
farmland
(primarily
in the
delta),
evaporation
ponds
for
salt,
and,
later,
residential
and industrial
land.
Reclamation
of
freshwater
marshlands in the
Delta was
essentially
complete by
the
early
1920's,
but
filling
of the
bay's
saltwater
marshes continued
into
the
early
1970's
(8).
Of
the
original
2200
km2
of tidal
marsh,
only
about
125
km2 of undiked
marsh remains
today (Fig.
2)
(7).
Long-
term effects
of marshland
elimination on
estuarine
water
chemistry
and
productivity
are
possible
(17),
but,
again,
no
appropriate
records
predating
these
changes
exist.
Nonetheless,
because half
of
the
migratory
birds on
the Pacific
Flyway
winter
on
or near
San
Francisco
Bay
(18),
we
assume that the
loss of food and
habitat
provided
by
the
bay's
former marshes
has
been detrimental
to
these
bird
populations.
Water
Development
and
Altered
Freshwater
Inflow
California's
climate
consists
of
a wet winter
(November
through
April)
and
a
dry
summer
(May
through
October).
The
absence
of
summer
rainfall
necessitates
irrigation
of
Central
Valley
farmlands
with
water diverted
from
the Sacramento
or
San
Joaquin
rivers
and
their
tributaries.
Further,
because about
70
percent
of
the
state's
annual
runoff occurs north
of
Sacramento
(Fig.
1)
and
80
percent
of
water
consumption
occurs
south
of that
city
(19),
increased
manage-
ment of
the
water that flows
toward San Francisco
Bay
has
SCIENCE,
VOL.
231
accompanied
the
state's
growth
(16).
One result has been
a
greatly
reduced
freshwater
flow
into the
estuary.
The Sacramento
and
San
Joaquin
rivers
discharged
about 34 km3
of
fresh
water
into
San
Francisco
Bay
annually
before 1850
(20).
As
California's
population
grew
(Fig.
4A),
the area under
irrigation
increased
by
about
30,000
ha
per
year (Fig.
4B),
creating
demands
for both
flood
protection
and reliable water
supplies.
In
response,
state and
federal
agencies
built
dams,
reservoirs,
and canals
to
increase
storage capacity
(Fig.
4C)
and
annual
export
rates
(Fig.
4D).
These
facilities
represent
the
world's
largest
man-made
water
system (Fig.
1),
with
a
water-storage
capacity
of about
20
km3
(16).
At
present,
nearly
40
percent
of the
historic
(1850)
flow of the
Sacramento-San
Joaquin
river
system
is removed
for
local
consump-
tion
upstream
and
within the
Delta.
Another
24
percent
is
pumped
from the
Delta and
exported
in
aqueducts
for
agricultural
and
municipal
consumption
in
central
and
southern California
(Fig.
5).
Now,
the
flow into San
Francisco
Bay
is less than
40
percent
of
historic
levels.
To minimize
up-estuary
salt intrusion that
results
from lowered
freshwater
flows
(and
that
is exacerbated
by
dredged
channel
deepening
between
San
Pablo
Bay
and
the
Delta) (11),
inflow
during
summer
has been
increasingly
augmented (Fig.
6).
Nearly
86
percent
of
California's
managed
water
supply
is used
in
agriculture
(21).
If
the
state's
reservoir
capacity
increases as
project-
ed
(Fig.
4C)
and conversion
of arid
land to
new
farmland
through
irrigation
continues
to be
profitable,
demands
for water
export
will
increase
(Fig.
4D).
As a
result,
average
freshwater
inflow
to the
bay
in the
year
2000
is
projected
to
drop
to 30
percent
of the
historic
average (Fig.
5).
Ecological
consequences of
reduced
river
inflow.
Both
the
physical
process
of
diverting
water and the
changes
in flow
patterns
resulting
from water
management
have affected
biological
communities
of the
San Francisco
Bay estuary. Disruption
of the natural
flow of water
has most
noticeably
affected
migratory
fish-species
dependent
on
the rivers
for
spawning.
Construction
of Shasta
Dam
(Fig.
1)
in
1944
eliminated
half of the salmonid
spawning
habitat
in the
Sacramento
River
system
(5),
requiring
the
augmentation
of natural
stocks
with
hatchery-reared
fish.
The
operation
of water diversion
pumps
at the southern
end of the
Delta
during
summer
periods
of
low
river flow causes
water in Delta channels
to
flow
upstream.
Thus,
hundreds
of
millions
of
juvenile
salmon and
striped
bass
(31
and
25
percent
of
typical
year
classes,
respectively)
are drawn into
the
water diversion
pumps
each
year
(22).
Equal
numbers are
lost
to
numerous small
siphons
and
pumps
that collect
irrigation
water for
local
consumption
in the Delta
(23).
These
losses
have contributed
to a
decline
in the abundance
of adult
striped
bass to
less than 25
percent
of that
in
the mid-1960's
(24).
Effects
of water diversions
on the
biology
of the
bay
itself,
although
more difficult to
identify
or
quantify
because
of simulta-
neous
changes
due
to
land
reclamation,
fishing,
and waste
disposal,
can be deduced
from observations
made
during
two consecutive
years
of
naturally
low
flows
(1976
and
1977).
Normally,
fresh water
is
released
during
summer at a controlled
rate between
100
and
400
m3/sec
(Fig.
6).
Under
these
conditions,
the
downstream-flowing
river currents are
balanced,
in
Suisun
Bay,
by
the
upstream-flowing
bottom
currents
carrying
salt water
(Fig.
7).
This
convergence,
or
null
zone,
is a
point
where
suspended particles,
including
sediment
and
planktonic
diatoms,
accumulate
(7,
25,
26).
Associated with
this
phytoplankton
maximum are
high
abundances
of
pelagic
herbivores
(copepods
and
the
mysid
shrimp
Neomysis
mercedis)
that are
impor-
tant food sources for larval or
juvenile
fish
(27).
During
1977,
when
Sacramento-San
Joaquin
river
discharge
in summer
dropped
below
100 m3/sec
(Fig.
6),
phytoplankton
biomass
in
the
upper
estuary
was
reduced
to
20
percent
of normal levels
(26),
zooplankton
abundance was
significantly
reduced,
and both
Neomysis
abundance
7
FEBRUARY
1986
and
striped
bass
recruitment
fell to
their lowest recorded levels
(27,
28).
Suppression
of the
pelagic
food web
during
this natural
occurrence
of
extremely
low flow
suggests
that
(i)
production
of
some
pelagic
fishes in the
upper
estuary may depend
on a
high
biomass of
primary
producers
and
(ii)
high phytoplankton
biomass
develops
only
when freshwater
inflow
exceeds 100
m3/sec
(26).
Two
theories have
been
proposed
to
explain
the absence
of a
summer
phytoplankton
bloom
in northern
San Francisco
Bay
during
extremely
low
inflows. The first
theory
(26)
holds that the
typical
summer biomass maximum is
dependent
on
a circulation
pattern
that
positions
the null zone
adjacent
to the
productive
shallows of Suisun
Bay,
where
light
availability
is sufficient to
sustain
algal growth.
When river
discharge
falls below 100
m3/sec,
the
null
zone
moves
upstream
into
the
deeper
Sacramento
River,
where
light
availability
is
insufficient to sustain net
photosynthesis
and
phytoplankton
biomass remains low. The second
theory
(29)
holds that reduced
phytoplankton
biomass
during periods
of
persist-
ent low river flow and
high salinity
results
from increased
grazing
losses to
immigrant
benthic
suspension
feeders
that
are
normally
excluded from this
region
by
winter freshets.
Both
mechanisms,
direct
consequences
of
reduced freshwater
inflow,
probably
contributed
to
the absence of a summer bloom
during
the 1977
drought.
These
findings
illustrate the
sensitivity
of
northern San Francisco
Bay
biological
communities
to
persistent
low river
flow
and
suggest
that
further reductions
in
freshwater
inflow
(Fig.
5)
could
permanently
alter the
pelagic
food web and
fisheries
yield
there.
Other
consequences
of
reduced
inflow.
Reduced freshwater inflow
from
the
Sacramento-San
Joaquin
river
system
may
also reduce
the
estuary's
capacity
to
dilute,
transform,
or
flush contaminants
that are
discharged
into
San Francisco
Bay.
Estimated
residence time
of
water in
northern
San Francisco
Bay
ranges
from
a minimum of
1
Fig.
2. Distribution of
undiked tidal marshes around
San
Francisco
Bay
before 1850 and
at
present
(7).
ARTICLES
569
Cumulative number
Littorina
litto
of
Tapes japonica
introduced
mollusks
Tapesapoca
Musculus senhousia
Busycotypus
canaliculatus
Petricola
pholadiformis
Lyrodus
pedicellatus
Teredo navalis
Ilyanassa
obsoleta
Crepidula
plana
Crepidula
convexa
Ischadium
demissumn
Gemma
gemma
Urosalpinx
cinerea
Mya
renaria
Ovatella
nmyosotis
I
,
I
,
I
,
I
, I , I
,
1860
1900 1940
Year
of
discovery
Fig.
3. Cumulative number of
introduced mollusks
by
date of
disco)
The
period
of most
rapid
increase,
the
1890's,
coincides
with the
p
maximum
oyster
importation.
day during
peak
winter flows
to a
maximum
of
2
months
during
)rea
sustained
low
summer
flows
(30).
Winter
peaks
in river
inflow
also
carry
fresh
water into the
semienclosed
embayment
of
South
San
Francisco
Bay
(hereafter
called
South
Bay)
(Fig.
2),
which
has no
other
important
source of
freshwater
inflow. In the
process,
salinity
of
South
Bay
drops
from
about 30 to
15
per
mil
(well
below
that
of
seawater at
the
Golden
Gate).
The
resulting
horizontal water-
density
gradient
causes
the fresher surface
layer
to move
seaward and
more
saline bottom
water to move
landward
(30,
31).
This
increase
(up
to
tenfold)
of nontidal
currents
following
periods
of
high
river
discharge
accelerates the
exchange
of water
between
South
Bay
and
Central
Bay,
decreasing
water
residence time in
South
Bay
from
several
months to several
weeks
(30).
Changes
in
circulation that
accompany
freshwater intrusion into
South
Bay
apparently
affect concentrations
of
dissolved constitu-
ents,
including
trace
contaminants.
Silver and
copper
concentrations
in
benthic
organisms
near a waste
outfall in
South
Bay
decrease
after
,winter
floods,
when
salinity drops
(30).
Moreover,
less silver
1980
accumulates in the
organisms during years
of
highest
freshwater
inflow in
winter
(Fig.
8).
Although
mechanisms
are not
well
understood,
such evidence
suggests
that
(i)
concentrations of
bio-
eryd
7)f
logically
available metals
may
be linked to
the
river-driven circula-
tion of South
Bay
and
(ii)
a
significant
reduction
of
river inflow
could reduce the
effectiveness of
processes
that
facilitate
waste
assimilation in
South
Bay.
c
0
1d
:3
-
20
-
OC
U
0c~.
a.
E
5
to-
0
0
0
-0
4
x
2-
cat
0
40
0.. -
2-
co
co!
0 0
Ott
40
1.0
,
co
E
20
-
0
CL
A
0)
to
-
cr0
o -
CL (
xa
0'
B
I I
i_1 1
i , 1 i
C
I _
0
_'
D
8-
/"
-
8-
-
4-
o
0
t I I I
I I
1850
San
Francisco
Bay
33.9
1980
San
Francisco
Bay
12.7
13.1
Upstream
and
Delta
consumption
Delta
export
2000
San Francisco
Bay
<
9.7
15.2
9.0
Upstream
and
Delta
consumption
Delta
export
Freshwater flow
(km3/year)
1860
1900
1940
1980
Fig.
4
(left). (A
and
B)
California
population growth
and land under
irrigation
(50); (C)
water
storage capacity
of
reservoirs
in the Sacramento
and
San
Joaquin
river basin
exclusive
of those
smaller
than
8000 ha
(dashed
line
represents
an estimated increase
of 15.2 km3 in the
year
2005
for the
Auburn Reservoir
now under construction
and the
proposed
increased
height
of
Shasta
Dam) (51); (D)
historic and
projected
export
of
water
from
the
delta
by
the federal Central
Valley
and state water
projects
(19,
52).
The
effect of the
1976-77
drought
on
Delta
export
is
clearly
seen.
Fig.
5
(right).
Disposition
of Central
Valley
runoff
(exclusive
of
transpiration
and
other natural
losses)
before
about
1850,
in
1980,
and
projected
for the
year
2000. Water removed in
the watershed
and
within
the delta
for
local
irrigation
and domestic
consumption
is
shown as
upstream
and delta
consumption;
that withdrawn
from
the
Delta
for
export
to central and
southern
California
is shown
as Delta
export
(19,
20).
Waste
Disposal
Wastes from
municipal
and industrial outfalls and in
runoff from
urban and
agricultural
lands have
flowed into the
estuary
since the
Gold
Rush.
Nonetheless,
determining
their effects on the
bay's
aquatic
life
has
been
difficult.
Agricultural
waste.
Beginning
in
the late
1940's,
use of
fertilizers,
soil
amendments,
herbicides,
and
pesticides
in
Central
Valley
farm-
lands became
widespread
and
altered
the
composition
of river
water,
most
notably
in
the San
Joaquin
River.
The
San
Joaquin
River
Valley
is
arid,
with a
discharge per
unit area about one-third
that of
the Sacramento River
Valley.
Agricultural
waste
water
(residual
irrigation
water,
containing
salts
leached
from the
soil,
that is
returned to
the
river in
subsurface
pipe drainage
systems)
makes
up
more
than 20
percent
of the
total San
Joaquin
River flow
(32).
Maximum
annual concentrations
of
sulfate and nitrate in the
river,
normally
occurring
during
the
irrigation
season,
have
increased
nearly
threefold and
fivefold,
respectively,
since
1950
(Fig.
9).
The
increases
reflect,
in
large
part, expanding irrigation
of soils
contain-
ing
natural sources of
gypsum
(CaSO4
?
2H20)
and
the
addition of
fertilizers as
well
as
gypsum
and
other
forms
of sulfate as soil
amendments.
To
dispose
of
the
increasing
volume of
agricultural
waste water
(including
water
used
to
flush salts from salinated
soils),
an artificial
channel
connecting
the Central
Valley
with
San Francisco
Bay
near
Suisun
Bay-the
San Luis
Drain
(Fig.
1)-was
authorized
for
construction
by
Congress
in 1960
(33).
As
proposed,
the
drain
would
discharge
natural and
agriculture-related
chemicals into the
bay, including
an
estimated
17 tons of
nitrogen per
day
(34),
a
rate
equal
to that from
all
point
sources north
of
San
Francisco
(7).
A
portion
of the
San
Luis Drain that serves about
3000
ha of
farmland
(less
than 10
percent
of the
area
proposed
to be
served)
was
constructed.
In
1978 drain
water
began
to flow into a
tempo-
rary holding facility,
the
Kesterson Reservoir-a
marshy
lowland
used also as
a
wildlife
refuge
(33).
In 1982
dying vegetation
and
declining
wildlife
abundances were noted
in
the
reservoir.
A
year
later,
unusually
high
incidences
of
physical
deformities,
reproductive
SCIENCE,
VOL.
231
14
-
10
-
6
-
2
-
I
570
failure,
and
mortality
were
observed
in
aquatic
birds
using
the
bay
organisms,
when
compared
with
averages
in
organisms
from
reservoir:
greater
than 40
percent
of nests
contained
at least one
other
estuaries,
are
not
especially high,
reflecting
the
many
locations
dead
embryo
and
20
percent
contained
at
least one
embiyo
with
in
the
bay
unaffected
by
local
discharges
and the
rapid
dilution
of
obvious
external
abnormalities
(35).
Subsequent
chemical
analyses
those
wastes
discharged
by
the
major
cities
near
the
mouth of
the
of
animal and
plant
tissues taken
from
reservoir
populations
showed
estuary.
On
the
other
hand,
localized
patches
of
metal
contamina-
mean selenium concentrations
ranging
from 22 to
175
p.g/g (dry
tion,
with
concentrations
as
high
as
those
observed
anywhere
in
the
weight),
or
up
to 130 times those found at a
nearby
control
site
world,
occur
near
past
and
present
waste
disposal
sites
(8,
41).
(35).
Samples
of waste water
from the San Luis Drain and
the
Kesterson
Reservoir
also contained
very
high
selenium levels
(140
to
1400
ng/liter)
(36).
Selenium,
occurring
naturally
in alluvial soils
of the
arid western
-
r
i
i
San
Joaquin
Valley,
is leached
by
irrigation
water and
concentrated,
2000-
with
other
salts,
in
the
topsoil
by
evaporation.
The
selenium is
I
mobilized when
the soils are
drained
to
remove
all
accumulated
salts1
and
is
carried into
the
reservoir.
There,
it causes the
reproductive
;io
1000
failures
and
deformities
in
resident
birds
(33, 35)
WE
The
discovery
of
bird
mortalities
and
deformities in the
Kesterson
,
,
-
Reservoir
has
resulted in
recent
state and
federal decisions
to halt
1940
'
1950 1960
1970
1980
work on the Sal
Luis Dra
in
projct
andtoclose
the reservoir
im
work on
the
Sani
uis
Drain
project and
to close
the
reseroir
p
Fig.
6.
Mean monthly
freshwater
flow
in
the
Sacramento River at
Sacramen-
1986.
In
the
meantime,
agricultural
waste
water
from
west
San
to
since
1938. Note
theprogressive
increase
in
the summer flow rate
and
the
Joaquin
Valley
farmlands
not
served
by
the
existing
San Luis
Drain
major
anomaly
associated
with
the
1976-77
drought
[from
T.
J.
Conomos
continues
to flow
into the
San
Joaquin
River.
High
concentrations
e
a,d. fig
^e
9A,
in
(30)]
of
selenium
have
recently
been
found in
ducks
in
South
Bay
(37).
Whether the
seleniumn
originates
in the San
Joaquin
River or
from
local
sources in the
bay
area remains to be
determined.
Domestic and
industrial waste.
Significant
changes
in
the
composi-Sa
Pa
B
Su
Ba
tion
of
bay
waters have
occurred because of
the
urbanization and
industrialization
of
the
bay's
shore. At
present,
industrial
and
domestic
wastes,
as
well
as urban
runoff,
enter the
bay
at more
than
i
-
sacrame
to
100 locations. The
known
point
sources of
waste include more
than
/
i
Rier
30
municipal
and 40
industrial waste
treatment
facilities and an
/>
Freshwater
Nulizone
additional 100 smaller industrial
dischargers.
Together,
these facili-
/
E
Brackish
water
ties
discharged
0.7
km3
of waste
water in
1978,
or
nearly
4
percent
of the
average
annual
freshwater inflow to
the
bay.
The
annual
waste
hcific
Ocel
input
contains,
among
numerous
constituents,
300 metric
tons of
Fig.
7.
Nontidal
estuarine circulation and
the null zone in norther
San
trace
metals
(38).
The ratio of
wastewater to
freshwater
inflow is
Francisco
Bay. Suspended particles
(stippled
area)
accumulate
in
the null
expected
to
double
by
the
year
2000
(8).
Untreated
urban runoff
zone where the
upstream
flow of
salt water at the
bottom meets the
also
enters the
bay
through
more
than
50 small local streams
because
downstrcam flow of
fresh
water
and net movement
is
minimal.
This
zone
most
runoff and
sewage systems
are
separated.
Additional
contami-
vs
upad downtheestuary
in
responsetoriverdischarge.
nation
results from
daily
accidental
spills
of
industrial
chemicals
and
oil;
small
oil
spills
alone
account for
200
to
300
spills annually
(8).
Adverse
ecological
effects of
waste
discharge
have
been
suspected
26
-
since
the
early
1900's,
when industrial
wastes were
implicated
in the
A
gradual
failure
of the
oyster
industry
(2, 5).
A
detailed
analysis
of
3
I
3000-
pollution
effects was not
undertaken until
1951,
when a
study
220-
-
showed that
(i)
few
or no
benthic
invertebrates
were
present
f
2000-
.
inmlediately
adjacent
to
several
waste
outfalls,
(ii)
the
number of
3
180
-
7
/
.
1000-
*
wastes
(39).
0
14 K
79 /80
species nearby
was
depressed
below
area
averages,
and
(iii)
industri-
a
779
al
wastes
suppressed
the
number
of
species
more
than did
domestic
I
7
80
so/.
X
r
'
76
wastes
(39).
>
140
-
Improvements
in
sewage
treatment
facilities
beginning
in
the
X
-
30
1960's reduced some of
the adverse
effects ofwastes.
Concentrations
<10
7
200
-?
of
oxygen-consuming organic
matter
and
ammonia in
South
Bay
E
200-
*
have
been
reduced to
the
point
that
the summer
depletion
of
81/82
-
-
dissolved
oxygen,
typical
two
to three decades
ago,
no
longer
occurs
60
*
(8).
Summer
concentrations of
enteric
bacteria
have declined in
-
82/831
z
__
South
Bay
from
800
per
100 ml of
water in
1964
to 4
per
100
ml
in
I
20
_ i
1950 1960
1970
1980
1977
(38, 40).
Collection of
shellfish for
hunan
consumption,
c
o
i
15002000
~~bann~~Fred
for
decades,
has
recently
been
pershitated
drg
sr
inflow in
December
(m3/sec)
banned
for
decades,
has
recently
been
pernufitted during
suraner
on
selected mud
flats well
removed
from outfalls or
other
sources
of
Fig.
8
(left).
Maximm
concentrations
of silver
found
in
the
clam
Macoma
hazardous
waste.
balthica
living
in
a
metal-enriched
mud flat in South
San Francisco
Bay
as a
fun,ction ofifeshwater
inflow
in
December
[from
S. N.
Luoma et
al.,
figure
Despite greatly
upgraded
sewage
treatment,
bay
sedimlents
and
^
offrshwa
ntmflv
December
from S. N. Luoma
et
.
figre
.
,
'i
(
30)].
Fig.
9
(right).
Maximumn
annual
concentrations
of
dissolved
organisms
are
contaminated to various
degrees
with trace
organic
sulfate
(A)
and
nitrate
(B)
in
the
San
Joaquin
River
near
its mouth
(53).
and
inorganic
materials.
Average
concentrations of trace
metals in Lines are
least-squares
regressions.
7
FEBRUARY
1986
ARTICLES
571
Phosphate
E
0-3
1
6-10
>
20
(pmole/liter)E
3
-
6
10
-
20
Fig.
10. Dissolved
phosphate
distributions in South San
Francisco
Bay
at
four times of
year
(54).
Distributions of toxic
organic
materials
[polychlorinated
biphenyls
(PCB's)
and
petroleum hydrocarbons]
are also
patchy,
with concen-
trations in some
organisms
reaching
levels
comparable
to those
in
highly
contaminated estuaries.
For
example,
PCB concentrations
observed
in the
blubber
of
bay
harbor
seals
(Phoca
vitulina
richardii)
in
1977
(42)
equaled
those concentrations
thought
to
cause
repro-
ductive failure in Baltic Sea
gray
seals
(43).
Concentrations
of
petroleum
hydrocarbons
in mussels collected
in central
San
Francis-
co
Bay
nearly
equal
those
in
Los
Angeles
and
San
Diego
harbors,
which are
subjected
to
frequent petroleum
contamination
(8).
Although
no studies have
clearly
linked trace
contaminants to the
permanent
elimination of
any
species population,
elevated
toler-
ances to
trace
metals
have been observed
in the clam
Macoma
balthica and
the
copepodAcartia
clausi from contaminated
locations
in
the
bay
(44).
These
results
imply
an
importance
of
adaptive
flexibility
to the survival of some
populations.
Studies
near a South
Bay sewage
outfall
also indicate
that
physiological
stress caused
by
trace metal contamination
occurs
even
in
highly adaptable
bivalves
when metal
availability
is
highest
(30).
High
incidences
of skin
lesions, tumors,
and increased
parasitism
in
the
bay's
striped
bass
may
be
consequences
of
exposure
to
synthetic
organic compounds;
moreover,
the concentrations
of
petroleum-derived
hydrocarbons
found in
striped
bass are
as
high
as those that
adversely
affect
the
hatching
success of
eggs
in the
laboratory
(45).
Physiological
indicators
of
stress
in mussels
transplanted
along
a transect
in
South
Bay
increased coincident
with
a
gradient
of
increasing
trace metal
concentrations
in
water,
sediment,
and
organisms
(46).
Nutrient
enrichment
of
the
bay.
Stimulation
of
plant
growth
through
nutrient
enrichment,
with
subsequent
declines
in
oxygen
content
of the water as the
plant
material
decomposes,
is
another
potentially
important
result of waste
discharge.
Sewage-derived
nutrient
inputs
in
northern
San
Francisco
Bay
are not
easily
distinguished
from
the
large
riverine
inputs.
Waste-derived nutri-
572
ents
are
more
apparent
in South
Bay,
where storm
drains
and waste
treatment
plants
are
the
principal
sources of
freshwater
inflow
(7).
During
the
winter-spring
period
of
high
river
runoff,
levels
of
nutrients
[for
example, phosphate (Fig.
10A);
nitrate
concentra-
tions
vary
similarly]
in
South
Bay
are low because of dilution
with
low-salinity
water
in
central San
Francisco
Bay
(7).
During
the
rest
of
the
year,
when
runoff
is low
and dilution and
mixing
with
central
bay
water
diminish,
nutrient levels increase
(Fig.
10,
B to
D)
to
a
summer-autumn
maximum
that
is
often the
highest
level found in
San Francisco
Bay.
Although
nutrient
concentrations
are
periodically high,
the
bay
does
not exhibit
symptoms
of
eutrophication-nuisance
phyto-
plankton
blooms
and associated
depletion
of
oxygen [although
localized,
episodic
blooms of
drift
macroalgae
occur in
some
years
(30)].
Benthic
filter
feeders
in
South
Bay
are
apparently
sufficiently
abundant to reduce the
standing
crop
of
phytoplankton
well below
expected
levels
(47).
Thus the benthos
may
act as
a
natural
biological
control on
eutrophication-a
process
employed
in
aquaculture
(48)-by
converting
sewage-derived
nutrients
to animal biomass.
It
follows, therefore,
that
events that
selectively
disturb
the
benthos
(for
example, exposure
to
contaminants)
could
promote
the devel-
opment
of noxious blooms.
In
Perspective
Few of the
changes
we have described
are
unique
to San Francisco
Bay. Many
estuaries,
such as those of the
Delaware, Hudson,
Potomac,
Rhine,
Susquehanna (Chesapeake Bay),
and,
until
recent-
ly,
Thames
rivers,
have seasonal or
permanent oxygen depletion
resulting
from
high organic
waste
loading
or nutrient
enrichment
as
well as
contamination
by
toxic
wastes
(49).
Other estuaries in arid
regions
around the world
are
also
affected
by
river
water
impound-
ment
and diversion
(4).
Measured in terms
of
concerns
that attract
public
attention or
interfere with
commerce,
the
problems
of
San
Francisco
Bay
appear
less severe than those of other
large
urbanized
estuaries.
This
appearance
results,
in
part,
because
(i)
much
of
the urban and
industrial
development
in
the
bay
area
has
occurred near
the
estuary
mouth,
where dilution and
dispersal
of wastes are
greatest,
rather
than on the
tributary
rivers;
(ii)
corrective actions taken since
the
1960's
have
eliminated
oxygen depletion
and
greatly
reduced
patho-
genic
bacteria;
and
(iii)
many
of the
major
changes
(such
as
the
disappearance
of
wetlands,
introduction
of
exotic
species,
and loss of
many
commercial and
sports
fisheries)
occurred decades
ago
and
have been
forgotten.
Despite
the
difficulties
in
measuring
ongoing,
human-induced
changes,
it
is
clear that San Francisco
Bay
is sensitive
to
diverse
human
activities.
Toxic
wastes derived
from
agricultural
and indus-
trial activities
have
been
locally
detrimental
to
birds
and bottom-
dwelling
invertebrates.
Suggested
links between the
striped
bass
decline and contamination with
synthetic organic
compounds
or
between
physiological
stress
in
bivalves
and trace
metals,
although
largely
circumstantial,
indicate
that chronic
regional
effects
of
contamination
exist
in San Francisco
Bay.
There
is
also
evidence
that
decreased freshwater
inflow
can
contribute to altered balances
among plant
and animal communities that
may
lead,
for
example,
to
decreases
in
some fish stocks.
In
addition,
there is an
apparent
link
between
river flow
and
the
capacity
of
the
estuary
to assimilate
wastes.
The future
well-being
of this
estuary
(like
that of
other
urbanized
estuaries)
lies
in
achieving
an
increased
understanding
of
its
interact-
ing
physical,
chemical,
and
biological processes
and
how
these
processes
are affected
by
specific
human activities.
The effects
of
SCIENCE,
VOL.
231
increased
toxic
waste
inputs
and
further
reductions in
freshwater
inflow,
and
particularly
the
possible
synergy
between the
two,
are
among
the
critical
topics
requiring
increased research and
manage-
ment efforts.
Meanwhile,
economically important
issues,
such as
changes
in the treatment
and
disposal
of industrial and
agricultural
wastes,
deepening
of
channels to accommodate
larger
ships,
and
increasing
river
water
diversion,
are
being
considered
without
sufficient
quantitative
understanding
of the effects of these
actions
on
the
estuary.
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less
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Hills,
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Flows
for
I980
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2000
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o5
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51
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160
(1983),
with flow for
an
average
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being computed
as San Francisco
Bay
inflow
=
delta inflow
-
(delta
export
+
delta
consumption),
and
upstream
and
delta
consumption
=
1850
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-
(San
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delta
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2I0
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J.
E.
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W. R.
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Toth,
A. M.
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224
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L. B. Kost and
A. W.
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(1975).
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Sacramento-San
Joaquin
Estuary
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Department
of
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Game,
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U.S. Fish
and
Wildlife
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U.S. Bureau
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Sacramen-
to,
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F. H.
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J. E.
Cloern
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H.
Nichols,
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D. S.
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I;
2;
4
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E.
Marshall,
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I44
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R. L.
Brown,
Water Res.
9,
529
(I975),
tables
I
and 2. The calculations assume a
mean
annual drain flow of about
io
m3/sec
and a
nitrogen
concentration
of 20
mg/liter.
35.
H. M.
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D.
J.
Hoffman,
M. K.
Saiki,
T. W.
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Total
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T. E.
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C.
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Wildl.
Manage.,
in
press.
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Toxics
in
the
Bay:
An Assessment
of
the
Discharge
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to San Francisco
Bay
by
Municipal
and Industrial Point Sources
(Citizens
for a Better
Environment,
San
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1983).
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F.
P.
Filice,
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E. A.
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P. N.
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R. E.
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67-5
(1970);
R. C.
Cooper,
K. M.
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D.
C.
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D.
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Sanitary
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(1981).
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E. A.
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S. N.
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C.
E.
Johansson,
D.
J.
Cain,
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18,
755
(I984).
42.
R. W.
Risebrough,
J.
W.
Chapman,
R. K.
Okazaki,
T. T.
Schmidt,
Toxicants
in
San Francisco
Bay
and
Estuary
(Association
of
Bay
Area
Governments,
Berkeley,
CA,
1978).
43.
E.
Helle,
M.
Olsson,
S.
Jensen,
Ambio
5,
188
(1976).
44.
S.
N.
Luoma,J.
Fish. Res.
Board Can.
34,436
(1977);
,
D.
J.
Cain,
K.
Ho,
A.
Hutchinson,
Mar.
Environ.
Res.
o0,
209
(1983).
45.
M.
Jung,
J.
A.
Whipple,
M.
Moser,
Summary Report of
the
Cooperative
Striped
Bass
Study (Institute
of
Aquatic
Resources,
Santa
Cruz,
CA,
1984);
P. E.
Benville, Jr.,
J.
A.
Whipple,
M. E.
Eldridge,
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71,
132
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M.
Martin,
G.
Ichikawa, J. Goetzl,
M. de los
Reyes,
M. D.
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J.
E.
Cloern,
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R.
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H.
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C. B. Officer et
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U.S.
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5I.
G.
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(1980),
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18;
table
Io
in
(I9),
excluding
Auburn Reservoir.
52.
Unpublished
report.
53.
U.S.
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Water Resources data for
California.
54.
D. D.
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personal
communication.
55.
We thank
many colleagues
for
helpful
discussions and access to
unpublished
manuscripts,
J.
W.
Hedgpeth
for
sharing
much
knowledge
about San Francisco
Bay,
and
J.
D.
Bredehoeft,
H. E.
Clifton,
and
D.
S.
McCulloch
for
comments
on
the
manuscript.
7
FEBRUARY
1986
ARTICLES
573