The Ecology of the Soft-Bottom Benthos of San Francisco ... · Biologica1 Report 85(7.19) September...

Cover pho10gr;tphs tipper Icfl. Assorled spectes of oyster shell accunlu!~afed on a South Eay mudfiat Upper right ^The eastern ribbed mussel. Geukens~a demissa, an introduced species in Soulh Say. Lower. Soft-battorn haksitai of Sari Fraricisco Bay Photograph couflesy of D R Hopkins.

Biologica1 Report 85(7.19) September 1988

THE ECOLOGY OF THE SOFT-BOTTOM BENTHOS OF SAN FRANCISCO BAY: A COMMUNITY PROFILE

Frederic H. Nichols Water Resources Divi sion U.S. Geological Survey

345 Middlef i el d Road MS-496 Menlo Park, CA 94025

and

Mario M . Pamatmat Paul F. Romberg Tiburon Center fo r Environmental Studies

San Francisco State University P. 0. Box 855

Ti buron, CA 94920

Project Off i cer

Michael Brody National Wet1 ands Research Center

U.S, Fish and Wildlife Service 1010 Gause Boulevard

Sl idel 1, L A 70458

Prepared f o r

U.S. Department of the Inter ior Fish and Wildlife Service

Research and Development National Wetlands Research Center

Washington, DC 20240

Library of Congress Cataloging-in-Publieatio~~ Data

Nichols, Frederic H. (Frederic Hone), 1937- The ecology of the soft-bottom benthos of

San Francisco Bay

(Biological report ; 85(7.19) (Sept. 1988)) Bibliography: p.

Supt. of Docs. no.: 149.89/2:85 (7.19) 1. Marine ecology--California--San Francisco Bay.

2. Benthos--California--San Francisco Bay. I. Pamatmat, Mario Macalalag. [ I . Brody, Michael. Ill. National Wetlands Research Center (U.S.) IV. Title. V. Series: Biological report (Washington, D.C.) ; 85-7.19.

Th i s report may be c i t e d as:

N i cho l s , F.H., and M.M. P a m a t n a t . 1988 . The ecology o f t h e s o f t - b o t t o m benthos o f San Franc isco Bay: a community p r o f i l e . U.S. F i s h W i l d l . Serv . B i o l . Rep. 8 5 ( 7 . 1 9 ) . 73 FP.

PREFACE

This profile, part of a series of prof i l es concerning coastal habitats of the United States, i s a detailed examina- tion of the soft-bottom benthos of San Francisco Bay. A U.S. Fish and Wildlife Service and Cal i forni a Department of Fi sh and Game report (1979) entitled "Protec- tion and Restoration of San Francisco Bay Fish and Wild1 i f e Habitat" provides clear recognition of the importance of inter- t idal and subtidal soft-bottom habitats and the i r associated organisms to the bay's birds and fishes and t o the overall functioning of the estuary. The purpose of th is profile i s t o provide a description of the structure and functioning of the benthic community in San Francisco Bay (exclusive of i t s t idal marshes, which are discussed by M . Josselyn [1983] i n another profile). The habitats covered in th is vol ume i ncl ude a1 1 nonvegetated soft- bottom intertidal and subtidal areas of the bay between the Golden Gate and the mouths of the Sacramento and San Joaquin Rivers t o the northeast, and to the southern extremity of the bay.

The profile provides a reference to the sc ient i f ic information concerning the animals and plants of the bay's benthic communities, their importance to the bay ecosystem, and the i r value as a resource measured in human terms. Because there have been few process-oriented studies of the benthos of San Francisco Bay (e.g., f i e ld and 1 aboratory rate-measurement experiments) , the material presented herein i s 1 argely descriptive. None- theless, we have described the processes that interconnect the various physical, chemical, and biological components of the benthic environment, and the important couplings between th i s environment and the water column above, with reference to research results from other estuaries where necessary. We consider the role of

the benthic community as a food source for f ish, aquatic birds, and humans; as a consumer or degrader of organic materi a1 s including wastes; as a recycler of minerals and nutrients; and as an accumul ator of pol 1 utants.

The information in the profile should be useful to environmental managers, resource planners, estuarine ecologists, marine science students, and interested laypersons who wish to learn about those components of estuarine systems that are 1 argely unseen and unappreciated, but that play an extremely important role in the functioning of an estuary, particularly as a source of food for exploited fish stocks as we11 as for humans, and possibly as a biological control on eutrophication. The format, s tyle, and level of presentation are intended t o make th is report adaptable to a diversity of needs, from preparation of environmental assessment repor ts t o supplementary reading material in marine science courses.

The p r o f i l e includes chapters covering geographic background (Chapter I ) , b i o t i c communities--descriptive review (Chapter 2 ) , macrofaunal community dynamics (Chapter 31, cycling of matter in the benthos (Chapter 41 , an thropogeni c influences (Chapter 51, she1 1 f isheries (Chapter 61, and managing benthic resources (Chapter 7 ) .

The fo l lowing developments have occurred since t h i s profile was written in 1986-87: (i) There hair been further resolution of the status of Macoma ba'fthica as an introduced versus natjve species ( S e c t i o ~ 2 . 3 ) . Whi?e i t i s clear t h a t th is species was originally native to San Francisco Bay7 recent electrophoresis studies suggest that the present $an

Francisco Bay popul at1 ons a re more c f osel y re la ted t o western North At1 an t i c popula- t ions than t o populations from Oregon and northern Europe. Thus, the San Francisco Bay and U.S. eas t coast Macoma populations ( the former probably having been recent ly introduced from the l a t t e r ) probably represent a separa te s i bl ing species (B.W. Meehan, Virginia I n s t i t u t e of Marine Science; J.T. Carlton, University of Oregon; and R . Wenne, Polish Academy of Sciences; pers. cornm.) ( i i ) San Francisco Bay has been invaded by ye t another exot ic inver tebra te , t h i s time by an Asian bivalve, Potamocorbul a amurensi s , t h a t was possibly transported in to the bay

a s l a r v a e in ship b a l l a s t water. Increas- ing from one reported spe imen in l a t e 5 1986 t o as many as 25,00O/m in summer of 1987, t h i s clam has become the dominant macroinver tebra te throughout the northern p o r t i o n s of the bay and i s found in South Bay sloughs as well. A shallow-dwelling Suspension feeder, t h i s clam may become a major consumer of the es tuary 's phyto- PI an kton . ( i i i) Regarding pollution e f f e c t s assessment (Section 5.3) and e s t u a r y management (Chapter 7), in April 1988, San Francisco Bay was o f f i c i a l l y d e s i g n a t e d one of t h e t a r g e t e s tua r i es of t h e U.S. Environmental Protection Agency's "Na t iona l Estuary Program. "

CONTENTS

PREFACE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . FIGURES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . TABLES . .............................................................. CONVERSION FACTORS ................................................... ACKNOWLEDGMENTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

CHAPTER 1 . GEOGRAPHIC BACKGROUND . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 GEOLOGIC ORIGINS . ............................................ 1 . 2 PRESENT-DAY PHYSIOGRAPHY ..................................... 1 . 3 CLIMATE AND WATER PROPERTIES ................................. 1 . 4 TIDES ........................................................ 1 . 5 SEDIMENT TEXTURE AND DYNAMICS . . . . ............................

CHAPTER 2 - B IOTIC COMMUNITIES.. DESCRIPTIVE REVIEW ................... 2 . 1 BACTERIA, MICROFAUNA, AND MEIOFAUNA . . . . . . . . . . . . . . . . . . . . . . . . . . 2 . 2 BENTHIC MACROINVERTEBRATES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 . 2 . 1 G e n e r a l i z e d D i s t r i b u t i o n s and Re1 a t i v e Abundances o f Common S p e c i e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . 2 . 2 . 2 B a y w i d e P a t t e r n s o f M a c r o i n v e r t e b r a t e B iomass 2 . 3 INTRODUCED INVERTEBRATES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 . 4 PREDATORS ON THE BENTHOS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 . 5 INVERTEBRATE FEEDING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 . 5 . 1 F e e d i n g Modes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 . 5 . 2 B e n t h i c F o o d Web . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

CHAPTER 3 . MACROFAUNAL COMMUNITY DYNAMICS . . . . . . . . . . . . . . . . . . . . . . . . . . 3 . 1 SEASONAL PATTERNS I N THE BENTHIC COMMUNITY . . . . . . . . . . . . . . . . . . .

3 . 1 . 1 Abundance Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 . 1 . 2 S e a s o n a l G r o w t h . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 . 1 . 3 S e a s o n a l P r e d a t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

3 . 2 APERIODIC PATTERNS OF ABUNDANCE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 . 2 . 1 E f f e c t s o f E n v i r o n m e n t a l P e r t u r b a t i o n s . . . . . . . . . . . . . . . . . 3 .2 .2 I m p o r t a n c e o f S p e c i e s I n t e r a c t i o n s . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 . 3 LONG-TERM TRENDS

CHAPTER 4 . CYCLING OF MATTER I N THE BENTHOS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 . 1 INTRODUCTION

4 .2 SOURCES OF ORGANIC MATTER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 . 2 . 1 V a s c u l a r P l a n t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 . 2 . 2 B e n t h i c M a c r o a l g a e . . ................................... 4.2.3 P h y t o p l a n k t o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 . 2 . 4 B e n t h i c B a c t e r i a and M i c r o a l g a e . . . . . . . . . . . . . . . . . . . . . . . . 4 .2 .5 M i c r o a l g a l P r o d u c t i o n .................................. 4 .2 .6 O t h e r S o u r c e s o f O r g a n i c Matter t c t h e S e n t h o s . . . . . . . . .

4 .3 RATE OF ORGANIC MATTER SUPPLY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 .4 FATE OF ORGANIC MATTER I N SEDIMENTS . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5 SEDIMENT OXYGEN CONSUMPTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

4.6 BENTHIC NUTRIENT REGENERA7 10N I N SAN FRANCISCO BAY . . . . . . . . . . . 35 4.7 MODELS OF ORGANIC MATTER BUDGETS OF ESTUARINE BENTHOS . . . . . . . . . 35

CHAPTER 5 . ANTHROPOGENIC INFLUENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 EARLY PHYSICAL AND BIOLOGICAL CHANGES . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . 5.2 INTERFERENCE WITH THE NATURAL HYDROLOGIC CYCLE 5.3 EFFECTS OF POLLUTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

5.3.1 Methods o f Eva lua t i on . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.2 Sewage-Induced N u t r i e n t Enrichment

5.3.3 E f f e c t o f P o l l u t i o n on Benth ic Community Metabal ism . . . . 5.4 SEDIMENT BUDGET AND DREDGING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

5.4.1 Est imates o f Sediment Budget . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4.2 E f f e c t s o f Dredging on t he Benthos

5.4.3 E f f e c t s o f Contaminated Dredged Sediments on Organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

5.4.4 E f f e c t o f Channel Dredging on Sa l twa te r I n t r u s i o n . . . . . .

CHAPTER 6 . SHELLFISHERIES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 EARLY HISTORY OF BAY SHELLFISHERIES . . . . . . . . . . . . . . . . . . . . . . . . . .

6.1.1 Oysters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1.2 Clams and Mussels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1.3 Crabs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1.4 Shrimp . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

6.2 PRESENT STATUS OF BAY SHELLFISHERIES . . . . . . . . . . . . . . . . . . . . . . . . . 6 . 2 . 1 Spor t Harves t ing o f Mo l lusks . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 .2 .2 Commercial Harves t ing o f Crustaceans . . . . . . . . . . . . . . . . . . .

6 .3 THE FUTURE OF BAY MOLLUSK FISHERIES . . . . . . . . . . . . . . . . . . . . . . . . . . 6 .3 .1 Oysters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3.2 Clams . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3.3 The Threat of P o l l u t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

CHAPTER 7 . MANAGING BENTHIC RESOURCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55 7.1 INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 5 7 . 2 PUBLIC PERCEPTIONS, USES, AND CONCERNS . . . . . . . . . . . . . . . . . . . . . . . 5 5 7.3 SCXCNTXFIC BASIS FOR MANAGEMENT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56

7.3.1 Present Knowledge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 6 7 .3 .2 Hindrances t o Increased Understanding . . . . . . . . . . . . . . . . . . 57

7.4 NtEDS FOR RESEARCH AND MANAGEMFNT . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58

REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 1

FIGURES

Number Paqe

....... 1 Dra inage b a s i n o f t h e Sacramento-San Joaquin R i ve r s 1 2 The P a c i f i c coas t o f t h e Un i t ed S ta tes .................... 1 3 Past shore1 i nes o f San Franc isco Bay . . . . . . . . . . . . . . . . . . . . . . 3 4 The San Franc isco Bay Es tuary ............................. 4 5 Bathymetry o f San Franc isco Bay . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 6 H o r i z o n t a l and v e r t i c a l d i s t r i b u t i o n o f sa l i n i t y .......... 6 7 H o r i z o n t a l and v e r t i c a l d i s t r i b u t i o n o f t u r b i d i t y . . . . . . . . . 7 8 A m u d f l a t o f South Bay .................................... 7 9 Genera l i zed d i s t r i b u t i o n o f su r f ace sediment t e x t u r e ...... 8

10 Percentage o f mud c o l l e c t e d i n t h e sha l lows o f f o u r ................................................ embayments 9

11 Accurnul a ted o y s t e r she1 1 s o f assor ted spec ies on a m u d f l a t .............................................. 13

12 Cumulat ive number o f i n t r oduced mo l lusks by da te o f d i s cove ry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

13 D i s t r i b u t i o n and abundance o f an i n t r oduced amphipod . . . . . . 1 5 14 The i n t r oduced eas te rn r i b b e d mussel a t t h e edge o f a

. .......................................... cordgrass marsh 16 15 Erod ing edge o f a San F ranc i sco Bay marsh,

. ............ p e r f o r a t e d by burrows of an i n t r oduced i sopod 16 16 An unusua l l y h i gh concen t ra t i on of t h e i n t r oduced

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . mudsnai 1 16 17 P ropo r t i ons o f i n t r oduced and n a t i v e spec ies r e l a t i v e

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . t o t o t a l biomass o f mo l lusks 16 18 The sa l t - panne h a b i t a t o f t h e n a t i v e ho rnsna i l . . . . . . . . . . . . 1 7 19 Feeding depress ions, p robab ly made by

t h e b a t r a y . . . . .......................................... 1 7 20 Clam feed ing t r aces , w i t h t h e mudsnai l

f o r s ca l e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 21 Abundance o f t h e macrofauna c o l l e c t e d i n c o r e samples

on an i n t e r t i d a l mud f l a t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22 22 Abundance o f t h r e e numer i ca l l y dominant mudf l a t

spec ies over a 10-year p e r i o d . ............................ 22 23 Average l e n g t h of i n d i v i d u a l s i n two age c lasses o f

a n a t i v e c lam . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 24 S a l i n i t y , mean number o f macrofauna spec ies, and mean

number o f i n d i v i d u a l s a t a sha l low s i t e i n Suisun Bay . . . . . 25 25 Average abundance o f n u m e r i c a l l y abundant spec ies a t two

s i t e s i n Suisun Bay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25 26 Freshwater f l o w j n t o San Franc isco Bay and abundance

. . . . . . . . . . . . . . . . . . . . o f two spec ies a t a mudf la t s tudy s i t e 26 27 Contours o f nea r - su r f ace phy top lank ton biomass

. . . . . . . . (measured as c h l o r o p h y l l ) i n San Francicco Bay 30 28 Average c h l o r o p h y l l concen t ra t i on i n su r f ace sediments

. . . . . . . . . . . . . . . . . . . . . . . . a t s i t e s l e s s than 5 m water depth 3 i 29 D a i l y maximum ebb t i d a l v e l o c i t y , average month ly wind

. . . . . . v e l o c i t y , and average month ly i r r a d i a n c e a t lovt t i d e 3 1

vii

Number Paqe

30 Re1 ations among aerobic processes and anaerobic .................................... processes in sediments 33

........ 31 Distribution of Indian shell middens a t about 1900 38 32 Relation between the winter maximum concentration

of s i l ve r in clams and the r a t e of freshwater inflow ...... 41 33 Distribution and abundance of a polychaete species

................. from r e su l t s of many quant i ta t ive surveys 4 3 34 Concentrations of s i l v e r in a clam from a

South Bay study s i t e ...................................... 44 35 Relation between the depth of the r iver-es tuary

channel and the extent of 1 andward intrusion of s a l t ...... 49 36 Location of former oyster beds ............................ 51 37 Breakwater provides habi ta t and refuge fo r two

introduced clam species ................................... 53 38 A typical bay view ........................................ 56

viii

TABLES

Number &

1 Wet weight and percent of total sample wet weight for different faunal groups in each region of the bay . . . . . . . . . 1 2

2 Percent composition of food items occurring in the gizzard of shorebirds collected at Palo Alto . . . . . . . . . . . . . . 18

3 Reported feeding modes of common soft-bottom macroinvertebrates found in San Francisco Bay ............. 1 9

4 Rates of benthic oxygen uptake and carbon dioxide production in South Bay ................................... 34

CONVERSION TABLE

Metric to U.S. Customary

Rnolf iply millimeters (mm) centimeters (cm) meters (m) meters (m) kilometers (krn) kilometers (km)

To Obfain inches inches feet fathoms statute miles nautical miles

square meters (m2) square kilometers (km2) hectares (ha)

square feet square miles acres

liters (I) cubic meters (rn3) cubic meters (m3)

gallons cubic feet acre-feet

milligrams (mg) grams (g) kilograms (kg) metric tons (t) metric tons (t)

ounces ounces pounds pounds short tons

kilocalories (kcal) Celsius degrees (OC)

British thermal units Fahrenheit degrees

U.S. Customary to Metric

inches inches feet (ft) fathoms statute m~les ( m ~ ) nautical miles (nmi)

millime:ers centimeters meters meters kilometers kilometers

square feet (ft2) square miles (mi2) acres

square meters square kilometers hectares

gallons (gal) cubic feet jft3) acre-feet

liters cubic meters cubic meters

ounces (02) ounces (oz) pounds (Ibf pounds (Ib) short ions (ton)

milligrams grams kilograms metric tons metric tons

Briitsit 'ihurmai m t s $3;~; Fahrenhejt degrees (OF)

ki!oca!cries Celsius degrees

ACKNOWLEDGMENTS

Many people have helped us dur ing t h e prepara t ion of t h i s p r o f i l e . J . K . Thompson (U.S. Geological Survey) , a long-t ime co l league o f t h e f i r s t au tho r , has provided immeasureabl e a s s i s t a n c e both in g a t h e r i n g and i n t e r p r e t i n g t h e San Francisco Bay benthos d a t a t h a t comprise a l a r g e p a r t o f t h e mater ia l presented here in . R . N . Tas to , T.O. Moore ( C a l i f o r n i a Department of Fish & Game) and D.W. P r i c e (Cal i f o r n i a Department of Health Se rv i ce s ) provided much useful mater ia l and comments concerning bay she1 1 f i s h . S. Wyllie Echeverria (Cal i f o r n i a S t a t e Un ive r s i t y , San Franc isco) brought us up t o d a t e concerning ongoing s t u d i e s of e e l g r a s s beds. J .E. Cloern, S.N. Luoma, and D.S. McCul1 och (U . S. Geol og i c a l Su rvey ) provided comments on va r ious ind iv idua l chap t e r s . D . R . Hopkins (U.S. Geological S u r v e y ) r ev i ewed t h e p r o f i l e f o r t y p o g r a p h i c a l e r r o r s and p r o v i d e d

photographs ( a s i nd i ca t ed in cap t i ons ; a l l o ther photographs taken by t h e f i r s t author) inc lud ing t h a t on t h e cover . J . D i Leo-Stevens ( U . S. Geological Survey) d r a f t ed a11 of t h e i l l u s t r a t i o n s . J .T. Carl ton (Univers i ty of Oregon), E . B . Lyke (Ca l i fo rn i a S t a t e Univers i ty , Hayward),

M . N . J o s s e l y n ( C a l i f o r n i a S t a t e Univers i ty , San Francisco) , M.S. Race (Univers i ty of C a l i f o r n i a , Berkeley) , J.K. Thompson (U. S. Geological Survey) , and an anonymous reviewer provided d e t a i l e d and immensely he lpfu l reviews of t h e e n t i r e manusc r ip t . F i n a l l y , M.S. Brody, as Pro jec t O f f i c e r (U.S. Fish and Wi ld l i f e S e r v i c e ) , was extremely p a t i e n t and helpful as we prepared t h e p r o f i l e . To a l l of t he se people, we o f f e r our thanks.

Funding f o r t h i s r e p o r t was provided by t h e U.S. Environmental P ro t ec t i on Agency, Region 9 o f f i c e .

CHAPTER 1. GEOGRAPHlC BACKGROUND

1.1 GEOLOGIC ORIGINS

San Francisco Bay i s l oca t ed a t t h e mouth of t he Sacramento-San Joaqui n River system which c a r r i e s runoff from t r i b u t a r y r i v e r s and streams d ra in ing about 40% (153,000 km2) of Cal i f o r n i a ' s s u r f a c e a r ea (Figure 1 ) . The s u r f a c e a r ea of t h e e s - tuary (1,240 k m 2 ) makes i t t h e l a r g e s t coas ta l bay on t h e P a c i f i c coas t of t h e United S t a t e s (F igure 2 ) and one of North America's l a r g e s t e s t u a r i e s .

The topography of t he San Francisco Bay region r e s u l t s from recent deformation

Figure 3 . California and the drainage basin of the Figure 2. T h t Pacific coast of the United States, Sacramento-San Joaquin Rivers; Central Valtey illustrating the geographic separation of large west indicated by stippling (adapted from Conornos et al. coast estuariesandthe relatively larger sire of the San 1985). Francisco Bay Estuary and its drainage system.

of an o l d e r , t e c t o n i c a l l y a c t i v e cont inen- t a l margin. The coas t a l region of western North America i s composed of l a r g e blocks of d i s c r e t e geologic t e r r a n e s t h a t were c a r r i e d hundreds of ki l ometers northward and accre ted t o t h e North American con- t i n e n t (Howell 1985). Between 3 and 5 mil 1 ion yea r s ago, s t r e s s e s exe r t ed ac ros s t he con t inen t a l margin up1 i f t e d t h e presen t Coast Ranges. The long process of mountain bu i l d ing l e f t only a narrow con- t i n e n t a l s h e l f and l i t t l e coas t a l p l a i n . Most r i v e r s f lowing through t h e coas t a l mountains d r a i n re1 a t i v e l y sma l l , mostly a r i d a r ea s . As a r e s u l t , most e s t u a r i e s along t he west c o a s t (F igure 2 ) a r e smal l .

Local subsidence c r e a t e d t he bedrock trough in which San Franc isco Bay l i e s (Atwater 1979). Sea- leve l f l u c t u a t i o n s during t he pa s t few m i l l i o n y e a r s have c rea ted (and subsequent ly de s t royed ) e s - t u a r i n e embayments in t h e t rough a t t h e s i t e of t h e presen t San Francisco Bay (Atwater 1979). Core samples taken w i th in bay sediments suggest t h a t t h e r e have been a t l e a s t t h r e e cyc l e s of submergence and emergence of t h e bay reg ion , assoc i a t ed with t he major per iods of g l a c i a t i o n , i n t he mi l l i on yea r s before t h e formation of t he presen t e s t u a r y (Atwater 1979). Af t e r t he end of t h e l a s t g l a c i a l per iod , about 15,000 t o 18,000 yea r s ago, t h e s ea began i t s most r ecen t r i s e and en t e r ed t h e bay about 10,000 y e a r s ago. By 5,000 y e a r s ago, t he a r ea of t h e e s t u a r y was nea r ly what i t i s today (F igu re 3 ) . As po l a r icecap me1 t i n g slowed dur ing r ecen t mil - l e n i a , submergence of t h e bay slowed, and much of t h e re1 a t i v e change in s e a l eve l in t h e bay region s i n c e r e s u l t s from c r u s - t a l subsidence (Atwater e t a1 . 1977).

f .2 PRESENT-DAY PHYSlQGRAPHY

San Franc isco Bay comprises s e p a r a t e embayments: a d e e p e r c e n t r a l region near t he City of San F ranc i s co (Cent ra l Bay), and shal lower r e g i o n s (Suisun , San Pabl o , and South Bays; F igu re 4 ) t h a t a r e charac- t e r i z e d by broad s h a l l ows i nci sed by narrow channels f Figu re 5) whose depths w e maintained by r i v e r and t i d a l scour - ing . The average depth o f t h e bay i s about 6 m a t mean lower low water whi le median depth i s abou t 2 m (Conomos e t a1 . 1985). The p e r i m e t e r o f t h e bay, which once comprised 1 a r g e f r e s h - and s a l t w a t e r marshes, i s now l a r g e l y diked (Sec t i on 5.11, a1 though saa t evapo ra t i ng ponds and seasonal wet lands (some of them used f o r farming during t h e d r y season) cont inue t o provide wild1 i f e h a b i t a t ( Jo s se lyn 1983). Undi ked marshes remain on ly a t i s o l a t e d l o c a t i o n s .

1.3 CLIMATE AND WATER PROPERTlES

Cal i f o r n i a ' s c l imate c o n s i s t s o f a mild, wet win te r season (November-April ) and a dry summer season (May-October). As a r e s u l t , r i v e r i n f l o w i s high dur ing t h e midwinter months (1 ,000 t o 10,000 m3/s) and low (100-400 m v s ) dur ing summer and f a l l (Conomos e t a1 . 1985). The s t r o n g l y seasonal p a t t e r n o f r a i n f a l l and runof f imparts a s i m i l a r l y s t rong i n f luence on t he physical and chemical p r o p e r t i e s o f t h e e s tua ry , s een most r e a d i l y a s marked season- to -season d i f f e r e n c e s i n t h e s a l i n i t y of bay w a t e r s (F igure 6 ) . During a normal win te r , 1 ow-sal i n i t y (b r ack i sh ) water ( l e s s t han 2 pp t ) i s found a t t h e ea s t e rn end of San Pablo Bay, and s a l i n i t y in South Bay can f a l l below 15 p p t . During summer, b r a c k i s h water i s found a t t he ea s t e rn end o f Suisun Bay (and oc- ca s iona l l y f a r t h e r upstream), whi le t h e water in South Bay can be a s s a l i n e a s t h e adjacent ocean. Water t empera ture v a r i e s only about lOOC through t h e yea r ( roughly from 10 t o 200C).

Freshwater flows from t h e r i v e r s and River- i nduced seasona l v a r i a t i o n s i n streams of t h e Sacramento and San Joaquin the sa, i n i ty regime great ly in f luence the R i v e r system meet in a complex of i s l a n d s and channel s ( t h e Be1 t a ) , t hen empty i n t o dynamics of b i o l o g i c a l p o ~ u l a t i o n s (Cl oern t he nor theas te rn end o f San Francisco Bay and 1985) During high-winter (Figure 1). The t o t a l f l o w into t h e e s - r l v e r inf lows and 'lowered s a l i n i t y , p e l a g i c t ua ry from t h e Del ta r e p r e s e n t s about 90% spec i e s popu la t i ons I ~ h y t o p l a n k t o n , zoo- of t h e annual r i v e r inf low t o Sari plankton, f i s h ) i n t h e no r the rn reaches of Francisco Bay. A ? ? o t h e r r i v e r s and t h e bay can be d i s p l a c e d downstream by both streams e n t e r ~ n g t h e bay a r e comparat ively physical advec t ion and voluntary migra t ion . small , and most of t h e s e a r e i n t e r m i t t e n t This r i v e r in f low- induced movement a1 so with l i t t l e o r no flow dur ing t h e summer a f f e c t s some b e n t h i c s p e c i e s popu la t i ons months (Conornos e t a1 , 1985). (Chapter 3 ) .

Figure 3. Past shorelines of San Francisco Bay. (A) The advancement of sea level during the past 15,000 years (adapted from Atwater 1979); (0) the approximate position of the shoreline of the bay (landward edge of undiked tidal marshes) in 1850 and at present (adapted from Atwater el a!. 1979).

Hartman and Hammond (1985) have shown t h a t wind s t r e s s on the water surface i s the dominant fac to r maintaining water column oxygen a t or near atmospheric equilibrium concentrations a t a l l depths throughout the estuary. As a r e s u l t , the benthos of San Francisco, unlike t ha t of other es- tua r ies (e .g . , in the Chesapeake Bay estuarine complex; Officer e t a1 . 1984), i s not l imited by low oxygen. This was not the case several decades ago when the disposal of poorly t rea ted wastes caused severe depletion of water column oxygen, par t icular ly in South Bay in summer (Section 5 .1) . Wind mixing was apparently not suf f ic ien t t o counteract the e f fec t of waste-re1 ated oxygen demand before the construction of modern waste-treatment f a c i l i t i e s .

1.4 TIDES

Figure 4. The San Francisco Bay Estuary. Sites D6 Tides influence the dynamics of plant and D7 in Suisun Bay are California Department of and an imal species popul a t ens. I n par-

Water Resources sampling lacations for data shown t i cul a r , t hey a f fec t biological in Figures 24 and 25. productivity in i n t e r t i da l and subtidal

sediments by moving and mixing water masses (and associated organisms) and by varying the height of the water column above the bottom over a var ie ty of time

River inflow i s the major source of scales from hours t o seasons. Tides a l so the approximately 4.3 x lo6 tons of sedi - help t o disperse larvae, juveniles, and ment tha t en te r the bay each year from the adults of benthic species (Section 3.1.1). r ive rs , 80% of i t from the Sacramento-San Joaquin River drainage basin (Por terf ie ld e t a1 . 1961, Conomos e t a1. 1985). Most The t ida l range (maximum difference of the t o t a l sediment input occurs during between high water and low water winter, great ly increasing the tu rb id i ty elevations) i s g rea tes t (2.6 m) a t the ex- of the water (Figure 7 ) a s well as tremity of South Bay, decreasing t o 1.7 m sedimentation throughout the estuary. a t the Golden Gate ( the bay's narrow con-

nection t o the ocean), 1.3 m a t Suisun Strong seasonal winds a re important Bay, and t o progressively narrower ranges

in control 1 ing water c i rcu la t ion and fa r ther upstream. Such t i da l ranges, mixing (Conomos e t a l . 1985). Prevailing re la t ive t o the average bay depth of 6 m, west and northwest winds, reinforced by contribute to a t ida l prism ( the volume of so la r heating of a i r masses in inland water between low and high t i d e l eve l s California, are strongest during the sum- tha t passes in and out of the bay during mer. These winds generate complex each t ida l cycle) t ha t i s about 24% of the bay-wide water c i rcu la t ion pat terns tha t bay's t o t a l vof ume. The la rge , rapid ex- are superimposed on t i de - and r iver - change of water with the ocean produces induced c i rcu la t ion (Wal t e r s e t a1 . 1985). strong t i da l currents throughout the bay, The complex wind-induced c i rcula t ion pat- par t icular ly a t physiographic constr ic- terns have important implications fo r a l l t ions such as Carquinez S t r a i t and the physical and biological processes in the Golden Gate (Figure 4 ) . Current estuary (Cloern and Nichols 1985). Some ve loc i t i es a t the Golden Gate can reach of the e f f ec t s of c i rcula t ion pat terns on 280 cm/s. the benthos a re discussed in Chapter 4. Winds are a l so a major fac to r in control - The t i de s are of the mixed semidiur- l ing oxygen concentrations in the estuary. nal variety, with two lows and two highs

4

Figure 5. Bathymetry of San Francisco Bay (adapted from Nichols and Thompson 1985a).

dur ing each 24.84 hours. Any two succes- s ive highs o r successive lows are u s u a l l y very d i f f e r e n t i n he igh t . I n any month the i n t e r t i d a l zone i s exposed day and n i g h t dur ing both neap and spr ing t i des . Nonetheless, t he re i s a seasona l i ty i n t h e occurrence o f extreme low and h igh water: the greates t t i d a l exposure o f t h e mudflats occurs a t n i g h t i n the' w in te r months and dur ing t h e day i n spr ing and summer months. Thi s phenomenon accen- tuates the spr ing growth o f benth ic p lan ts

(Section 4 .2 .4 ) which, i n tu rn , con- t r i b u t e s t o h i g h l y seasonal growth o f benth ic herbivores (Sect ion 3 . 1 . 2 1 .

1.5 SEDIMENT TEXTURE AND DYNAMICS

Near ly h a l f o f t h e sur face area of San Francisco Bay a t h igh t i d e i s covered by water l e s s than 2 m deep, and more than 15% i s above the l e v e l o f mean lower low

South flay

,

- -4 ?

I

25' S-SJ flow 150 m3 s

30 b SBS flow 3 rn3s

\-

Typical Winter

" S SJ flow 2700 m3s 1

SBS flow 13 m3 s

Figure 6. Horizontal and vertical distribution of salinity, uncorrected for tidal variations, undertypical summer (A) and winter (El) flows for the Sacramento-San Joaquin River system (S-SJ) and South Bay streams (SBS); plan view distorted for ease of display (adapted from Conomos et al. 1985).

water. These broad a r e a s with l i t t l e ver- t he r i v e r s and resuspended by wind waves t i c a l re1 i e f (Figure 8) a r e covered with and t i d a l cu r r en t s . s o f t mud (genera l ly more than 80% s i l t + c l a y ) . Mud i s found a t a l l depths The bottom of Central Bay i s covered in t h e southern end of t h e bay, although by sand waves up t o 8 m high t h a t move the mud o f l a r g e a reas of t he eas t e rn with t h e s t r o n g ebb and f lood t i d a l flow shallows of South Bay i s mixed with s h e l l through t h e Golden Gate (Rubin and fragments- -remnants o f once- thr iv ing beds McCull och 1979). Only a1 ong t h e s h a l l ow of na t ive and introduced oys t e r s (Chapter ea s t e rn s h o r e l i n e o f t h i s a rea does mud 6) . Strong t i d a l c u r r e n t s and r i v e r - in- again predominate (Figure 9 ) . Surface duced g r a v i t a t i o n a l cu r r en t s , p a r t i c u l a r l y sediment t e x t u r e v a r i e s markedly with time during winter , a r e focused in t h e deep as a r e s u l t o f seasonal v a r i a t i o n s in a reas of Central Bay, in t h e narrow r i v e r i n f low, t i d e s , and winds (Thompson s t r a i t s s epa ra t ing t h e major embayments, e t a1 . 1981; Nichols and Thompson 1985b). and i n t he narrow midbay channels (Figure Much of t h e f ine-gra ined r iver -borne s e d i - 5). This focusing of c u r r e n t s con t r ibu te s ment t h a t i s t r anspor t ed down r i v e r during t o well -winnowed, coa r se channel -bottom the high-flow per iods of winter and e a r l y sediments i n t h e c e n t r a l and northern em- spr ing bypasses Suisun Bay and accumulates bayments (Figure 9) . Conversely, cu r r en t in San Pabl o Bay (Kl ingeman and Kaufman v e l o c i t i e s a r e lower over t h e l a t e r a l 1963, 1965; Conomos and Peterson 1977). shoals in each embayment, permi t t ing t h e I n t h e process , Suisun Bay f i n e sediment deposi t ion of f i n e sediments supplied by i s winnowed during t h e high-flow season,

6

: L't~ilrral i Sarz Pahlu j Suivr,,, ecau Sortrh HUJ, i HUJJ j Ray :

Figure 7. Horizontal and vertical distribution of turbidity, uncorrected for tidal variations, undertypical summer (A) and winter (B) conditions; plan view distorted for ease of display (adapted from Conomos et ai. 1985).

Figure 8. A mudflat of South Bay.

leaving re1 atively more coarse sediment (Figure 10). During summer and autumn the pattern is reversed: fine sediment is resuspended and transported away from San Pablo Bay at the same time that it is being deposited in Suisun Bay. In South Bay, sediments may locally accumulate on intertidal mudfl ats during autumn and winter, but these deposits are usually removed during the following spring and summer (Figure lo), a result of increased wind- and t ide-induced current scour (Nichol s and Thompson 1985b).

Repeated deposi tion and resuspension of the same sediments are predominant characteristics of San Francisco Bay. Full er (1982) concluded from a comparison of resuspension and aecumul ation rates

n Silt/Clay Sand Shell - 2m

,-,--- 1 Om

Figure 9. Generalized distribution of surface sediment texture in San Francisco Bay (from Nichols and Thompson 1985b).

tha t sediments in deep a reas of South Bay are resuspended a t l e a s t two t o f i v e times before f ina l bur ia l . Apparently superimposed on typical seasonal cycles of deposition and resuspension are intense periods of erosion or deposi t ion t h a t can rapidly change the sediment st:; face (Section 3.2.1; Nichols and Thompson 1985a).

Surface sediments are we1 1 oxidized throughout the year in San Francisco Bay, l argely because the water column above remains we1 1 oxygenated. Occasional l y , 1 ocal i zed accumul a t i ons of decaying macro- a1 gal species f o l l owing unusual summer blooms (Horne and Nonomura 1976; Josselyn and West 1985) have resul ted in anoxia a t the sediment surface (Section 3.2.1).

northern South Bay

southern South Bay

M A M J J A S O N D J F ' M A M J J A S O N D J F

Figure 10. Percentage of mud (silt + clay) collected in the shallows (less than 5-rn deep) during 1980-81 in four embayrnents of San Francisco Bay; average of 4-6 stations in each embayrnent (from Nichols and Thompson 1985b).

CHAPTER 2. BIOTIC COMMUNITIES--DESCRIPTIVE REVIEW

The benthos of t h e e s t u a r y encom- passes a wide range of taxonomic and func t iona l e n t i t i e s , from b a c t e r i a t o l a rge c r abs . This prof i 1 e focuses , however, on ly on infaunal i n v e r t e b r a t e s , t he sma l l e r , r e l a t i v e l y s e s s i l e animals l i v i n g on o r in s u r f a c e sediments t h a t can be c o l l e c t e d in c o r e o r g rab samples. In t h i s chapter we cons ide r t h e d i s t r i b u t i o n and abundance o f t h e major taxonomic ca t ego r i e s of i n v e r t e b r a t e s p r imar i l y by s i z e groupings, a l though i n many ca se s t he se a r e func t i ona l groupings a s we l l . In t h e fol lowing chap t e r , we cons ide r t h e population dynamics w i th in macrobenthic spec ies and spec i e s groups, a s well a s t h e i n t e r a c t i o n s among them.

2.1 BACTERIA, MICROFAUNA, AND MEIOFAUNA

The smal le r organisms of aqua t i c ben- t h i c communities inc lude t h e microfauna ( u n i c e l l u l a r organisms such a s f l age1 1 a t e s and c i l i a t e s t h a t a r e seen only under high magni f ica t ion) and meiofauna (small metazoans t h a t a r e mostly v i s i b l e with t h e unaided eye but r e q u i r e low magni f ica t ion f o r i d e n t i f i c a t i o n and count ing , along with some l a r g e u n i c e l l u l a r forms) . The meiofauna, g e n e r a l l y i n t h e s i z e range of 0.1 t o 0.5 mm, i s a d i v e r s e group t h a t i n - c l udes permanent mei ofauna (nematodes, os t racods , kinorhyncns, harpac t i co id copepods, f o r amin i f e r ans ) and temporary meiofauna ( t h e l a r v a e and young of the macrofauna). The 1 a r g e s t animal s , t h e macrofauna, a r e those organisnls t h a t a r e r e t a ined on a 0.5-mm s i e v e .

The re1 a t i v e d e n s i t i e s and biomass of b a c t e r i a , microfauna, mei ofauna, and macrofauna vary among t h e many benth ic systems s tud ied (Gerl ach e t a1 . 1985). What i s known from s t u d i e s worldwide, however, sugges t s t h a t small organisms can be importamt. For example, Fenchel (1969) showed t h a t whi le macrofauna may be

dominant in biomass, t h e sma l l e r c i l i a t e s may be dominant i n terms of t o t a l metabo- l i sm ,

The r o l e of meiofauna i n t h e benthos i s s t i l l being c l a r i f i e d . Considerable research on meiofauna i n o t h e r e s t u a r i e s has demonstrated t h e importance of i t s r o l e in benth ic food webs(Coul1 1973; Coull and Bell 1979; Reise 1979; Heip 1980; Bouwman e t a l . 1984). In t h e Dutch Wadden Sea, f o r example, t h e meiofauna may be more important than t he macrofauna i n t h e t r oph i c cha in lead ing t o demersal f i s h production (Kuipers e t a l . 1981).

Q u a n t i t a t i v e knowledge of b a c t e r i a , mi c rofauna , and meiofauna i n San Francisco Bay i s , however, nea r ly nonexis ten t . Some b a c t e r i a l processes i n San Francisco Bay sediments have been s tud i ed (Sec t ions 4 .2 and 4 . 4 ) . B u t , o t h e r than severa l s t u d i e s of recent foramini f e r an d i s t r i b u t i o n s i n San Francisco Bay (Arnal e t a l . 1980, and t h e papers c i t e d t h e r e i n ) , no l i t e r a t u r e e x i s t s on t he bay meiofauna. The i r small s i z e and t he absence of l oca l s p e c i a l i s t s on t h i s group ( o t h e r than f o r t h e foramini fe ra ) have con t r i bu t ed t o t h e pauci ty of publ ished s t u d i e s . An unpublished s tudy of t h e abundance of meiofauna in oxygenated s u r f a c e sediments of t he e a s t e r n shore of South Bay near Wayward showed t h e presence of more than 2.5 x l o6 nematode worms pe r square meter, more than 5 x l o 5 ha rpac t i co id copepods per square meter , and fewer amphi pods, po lychae tes , o s t r acods , and foramini fe rans (E.B. Lyke, Ca1 i f o r n i a S t a t e Univers i ty , Hayward; pe r s . comm.) . Other unpublished observa t ions of meiofaunal d i s t r i b u t i o n s a t two l o c a t i o n s s? t h e western shore (Cor te Madera and Palo Al to ; Figure 4 ) showed t h a t o s t r acods and nematodes predominate i n muddy i n t e r - t i d a l sediments, while ha rpac t i co id s a r e much l e s s numerous ( M . M . Pamatmat, unpubl . ) .

2 .2 .1Gene ra l i z ed D i s t r i b u t i o n s and Re1 a t i ve Abundances of Common Species

The d i s t r i b u t i o n of s p e c i e s in t h e o f t - s t u d i e d sof t -bo t tom macrobenthic i n - v e r t e b r a t e community of San Francisco Bay (organisms r e t a ined on 0 .5 o r 1.0-mm screens) appears t o be most s t r ong ly i n - fluenced by temporal v a r i a t i o n s i n sa l i n i t y (Nichols 1979; Nichols and Thompson 1985b). Away from t h e marine environment of Central Bay, t h e benthos i s cha rac t e r i zed by low d i v e r s i t y and dominated numerical1 y by a few spec i e s (common t o many U.S. e s t u a r i e s ) t h a t a r e t o l e r a n t of wide s a l i n i t y v a r i a t i o n s (Ni chol s and Thompson 1985a).

Suisun Bay i s a b rackish-water embayment cha rac t e r i zed by i s l ands and s h a l l ow sub-bays i n t e r s e c t e d by t i d e - and r i v e r - scoured channels . I t i s inhabi ted by fewer than 10 permanent macrobenthi c spec ies because t h e reg ion i s inundated each w in t e r by f reshwater . Spec ies t h a t can surv ive t h e r e i nc lude t h e mollusks Macorna b a l t h i c a , a r e n a r i a (and occasional l y t h e f r e shwa te r spec i e s Corbicula fluminea when r i v e r inf low i s unusually h i g h ) ; t h e amphipods Coroohium stimpsoni and C. sp in i co rne ; and t he an- nel i d s Nereis succ inea and Limnodril us hof fmeis te r i ( F i l i c e 1958; Aldrich 1961; Pa in t e r 1966; C a l i f o r n i a Department of Water Resources 1986) . Occas iona l ly , during pro1 onged pe r iods - of 1 ow r i v e r flow and increased s a l i n i t y , t h e polychaete S t r eb lo sp io benedic t i and t h e amphipod Amoelisca abd i t a ( i d e n t i f i e d u n t i l r e cen t ly a s Amoelisca m i l l e r i , and in some r epo r t s dur ing t h e 1960's a s Phot i s cal i f o rn i c a ; Carl ton 1979a, b) migra te upstream t o Suisun Bay (Nichols 1985b). These l a t t e r two s p e c i e s a r e normally r e s t r i c t e d t o t h e p a r t s of t h e bay west of Carquinez S t r a i t because of t h e i r i n - to1 erance of f reshwater .

West of Carquinez S t r a i t , where s a l i n i t y seldom f a l l s below 5 pp t , d i v e r s i t y i nc r ea se s ( F i l i c e 1958; Nichols 1979). The macrobenthic community of t h e broad, shal low s u b t i d a l expanses of San Pablo Bay comprises, i n add i t i on t o Macoma ba ' l thica and &a a r e n a r i a , t h e mollusks Gemma gemrna, Muscu'lista senhousia , Tapes --

phi l i m i narum (= Tapes Jaooni c a ) , and I1 yanassa obso l e t a ; t h e amphi pods Ampel i s c a abd i t a , Grand id i e r e l l a j a o o n i c a , and Corophium spp. ; t h e po lychae tes S t r e b l o s ~ i o bened i c t i , Heteromastus f i l i f o r m i s , Glvcinde sp . , and severa l s p e c i e s of Polvdora inc luding 1. 1 i s n i ; and severa l 01 igochaetes (F i l i c e 1958; Hopkins 1986; F . H . Nichols and J.K. Thompson, U.S. Geological Survey, unpubl . ) . Some of t h e s e spec i e s a r e "euryhal i n e oppo r tun i s t s " (Grass le and Grass le 1974; Boesch 1977) t h a t a r e common i n many U.S. e s t u a r i e s . Macoma b a l t h i c a predominates in both abundance and biomass in t h e macrobenthic community of t h e broad shal low i n t e r t i d a l reaches of nor thern San Pablo Bay. The abundance of o t h e r s p e c i e s t h a t a r e common s u b t i d a l l y may be 1 imited i n shal low a r e a s by reduced s a l i n i t i e s and heavy s i l t a t i o n during w in t e r and windwave scour ing i n summer (Hopkins 1987).

The e s t u a r i n e community t y p i c a l of San Pablo Bay grades i n t o a marine community i n t h e deeper and more s a l i n e Central Bay ad j acen t t o t h e C i ty of San Francisco. Here, s t r ong t i d a l c u r r e n t s c r e a t e a h igh ly dynamic bottom c o n s i s t i n g of l a r g e sand waves t h a t r e v e r s e d i r e c t i o n on each t i d e (Rubin and McCulloch 1979). The benth ic community i s composed l a r g e l y of spec ies t h a t a r e found in sand s e d i - ments along t h e o u t e r c o a s t ( S t o r r s e t a l . 1965; Liu e t a l . 1975; Nichols 1979). I s lands and o t h e r rock outc rops i n Central Bay a r e inhabi ted by ha rd - subs t r a t e o r - ganisms with marine a f f i n i t i e s , a s well a s by t he cosmopol i t a n bay mussel Mvti 1 us edul i s .

South of San Franc isco , t h e spec i e s found i n San Pablo Bay a r e jo ined , in t h e sub t ida l mud a r e a s , by high d e n s i t i e s of t h e l a r g e tube-dwell ing polychaete Asvchis e lonqa ta . In t he i n t e r t i d a l and shaf low sub t ida l reaches o f South Bay, Gemma gemma, Amoel i s ca abdi t a , and S t r eb l o s ~ i o benedic t i a r e t h e overwhelming numerical dominants, a l though l a r g e numbers of i n - d i viduaf s of o t h e r s p e c i e s occasional l y appear (Nichol s and Thompson 1985a). While much l e s s abundant than Gemma, Am~el i s c a , and S t r e b l o s ~ i o , t h e molfusks Macoma b a l t h i c a , a r e n a r i a , and I l vanassa obsol e t a o f t e n r ep re sen t t h e bulk of benth ic i n v e r t e b r a t e biomass (Ni chol s 1979; Thompson and Ni chol s 1981 j . Where t h e bottom i s covered with she77 depos i t s (F igure 9 ; remnants both of t h e

e a r l y P a c i f i c o y s t e r i n d u s t r y and the a n - c i e n t d e p o s i t s o f t h e n a t i v e o y s t e r , Ost rea l u r i d a ; H a r t 1966), i n v e r t e b r a t e s -- assoc ia ted w i t h hard bottoms, such as Crep idu l a spp., Urosal p i n x c ine rea , Moqul a manhattensi s, Muscul i s t a senhousi a, and u n i d e n t i f i e d hydrozoans, che i l ostome bryozoans, and a c o n t i a t e anemones, a re found. T a ~ e s p h i l i pp inarum i s a1 so common i n t h e s h e l l y depos i t s .

2 . 2 . 2 Baywide P a t t e r n s o f Macro- i n v e r t e b r a t e Biomass

The o n l y s y n o p t i c survey o f macro in - v e r t e b r a t e biomass (sampled t w i c e d u r i n g 1973; N i cho l s 1979; Thompson and N i c h o l s 1981) demonstrated (1) t h e ma jo r c o n t r i bu- t i o n o f mo l lusks t o t o t a l i n v e r t e b r a t e biomass everywhere i n t h e bay, and (2 ) t h e concen t ra t i on o f g r e a t e s t t o t a l biomass i n South Bay (Table 1 ) .

The p r i n c i p a l c o n t r i b u t o r s t o biomass throughout much o f t h e bay a re t h e mol - l u s k s Tapes p h i l i ~ p i n a r u m , Muscul i s t a senhousia, Macoma ba l t h i c a , ~ arena r i a , Gemma gemma, and I l vanassa obso le ta . I n a d d i t i o n , t h e 1 a rge tube-dwe l l i n g po lychaete Asvch is e l onqa ta i s a ma jo r c o n t r i b u t o r t o t o t a l biomass i n t h e muddy s u b t i d a l areas o f South Bay (N i cho l s 1979). Because sampl i ng d u r i n g t h i s s i n g l e baywide survey was conducted o n l y t w i c e d u r i n g one year , meaningfu l seasonal comparisons a re n o t p o s s i b l e .

2.3 INTRODUCED INVERTEBRATES

O f a l l t h e common b e n t h i c spec ies l i s t e d above, o n l y t h e po lychae te G lyc inde sp. ( a spec ies be l ong ing t o t h e G. armiqera/pol yqnatha compl ex ) , and t 6 e b i v a l v e m o l l usks Macoma ba l t h i c a and M v t i l u s e d u l i s a re n a t i v e s . The o t h e r s were a c c i d e n t a l l y o r i n t e n t i o n a l l y i n t r o - duced (Ca r l t o n 1979a, b) . Moreover, t h e r e i s devel op i ng ev idence f r om e l e c t r o p h o r e t i c s t u d i e s t h a t Macoma b a l - t h i c a may a l s o be i n t r oduced : t h e y a r e g e n e t i c a l l y much more s i m i l a r t o U.S. e a s t coas t 1. b a l t h i c a t han t hey a re t o those c o l l e c t e d f rom Coos Bay, Oregon (B.W. Meehan, V i r g i n i a I n s t i t u t e o f Mar ine Science; pers . comm.). However, because i t s na t i ve / i n t r oduced s t a t u s has n o t been f o rma l l y reso lved , we c o n t i n u e t o r e f e r i n t h i s p r o f i l e t o M. b a l t h i c a as a n a t i v e spec ies.

The immigrants who f l o c k e d t o t h e west coas t o f t h e U n i t e d S t a t e s d u r i n g t h e Gold Rush o f t h e l a t e 1840's and 1850's brought w i t h them a t a s t e f o r f r e s h oys te rs , b u t d i d no t ca re f o r t h e dark , s t r o n g - t a s t i n g meat o f t h e l o c a l o y s t e r Ost rea l u r i d a . L i v e o y s t e r s were impor ted -- t o San Franc isco by s h i p f rom Mexico, t h e P a c i f i c Nor thwest , and Japan. S h e l l s o f t h e va r i ous spec ies can s t i l l be found on bay i n t e r t i d a l f l a t s ( F i g u r e 11) . W i t h t h e comp le t ion o f t h e t r a n s c o n t i n e n t a l r a i l r o a d i n 1869, l a r g e - s c a l e shipment o f

Table 1. Weight (g10.1 m2) and percent (%) of total sample wet weight for Molluscs, Annelida, Arthropoda, and all other phyla combined; data are averages of 4 to 13 stations in each region of the bay. Samples were collected during January-February (winter) and during August (summer) 1973 (Thompson and Nichois 1981).

Mol lusca Anne l i da Arthropods Other Phyla Total - winter s m r winter s m r inter s m r winter s-r u in te r smr

Locat i an 9 (%I g (%I g (%) g (%) g (%) 9 9 9 (%I 9 (%) g (%)

Suisun Bay 13(81) 4(67) 3(19) 1(17) <1(<1) <1(<1) < I ( < ? ) l (17) 16 6

San Pablo Bay 36(90) 56(88) 2 ( 5 ) 1 (2) < I ( < ? ) 2 ( 3 ) 1 (2) 4 (6 ) 40 64

Centra! Bay 41(70) 6(14) ?(I21 13(31) 1 ( 2 ) 59 42 2 (5 ) Y(15) 21(50)

U w r South 6ep 466(85) 332(83) & ( i 2 > 49(IZ) 5 ( I j b (2) 13 ( 2 j : 5 (41 549 402

Lower South Bay 81(92) 1?1(92; 6 (7 ) 8 ( 4 ) <1i<1) 2 (1) 1 ( 1 ) 6 (3) 88 207

Figure 11. Accumulated oyster shells of assorted species on a South Bay mudflat.

mature eastern oysters , Crassostrea *- i n i c a , and, l a t e r , seed oysters fo r maturing on t he mudflats of coastal bays, became possible. An average of 100 car- loads of seed oysters were shipped each year between 1875 and 1910. By the l a t e 1890's, oys te r s became Cal i fo rn ia ' s most valuable f i shery product (Barret t 1963).

The eastern oyster never became naturalized i n San Francisco Bay (transplanted adul ts fa i 1 ed t o produce suff ic ient young), b u t i t s large-scale introduction contributed to one of the most s ignif icant bay-wide ecological changes recorded s ince. Species associated with the oyster in i t s native habi ta t became unintentional fellow t ravelers on the transcontinental t r i p and subsequently es - tab1 i shed themselves in San Francisco Bay with phenomenal success. Carlton, in h i s review (1979b) of species introductions in the bay, commented t ha t "A s ingle oyster she1 1 may have upon i t representatives of 10 or more inver tebrate phyla, comprising dozens of species , and these numbers can be great ly increased when oysters are packed together fo r shipment with associated clumps of mud and algae, and with water pockets in empty valves used as cul tch. " Biologi s t s recorded the ap- pearance of many o f these exotic specles during the period of oyster importation (Figure 12). However, the enormous s ig - nificance of species introductions,

including those associated with the oyster industry as we?? as those attached t o or bored into ship hulls or contained in ship bal las t and subsequently released t o the bay, was not realized fo r nearly 100 years (Carlton 1979a,b). In t o t a l , about 100 species of exotic estuarine/marine invertebrates have become establ i shed. These include the edible sof t -shel led clam arenaria and the Japanese 1 i t t leneck clam Tapes phi1 ippinarum--the only two moll usk species represented today in the bay sport f isheries--and such pest species as the shipworm Teredo navalis and the oyster d r i l l Urosa l~ inx cinerea. Now, nearly a l l the common macroinvertebrate species present on the inner shallows of the bay are introduced (Nichols 1979; Nichols and Thompson 1985a). Some of these species, such as the amphipod Ampel isca abdita, are abundant nearly everywhere in the bay (Figure 13). The t ida l freshwater water- ways of the lower Sacramento and San Joaquin Rivers and Delta, as we1 1 as of California 's i r r iga t ion canals, contain huge numbers of the introduced freshwater cl am Corbi cul a f l umi nea.

Introduced invertebrates are evident a t the edge of the bay t o even the most casual observer. The bayward edges of the Sa l icorn ia /S~ar t ina marshes throughout the bay are populated by the eastern ribbed mussel Geukensi a demi ssa (= Ischadium demissum, Modiolus demissus) (Figure 141, and the slopes formed by ongoing erosion of the marsh edge in many South Bay and San Pablo Bay locations (Atwater e t a1 . 1979; Carlton 1979b) are perforated with (and ultimately destroyed by) the burrows of the introduced isopod Sohaeroma auoyana (Figure 15). A t the base of these slopes and in t ida l channels the mudsnail Ilvanassa obsoleta resides in great numbers. While i t i s typical ly found in re la t ive ly small numbers on open South Bay mudfl a t s , I1 yanassa i s occasionally extremely abundant (Figure 16) . A t the base of r iprap dikes and breakwalls, par- t i cu l a r l y where the sediments contain some cobbles and sand, the Japanese 1 i ttl eneck clam Tapes philiapinarum i s eas i ly found by clam diggers.

Total mollusk biomass i s dominated by introduced species in a l l regions of the bay except Central Bay, where a variety of native marine species predominate, and i n Sui sun Bay, where Macoma bal th i ca normally predominates (Figure 17; Thompson and Michols 1981), I f , as mentioned above,

I I

l 4 t Cumulative Nur-nber 0 f

/ l ntroduced Mollusk Species :~fusctrlisrrt senltousia

N~l.sj.cocyprrs cut~alic~rtluitts

phciludifhrttris

Lyrodtcs priiirellutns

Figure 12. Cumulative number of introduced mollusks by date of discovery (adapted from Nichols et a!. 1986; derived from data in Gariton 1979b).

Macoma ba l th i ca proves t o be another i n - *-- ---- traduced spec i e s , t he percentages shown in Figure 17 f o r n a t i v e spec ies in Suisun, San Pablo, and South Bays would be g r e a t l y diminished.

Accidental ly introduced spec i e s may have th r ived in San Francisco Bay in pa r t because t h e bay, l i k e o the r P a c i f i c coas t e s t u a r i e s , contained r e l a t i v e l y few na t ive spec ies as compared with the e s t u a r i e s on the U.5, e a s t coas t (Jones 1940, Hedgpeth 1968, Carl ton 1979a,b) . i h i s was t he case , apparent ly , because of t h e geologic y o u t h and geographic i s o l a t i o n of west coas t e s t u a r i e s (F igure 2 ) : a d ive r se l o - cal fauna had apparent ly not y e t evolved p r i o r t o t he i n t roduc t ion of spec ies (f-ledgpeth 1968). The predominance of a s i n g l e h a b i t a t type { s o f t mud) over wide a reas of t h e bay may a1 s o have r e s t r i c t e d the number of spec i e s t h a t were e s t ab - 1 ished t h e r e . Sources s f po ten t i a1 colonizing spec i e s not commonly a p a r t o f t he soft-mud community may have been too small o r t oo f a r removed s p a t i a l l y from

the bay's mudflats t o be e f f e c t i v e sources of co lonizers (Nichols and Thompson 1985a).

The success of t h e introduced spec ies may a l so be r e l a t e d t o t h e i r f l e x i b l e 1 i f e s t y l e s . The introduced s ~ e c i e s a r e we11 known in e s t u a r i e s o f t he ea s t e rn United S t a t e s a s o p p o r t u n i s t i c co lon ize r s of underexploi t ed o r d i s tu rbed h a b i t a t s (Nichols and Thompson 1985a). They have sho r t l i f e spans, produce l a r g e numbers a f young, a r e t o l e r a n t of a wide range of sa l i n i t y , temperature, and s u b s t r a t e t ype , and can be r e a d i l y d ispersed around t h e bay by t i d e - and wind-driven c u r r e n t s . The l a rge seasonal v a r i a t i o n s in r i v e r i n - flow, with consequent v a r i a t i o n s i n s a l i n i t y , con t r ibu t e t o an i n s t a b i l i t y of the benthic environment t h a t enhances t h e success of the oppor tun i s t s r a t h e r than longer l i ved "equi 1 i b r i um" spec i e s f as in McCall 1977) . The same hard iness t h a t pcrmitted t h e e a s t e r n spec i e s t o surv ive the long t r anscon t inen ta l t r a i n r i d e s

20K ~ l r i 1 _

Figure 13. Distribution and abundance of Ampelisca abdita (= Ampelisca rnilleri = PhofiS caiifornica in earlier local studies; Carlton 1979a,b) (from Hopkins 1986).

Figure 14. The introduced eastern ribbed mussel, Figure 16. An unusually high concentration of the Geukensia demissa, at the edge of a Spartina foliosa introduced mudsnail llyanassa obsolefa on a South marsh in South Bay. Bay mudflat, November 1985.

Figure 17. Proportions of introduced 311d native species relative to 'total biomass (wet weight) of mollusks in major subareas of San Francisco Bay (averages trom four to seven stations per subarea,

Figure 95. Eroding edge of a San Francisco Bay three samples per station). These propsrtions marsh, perforated by burrows sf the introduced assume that Macoma balthica is a native species, an isopad Sphaeroma quoyana. assumption that may be invalid; see text.

probably insured t h e i r successfu l e s t a b - 1 ishment i n San Fra.nci sco Bay.

We do not know how t h e introduced spec ies a f f ec t ed the n a t i v e benth ic community, but they may have a1 t e r e d t h e d i s t r i b u t i o n and surv iva l of some of t h e i r na t ive coun te rpa r t s . In one documented case (Race 19821, t h e range o f t he na t ive hornsnail Ceri t h idea ca l i f o r n i c a i s r e s t r i c t e d mainly t o marsh pannes (F igure 18) by competi t ive i n t e r a c t i o n with and predation by t h e introduced mudsnai l I lyanassa obso le t a . I t i s l i k e l y t h a t , before I1 vanassa was introduced,

Figure 18. The sart-panne habitat of the native hornsnail Cerithidea califorffica.

CerithSdea was found on t h e open mudflats o f t h e b a y . I t i s a l s o poss ib l e t h a t before t h e i n t roduc t ion of Ameel i s c a &- m, Macoma b a l t h i c a was t h e most abundant i n v e r t e b r a t e of t h e bay 's i n t e r - t i d a l mudflats (Sect ion 3 .2 .3 ) . I f so , i t may have provided t h e most important source of n u t r i t i o n f o r migratory shorebi rds .

2.4 PREDATORS ON THE BENTHOS

The importance of preda t ion on t h e bay's clams and o y s t e r s has been recognized s ince t h e e a r l y days of s h e l l f i s h harves t ing in t h e bay (Bonnot 1932a, 1935; Ba r r e t t 1963). The beds of o y s t e r s (Ostrea l u r i d a ) imported from t h e S t a t e of Washington during t h e 1850's were fenced with s t akes t o keep out p reda to r s , par - t i c u l a r l y r ays ( B a r r e t t 1963). Bonnot (1932a) noted t h a t "The s t i n g r a y s and f lounders e a t va s t q u a n t i t i e s of t h e [ s o f t - s h e l l clam a rena r i a ] . The s t i ng rays w i l l d ig and e a t t h e whole clam. The f lounders b i t e o f f t h e i r s iphons." The preda tors mentioned by Bonnot a r e probably t h e bat ray My1 i o b a t i s c a l i f o r n i c a and t h e s t a r r y f lounder P I a t i c h t h ~ s s t e l l a t u s which, with t h e leopard shark T r i a k i s s emi fa sc i a t a , may be respons ib le f o r some of the d i s c e r n i b l e feeding depress ions on mudflats (F igure 19 ) . The p r a c t i c e of s h e l l f i s h bed fencing t o prevent t h e s e

Figure 69. Feeding depressions (about 15 cm in diameter), probably made by the bat ray (MyIiatratis californicaf, known to feed on the mudftats at high tide.

species and o the r s from deple t ing t h e beds continued throughout t h e period of oys t e r growing and s o f t - s h e l l clam harves t ing (Chapter 6 ) . Native epi benthic inver- t e b r a t e s such as t h e Dungeness c rab Cancer maqister , t h e bay shrimp Cranson spp . , t h e shore crab Hemis ra~sus oresonens is , and the channeled whel k Busycotv~us canal i cul a t u s a r e a l s o important predators , depending on loca t ion within the bay and time of yea r .

S tudies of bay f i s h e s , c rus taceans , and b i rds ( e . g . , Heubach e t a l . 1963, Ganssle 1966, Radtke 1966, Stevens 1966, Boothe 1967, Thomas 1967, McKechnie and Fenner 1971, Daniels and Moyle 1983 f o r f i s h e s ; Russo 1975 f o r e l asmobranchs; Recher 1966 f o r b i r d s ; Wahle 1985 f o r shrimp) o f t en have included observa t ions of stomach con ten t s . While not q u a n t i t a -

t i v e , t hese s t u d i e s show c lea r ly t h a t t h e benthos i s a major source of n u t r i t i o n . Use of such s t u d i e s f o r purposes of d e t e r - mining p rec i se feeding h a b i t s and r a t e s i s l imi t ed , however, in t h a t p a r t l y d iges ted stomach contents may not neces sa r i l y provide a t r u e p i c t u r e of food s e l e c t i o n . Recher (1966), f o r example, showed from shorebird g izzard contents t h a t prey se l ec t ion was spec ie s s p e c i f i c (Table 21, and t h a t the l a r g e polychaete Nereis succinea was the apparent prefer red food item f o r many spec ie s . He noted, on t h e o the r hand, t h a t while clams represented only a small percentage of stomach contents of l ong-b i l l ed shorebird spec ie s , t hese b i rds were rou t ine ly observed t o e x t r a c t clams (Macoma bal t h i c a and a r e n a r i a ? ) from the mud. Small sof t -bodied animals such as S t r e b l o s ~ i o benedic t i and o the r pol ychaetes would probably be over1 ooked in analyses of stomach contents a s wel l .

Table 2. Percent composition of food items occurring in the gizzards of shorebirds col!ected at Palo Alto (Recher 1966).

B i r d species ( w i t h number o f gizzards analyzed)

Black- Least Western Red- Semipalmated bellied Sand- Sand- Backed Marbled

inver tebrates Plover Plover Avocet Dowitcher p iper piper Sandpiper Knot Godwit U i i l e t

recovered ( 3 ) ( 3 ) ( 9 ) ( 2 7 ) ( 3 8 ) ( 7 8 ) ( 4 6 ) (3) (9) ( 1 6 )

Amph i pod species 4.0 21 .I 8.6 8.9

Hereis succinea -- 94.5 16.4 16.0 71.4 5.3 8.6 70.0 44.0 76.0 4.6

Ostraccd species 0.5 4.0 9.6 57.8 62.8 9.7

I lyanassa obsoieta

e1/4 inch 2.2 1 .8 2L. 0 7.4 10.5 11.4 5.8 2.5 9.9

>1 /4 inch 65.5 2.1 1 .B 0.7 8.7 33.2

Geukensia demissa -- 0.8

Mya arenaria and

b a l t h i c a

Hemigrapsus cregonensis - 3.1

Average nwrlbfr iif

items per g~zza-o 137 5 5 25 FL 38 35 '21 159 7'35 132

2.5.1 Feedinq Modes

There has been, t o our knowledge, only one s tudy of i n v e r t e b r a t e feeding i n t he San Francisco Bay Estuary: Foe and Knight9 s (1985a, 1986) s tudy of Corbicul a fluminea i n t h e t i d a l f reshwater region of t he e s t u a r y . l i f e h i s t o r i e s and feed ing modes of t h e common i n v e r t e b r a t e s of San Francisco Bay must, t h e r e f o r e , be i n f e r r e d from s t u d i e s of t h e s e spec i e s i n o t h e r United S t a t e s e s t u a r i e s . Feeding modes ( t h e mechanism of food t r a n s p o r t from t h e environment i n t o t h e organism; Fauchald and Jumars 1979), whi le h igh ly dependent on t he func t i ona l morphol ogy o f each spec i e s , a r e a1 so l o c a l l y inf luenced by s u b s t r a t e type a s well a s sources and r a t e s of food supply. Thus, our charac- t e r i z a t i o n of t h e bay ' s ben th ic i n v e r t e b r a t e feed ing modes (Table 3 ) i s based on obse rva t i ons of l oca l popul a - t i o n s , h a b i t a t t y p e , and po t en t i a1 sources of food a s well a s on pub1 ished s t u d i e s of t he same spec i e s e l sewhere.

I t i s apparent from Table 3 t h a t , with t h e except ion of some polychae tes , the common s p e c i e s o f San Francisco Bay macro inver tebra tes a r e f i l t e r f eede r s o r sur face d e p o s i t f e ede r s ( i nc lud ing su r f ace g r a z e r s ) . Moreover, t h e group of spec i e s represen t ing t h e bulk of i n v e r t e b r a t e biomass-- the b iva lve mo l lu sks - - i s composed e n t i r e l y of f i l t e r f e e d e r s , a1 though Macoma bal t h i ca i s a s u r f a c e depos i t feeder a s well as a f i l t e r f eede r (Hummel 1985): Macoma feeding t r a c e s a r e nea r ly always prominent on t h e bay mudflat s u r - f ace s (F igure 20 ) .

While d e f i n i t i v e s t u d i e s have not been conducted, t h e most r e a d i l y apparent food sources f o r t h i s abundance of f i l t e r f eede r s and s u r f a c e d e p o s i t f e ede r s a r e probably phytoplankton and benth ic microalgae. Because t h e e s t u a r y i s s h a l - low and well mixed, phytoplankton in t he water column i s d i r e c t l y a v a i l a b l e t o f i l - t e r f eede r s on t h e bottom. Cloern (1982) concluded t h a t t he benthos l i m i t s t he s i z e of phytoplankton blooms in South Bay. Benthic graz ing may a l s o have been respon- s i b l e f o r t h e unusual ly low l e v e l s of

Table 3. Reported feeding modes of common soft-bottom macroinvertebrates found in San Francisco Bay.

Surface Subsurface Grazers, F i 1 t e r deposi t deposi t carnivores ,

Species feeders feeders feeders omnivores References

Asvchis elonqata C a ~ i t e l l g sp. Heteromastus f i l i f o r m i s Glvcind? sp. Mereis succinea Pol vdora spp.

Crustacea Amoel i s ca abdi t a Coro~hi urn spp. S~haeroma auovana

Mol I usca Corbicul a f l uminea Gema aemma I1 vanassa obsol e tq Geukeasia derni s sa Macoma bal t h i c a Muscul i s t a senhousia && arenaria T ~ D ~ s ~ h i 1 i D D ~ narum

Fauchald and Jumars 1979 I1

Mills 1967 Newell 1970 Rotramel 1972

Foe and Knight 198% Sellmer 1967

X Cur t i s and Hurd 1981 Kuenmler 1961 Wummel 1985 Morton 1976 Newel1 1470 Lanqton e t a l . 1977

Figure 20. Macoma balthica feeding traces, with the mudsnail llyanassa obsoleta for scale (photograph courtesy of D.R. Hopkins).

phy top lank ton i n Suisun Bay d u r i n g t n e 1976-77 d rough t (N icho l s 1985b). Fu r t he r , because approx imate ly 45% o f t h e bay's su r face area a t h i g h t i d e i s covered by l e s s than 2 m o f water , a depth e q u i v a l e n t t o t h e bay 's average p h o t i c depth, b e n t h i c m ic roa lgae a re a l s o a p o t e n t i a l ma jo r source o f food (Chapter 4 ) .

A r ecen t s t udy o f growth i n Macoma b a l t h i c a (Thompson and N i c h o l s i n p ress ) shows t h a t t h e t i m i n g and r a t e o f growth are r e l a t e d t o t h e t i m i n g and magnitude o f blooms i n e i t h e r t h e phy top l ank ton o r phytobenthos o r bo th (Sec t i on 3.1.2) . Most o f t h e o t h e r b e n t h i c i n v e r t e b r a t e spec ies found i n h i g h abundance, e.g., A m ~ e l i s c a abd i t a , S t r e b l o s p i o b e n e d i c t i , and Gemma semma, as w e l l as t h e l a r g e mol- l u s k s a rena r i a , Geukensia demissa, Myt iTus e d u l i s , M u s c u l i s t a senhousia, and T a ~ e s ghil i ooinarum, a7 so d i r e c t l y consume microalgae,. e i t h e r by f i 1 t e r i n g wa te r o r s e l e c t i v e l y f eed ing a t t h e sediment s u r - face. The mudsnai l Tlvanassa obso le ta , a su r face g razer , i s known t o feed d i r e c t l y

on b e n t h i c m ic roa lgae o r sedimented phy top lank ton as we71 as on l i v e an imals and c a r r i o n ( C u r t i s and Hurd 1981).

R ive r -borne o rgan i c d e t r i t u s , decay- i n g vascu la r p l a n t s and assoc i a t ed microbes and ep iphy tes washed f rom t h e marshes, wastes f rom sewage-treatment p l a n t s (Chapters 4 and 5 ) , and microbes and meiofauna l i v i n g i n bo t tom sediments a l s o c o n t r i b u t e t o t h e d i e t o f f i l t e r and depos i t feeders (Sec t i on 4 .2 ) . As y e t , however, we have no unders tand ing o f t h e i r q u a n t i t i e s , r a t e s o f supply , o r r e l a t i v e importance t o b e n t h i c f eed ing .

2.5.2 Ben th ic Food Web

There have been no s t u d i e s o f f ood web i n t e r a c t i o n s w i t h i n t h e San Franc isco Bay benthos. Nonetheless, ou r knowledge o f t h e behav io r o f i n d i v i d u a l spec ies (supplemented by s t u d i e s i n o t h e r es tua r i es ) i s s u f f i c i e n t t o desc r i be a p robab le food web o f t h e sha l l ow benthos o f t h e bay: m ic roa lgae growing b o t h i n t h e sha l low water column and on t h e sediment su r face ( w i t h cons i de rab le o v e r l a p between t h e two "communi t ies" ) , mixed and t r a n s p o r t e d across t h e i n t e r t i d a l o r s h a l - l ow s u b t i d a l m u d f l a t s by wind- and t i d e - induced c u r r e n t s , a re d i r e c t l y a v a i l a b l e t o suspension o r su r f ace d e p o s i t f eed ing i n v e r t e b r a t e s . Thus, t h e r e i s an immediate t r a n s f e r o f food energy f r om mic roa lgae t o i n v e r t e b r a t e s . The b e n t h i c i n v e r t e b r a t e s are, i n t u r n , eaten by such l a r g e consumers as shoreb i rds , demersal f i shes, e l asmobranchs, j u v e n i l e Dungeness crabs i n t h e n o r t h e r n reaches o f t h e bay (Sec t i on 3.3.3), and by human clam d i gge rs (Chapter 6 ) . T h i s s imple, e f f i c i e n t food web t h a t l i n k s m ic roa lgae d i r e c t l y w i t h clams w i t h o u t an i n t e r m e d i a t e p e l a g i c consumer 1 i n k - -much 1 i ke t h a t o f an aquacu l tu re system- -shou ld be app rop r i a t e f o r commercial she1 1 f i s h g row ing (Chapter 6 ) . Whether microbe-coated sediment p a r - t i c l e s a re an e q u a l l y o r more impo r t an t source o f n u t r i t i o n f o r t h e mud f l a t i n - h a b i t a n t s remains t o be determined.

CHAPTER 3. MACROFAUNAL COMMUNITY DYNAMICS

Estuar ine ben th i c spec i e s undergo Francisco Bay, t h e small and h ighly abun- marked changes in abundance over a v a r i e t y dant amph i pod Amoel i sca abdi t a of t ime s c a l e s (Nichols 1985a) . Most demonstrated yea r - t o -yea r cons is tency , changes a r e a s soc i a t ed with over a 10-year per iod , in t h e t iming of spec ies -spec i f i c seasonal p a t t e r n s of abundance f l u c t u a t i o n s , wi th peak abun- recru i tment , growth, and m o r t a l i t y . Other dance occur r ing in October of most y e a r s equa l ly important changes r e s u l t from pre- (F igure 22 ; Nichols and Thompson 1985a). d i c t a b l e o r unp red i c t ab l e changes i n t h e This cons is tency may r e f l e c t t he f a c t t h a t e s t u a r i n e h a b i t a t t h a t occur over time t h i s spec i e s has two gene ra t i ons each s c a l e s ranging from t i d a l cyc l e s t o y e a r s yea r - - a small overwin te r ing gene ra t i on (e .g . , responses t o t h e seasonal i t y of comprising juveni 1 e s and subadul t s t h a t r i v e r flow o r p r eda t i on , o r t o c1 imat ic mature i n s p r i n g , and a subsequent sp r ing events and t r e n d s ) . A few changes r e f l e c t genera t ion t h a t r a p i d l y matures and hi s t o r i c even t s t h a t permanently a1 t e r e d produces t h e summer-autumn gene ra t i on . communities, and s t i 11 o t h e r s r ep re sen t The overwinter ing i n d i v i d u a l s come from modern anthropogeni c i n f l uences (Chapter t h i s 1 a t t e r gene ra t i on (Mi 1 l s 1967; 5 ) . Kinnet ic Labora tor ies , Inc. 1983; Nichols

and Thompson 1985a) .

3.1 SEASONAL PATTERNS IN THE BENTHIC COMMUNITY The t iming of recru i tment of t h e

northern temperate b iva lve Macoma b a l t h i c a The r e s u l t s from benth ic surveys t h a t i s a l s o reasonably p r e d i c t a b l e . In San

include sampl ing a t f i xed s i t e s through Francisco Bay, r e c r u i tment occurs mostly time show t h a t abundances of ind iv idua l during two per iods each yea r : in l a t e spec ies vary widely between seasons and win te r t o e a r l y sp r ing and again in l a t e from year t o yea r ( e . g . , Figure 21 ) . summer t o e a r l y autumn (Nichols and

Thompson 1982), a1 though t h e re1 a t i ve importance of sp r ing and autumn recru i tment va r i e s from l o c a t i o n t o l o c a t i o n w i th in

3.2.1 Abundance Chanqes t h e bay (Thompson and Nichols unpubi. d a t a ) . In t h e absence of co ld w in t e r s

L i t t l e i s known about t h e mechanisms (Macoma i s more t y p i c a l l y found a t h igher t h a t t r i g g e r reproduct ive a c t i v i t y o r t h a t l a t i t u d e s ) , t empera ture may not be t h e a f f e c t recru i tment success in t h e bay's major s t imulus f o r reproduct ive develop- benthic spec i e s popula t ions . Nonetheless, ment in San Francisco Bay. The t iming of some of t h e mechanisms c o n t r i b u t i n g t o food a v a i l a b i l i t y ( a s s o c i a t e d wi th major abundance f l u c t u a t i o n s have been phytoplankton and phytobenthos blooms) i d e n t i f i e d i n q u a n t i t a t i v e surveys and i n a l s o may be an important f a c t o r in t h e s t u d i e s of reproduct ive a c t i v i t y and l i f e reproduct ive matura t ion cyc l e {Thompson hi s t o r y of severa l numerical l y prominent unpubl . ms. ) . spec ies (Nichols and Thompson 1985af . We know l i t t l e about t h e na tu ra l h i s t o r y o f Although t h e t iming of Macoma abun- spec ies o t h e r than t h e s e few. dance peaks a t one South Bay s tudy s i t e i s

somewhat p r e d i c t a b l e , t h e maximum s i z e of General ly , macrobenthic i n v e r t e b r a t e s t he populat ion dur ing any year i s not

a t temperate and h igher l a t i t u d e s i nc r ea se (Nichols and Thompson 1985a) : in some in abundance i n p a t t e r n s a s soc i a t ed with yea r s Macoma i s extremely abundant, whi le t he annual temperature c y c l e . In San in o t h e r s i t i s nea r ly absent (F igure 21) .

21

r---. -T--.-.-.

TOTALABUUDANCE

7" / - Copirulh~ rpp.

0 1. --- --r.:i*.- ... ., ...... - .-J ........

19/4 1975 l v / b 19li 1918 1979 1980 1981 1987 1983

- I l f ' P I R STATION - - - - - - MILIDLI STATION. . LOWER STATION

Figure 21. Abundance of the macrofauna collected in core samples at three stations on an intertidal mudflat at the Palo Alto study site (Figure 4), including three numerically dominant species (Gemma, Streblospia, Ampelisca), the species that accounts for the largest percentage of biomass (Macoma), and three irruptive species (Mya, Corophium, Capitella) (from Nichols and Thompson 1985a).

Figure 22. Abundance (average rtl s.d., 1974-76) of three numerically dominant mudflat species over a 10-year period (straight lines), and computed average annual cycles from least-squares regression of the data (curvisinear lines) (from Nichols and Thompson 1985b).

22

The l a rge yea r - t o -yea r d i f f e r e n c e s could r e s u l t from v a r i a b l e preda t ion on a d u l t s by b i r d s , r a y s , and f i s h e s ; v a r i a b l e predat ion on p lanktonic 1 arvae ; v a r i a t i o n in t h e number of l a r v a e in t h e water column ava i l ab l e f o r s e t t l i ng ; v a r i a t i o n s in t h e number of l a r v a e t h a t succes s fu l l y s e t t l e t o t h e sediment s u r f a c e ; o r i n t h e presence o r absence of p o t e n t i a l l y i n t e r - f e r i n g spec i e s once they have s e t t l e d (Sect ion 3 . 2 ) .

Abundance f l u c t u a t i o n s among o t h e r common bay i n v e r t e b r a t e s seem much more random. The t iming o f annual abundance peaks of two numerical l y dominant spec i e s , t he clam Gemma qemma and t h e polychaete S t r eb lo sp io benedic t i , i s h igh ly v a r i a b l e from year t o yea r (F igure 22; Nichols and Thompson 1985a).

The c l ima te of t h e §an Francisco Bay region, moderated by mild w in t e r s and by t he i n f l u x of c o l d e r , upwelled water from of fshore dur ing t he summer, maintains bay water temperatures wi th in a narrow range. Such a temperature regime may permit g r e a t l y increased reproduct ive f l ex i bi 1 i t y in some spec i e s . Gemma and S t r eb lo so io , l i k e Amoelisca, a r e brooders , but t h e i r females. remain reproduct ive ly a c t i v e during much of t h e yea r (Jones 1961; Thompson 1982; Nichols and Thompson 1985a). Addi t iona l ly , s t r ong water mixing within and between embayments probably con t r i bu t e s t o bay-wide d i s p e r s a l o f water-borne 1 a rvae , juveni 1 e s , and a d u l t s of t he se small spec i e s . T h u s , t h e poten- t i a l f o r r ap id co lon i za t i on of a v a i l a b l e s u b s t r a t e s throughout much of t he yea r i s g r e a t l y enhanced (Nichol s and Thompson 1985a). Successful r ec ru i tmen t , nonethe- l e s s , may depend on l oca l cond i t i ons (physical condi t ions a t sediment su r f ace , presence of compet i to rs o r p r eda to r s , e t c . ) a t t h e time of l a r v a l r e l e a s e .

All of t h e s e f a c t o r s ( tempera ture , water col umn mixing, sediment c h a r a c t e r , p reda t ion , spec i e s i n t e r f e r e n c e ) t oge the r undoubtedly c o n t r i b u t e t o extreme y e a r - t o - year v a r i a b i l i t y observed i n t he t iming of popul a t i on i nc r ea se s , and render s h o r t - term assessments of community s t r u c t u r e f o r t he purpose of environmental q u a l i t y analysi s f Chapter 5) re1 a t i ve ly use1 e s s .

3.1.2 Seasonal Growth

F ie ld and experimental s t u d i e s worldwide have shown t h a t r a t e of growth

in benth ic i n v e r t e b r a t e s a l s o v a r i e s markedly with t ime. Many s t u d i e s (reviewed in Nichols and Thompson 1982) have shown t h a t t h e clam Macoma b a l t h i c a t y p i c a l l y grows most r ap id ly during a b r i e f per iod i n sp r ing , t y p i c a l l y in a s - soc i a t i on with a temperature-dependent seasonal cyc le of reproduct ive development (de Wilde 1975) and t h e a v a i l a b i l i t y of food (Beukema e t a l . 1977; Chris tensen and Kanneworff 1985). Although Macoma in San Francisco Bay grows t o some degree throughout t h e year , most of t he growth in South Bay popula t ions t a k e s p lace dur ing a b r i e f per iod i n sp r ing (F igure 23) c o i n c i - dent with t h e sp r ing phytoplankton and benth ic microalgal blooms (Nichol s and Thompson 1982, 1985b). Growth r a t e s a r e a l s o higher i n San Francisco Bay than in any o the r 1 o c a t i on, worldwide, apparen t ly because of t h e warmer water temperature (Nichol s and Thompson 1982).

Growth i n bay popula t ions of t h e amphipod A m ~ e l i s c a a b d i t a , t h e clam Gemma qemma, t h e isopod Sphaeroma auoyana, t h e mussel Geukensi a demi s s a , t h e sna i 1 Ceri t h idea ca l i f o rn i ca , and t he f reshwater clam Corbicula fluminea i s a l s o s t r o n g l y focused i n sp r ing o r summer (Schneider 1976; Langlois 1980; Race 1981; Thompson 1982; Kinne t ic Labora tor ies , Inc. 1983; Foe and Knight 1985a) .

Figure 23. Average length of itldividuais in two year classes (recmited in 1979, 1980) of Macoma balfkrica (from Nichals and Thompson 1985b).

A more r ecen t s t udy , i n which growth of Macoma bal t h i c a was examined experimen- t a l l y a t f o u r d i f f e r e n t l o c a t i o n s in San Francisco Bay, has confirmed t h e e x i s t e n c e of a s t rong l i n k between maximum clam growth and seasonal peaks i n microalgal biomass. Furthermore, t h e t iming of microalgal -biomass and c l am-growth peaks var ied depending on l o c a t i o n wi th in t h e bay (Thompson and Nichols in p r e s s ) .

3.1.3 Seasonal Preda t ion

The e f f e c t s o f p reda t ion by r ep re - s e n t a t i v e s of o t h e r groups ( e . g . , b i r d s , f i s h , c r abs , e t c . ) on seasonal d i s t r i b u - t i o n and abundance p a t t e r n s have been demonstrated exper imenta l ly in many s t u d i e s around t h e world ( e . g . , Peterson and Peterson 1979; Baird e t a1 . 1985). However, wi th t h e except ion of Recher9s (1966) s tudy of shoreb i rd d i s t r i b u t i o n s and stomach con t en t s a t one i n t e r t i d a l s i t e i n South Bay (Table 2 ) , l i t t l e quan- t i t a t i v e information e x i s t s on t h e d i s t r i b u t i o n , abundance, and feeding behavior of l a r g e p r eda to r s from which seasonal e s t i m a t e s of p reda t ion l o s s e s could be made. S i m i l a r l y , on ly one s tudy of i n v e r t e b r a t e p r eda to r s has been conducted in $an Francisco Bay. In t h a t study Race (1982) found t h a t t h e i n t r o - duced sna i 1 I1 vanassa obso l e t a compet i t ive ly d i sp l aced t h e n a t i v e s n a i l Cer i th idea c a l i f o r n i c a from i t s p r e f e r r ed summer h a b i t a t and preyed upon i t s eggs .

The d i s t r i b u t i o n s of some p reda to r s a r e s t r o n g l y seasonal and, a s a r e s u l t , should c o n t r i b u t e t o seasonal p a t t e r n s i n i nve r t eb ra t e abundance. As exampl e s , migratory sho reb i rd s t h a t feed on many of t he common i n t e r t i d a l mudfl a t inver - t e b r a t e s a r e more abundant dur ing t h e autumn and w in t e r months (Recher 1966), while t he ba t r ay Myl ioba t i s c a l i f o r n i c a i s most p r eva l en t dur ing summer (Aplin 1967). A long-term baywide s tudy of f i s h d i s t r i b u t i o n s and stomach con t en t s , now i n i t s s i x t h yea r (Armor and Herrgese l l 1985), should begin t o provide p e r t i n e n t information on s p a t i a l and temporal pa t - t e r n s of feed ing on t h e benthos by f i s h and elasmobranch p reda to r s and on spec i e s - s p e c i f i c food p re f e r ences .

3.2 APERfODIC PATTERNS OF ABUNDANCE

The absence o f p r e d i c t a b l e p a t t e r n s in t h e abundance of many benth ic i nve r -

t e b r a t e s of t h e bay and t h e r a p i d i t y of community changes suggest t h a t s t o c h a s t i c processes c o n t r i b u t e markedly t o observed v a r i a b i l i t y .

3.2.1 E f f ec t s o f Environmental - Per tu rba t i ons

The 10-year s tudy of an i n t e r t i d a l ben th ic community i n South Bay (Sec t ion 3 .1 .1) revea led r ap id changes in i n - d iv idua l s p e c i e s abundances (F igure 21 ) t h a t , with r e s p e c t t o our understanding of spec ies l i f e h i s t o r i e s , a r e l a r g e l y unpre- d i c t a b l e . While t h e f a c t o r s con t r i bu t i ng t o t he se changes seldom a r e c l e a r l y under- s tood , pe r iod i c o r ape r iod i c d i s t u rbances of t h e environment a r e imp1 i c a t e d (Nichol s and Thompson 1985a, b) . As an example, t h e annual d e c l i n e i n Amuel i s c a during autumn and win te r a t any s i t e i s assumed t o be t h e r e s u l t o f na tu r a l autumn-winter mor- t a l i t y f o l 1 owing reproduct ion . Several da t a s e t s , however, sugges t a connect ion between observed rap id decl i n e s and inun- da t ion by l o w - s a l i n i t y s u r f a c e water and t he p o s s i b i l i t y of mass migrat ion of animals away from inundated s i t e s t o more s a l i n e , deeper o r down-estuary reg ions of t he bay (Nichols and Thompson 1985b).

S imi l a r l y , many of t h e most dramatic between-year community changes may be a t - t r i b u t a b l e t o extreme dev i a t i ons in t h e physicochemical environment from 1 ong-term norms t h a t , in turn, may in f luence t h e timing and success of recru i tment of new ind iv idua l s t o t h e community o r t h e s u r - vival of i nd iv idua l s a l r eady e s t a b l i s h e d . Interannual v a r i a t i o n s in r i v e r flow i n t o t h e e s t u a r y have a p a r t i c u l a r l y s t rong e f - f e c t . Extremely low r i v e r inf low from t h e Sacramento-San Joaquin River system during two success ive w in t e r s (1976 and 1977) r e su l t ed i n s t e a d i l y i nc r ea s ing s a l i n i t y and an i nc r ea se i n both spec i e s d i v e r s i t y and abundance i n Suisun Bay a t t h e upper end of t h e e s t u a r y (F igure 2 4 ) . I t i s a s - sumed t h a t l a r v a e and j uven i l e s of e s t u a r i n e benth ic spec i e s normally found only downstream o f Carquinez S t r a i t (Figure 4 ) were c a r r i e d upstream t o Suisun Bay by g r a v i t a t i o n a l c i rcuf a t ion and t i d a l cu r r en t s . The temporar i ly en1 arged ben- t h i c community (F igure 2 5 ) , comprising severa l f i l t e r f e e d e r s , may have con- t r i b u t e d t o t h e equa l l y unusual d e c i i n e i n phytoplankton biomass i n Suisun Bay a t t h e same time (Nichols 1985b). The r e tu rn of normal r i v e r f low and reduced s a l i n i t y a t

I Number

Figure 24. Salinity, mean number of macrofauna species, and mean number of individuals at a shallow site (Figure 4, site D7) in Suisun Bay (adapted from Nichols 1985b); data from California Department of Water Resources 1986.

t he end of 1977 qu i ck ly e l im ina t ed t he se t r a n s i e n t spec i e s popula t ions from Suisun Bay (F igure 24) .

A t t h e oppos i t e extreme, high r i v e r inflow "even t s , " such a s occurred during t he w in t e r and sp r ing o f 1982 and again i n 1983, cause a r ap id lowering of s a l i n i t y throughout t h e bay. Inundat ion by brack- i sh o r f reshwater dur ing t he se events resui t ed i n a decl ine of abundance wi th in the i n t e r t i d a l ben th i c community and t he near -e l imi n a t i on of t h e amphi pod Ampel i sca abdi t a (F igure 26 ) . Two yea r s passed f o l - lowing t h e 1982 per iod of high r i v e r inflow before Amoel i s c a rega ined i t s numerical prominence (Nichols and Thompson 1985a). The Japanese 1 i t t l eneck clam T a ~ e s phi1 ippinarum a1 so decl ined i n 1982 and again in 1986 fo l lowing unusual ly heavy r a i n f a l l and runof f and t h e subsequent s i l t a t i o n of clam beds (T.O. Moore, J r . , Cal i f o r n i a Department o f Fish and Game; pers . comm.). Coincident with t he inundation by 1 ow-sal i n i t y water during t h e w in t e r of 1982 was t he depos i - t i 0 5 c f f i n e t e r r i g e n o u s mud over t h e i n t e r t i d a l mudfl a t s throughout t h e bay (and probably t h e s u b t i d a l a s w e l l ) and t h i c k l a y e r s (up t o 15 cmf of sand on top

Figure 25. Average abundance of numerically abundant species at sites 136 (dashed Iine) and D7 in Suisun Bay (Figure 4); data as in Figure 24 above (adapted from Nichols 1985bf; no data between late 1973 and late 1975 (stippled area).

Figure 26. Average dailyflow of freshwater into San Francisco Bay from the Sacramento and San Joaquin Rivers (A) and abundance of two species at the Palo Alto intertidal mudflat study site (B, C; from Nichols and Thompson 1985b).

of t h e mudflat a t t h e mouths of l oca l s t reams. I t i s not c l e a r , in any i n - s tance , whether observed d e c l i n e s a r e r e l a t e d more t o r ap id sed imenta t ion , t o reduced s a l i n i t y , o r t o some o t h e r r e l a t e d f a c t o r ( s ) .

Epi sodes of unusual l y s t rong s u r f a c e sediment e ro s ion can a l s o a f f e c t abundance by sub j ec t i ng t h e small sur face-dwel l ing i n v e r t e b r a t e s t o physical removal o r b u r i a l . As an extreme example, approximately 8 cm of sediment was removed from a South Bay mudfl a t between observa- t i o n s separa ted by one month dur ing f a l l 1974 (Nichols and Thompson 1985a) . The occasional accumul a t i on and subsequent decomposition of macroal gal mats can a1 so a f f e c t t he ben th i c community. Again as an extreme example, a t h i c k accumulation of t he macroalga Polvsiahonia covered t h e upper i n t e r t i d a l zone of a South Bay s tudy s i t e during summer of 1975, smothering t h e organisms i n t h e sediments . Recolonizat ion of t h e s i t e r equ i r ed weeks t o y e a r s , depending on t h e a v a i l a b i l i t y and moti l i t.y of co loniz ing i n d i v i d u a l s , and seemed t o involve migra t ing a d u l t s a s well a s j uven i l e s (Nichols and Thompson 1985a) .

3 . 2 . 2 Imaortance of Benthic Spec ies I n t e r a c t i o n s

unknown number of s i bl ing s p e c i e s ; Grassl e and Grass le 1976; h e r e a f t e r r e f e r r e d t o a s C a ~ i t e l l a spp.) appeared about 6 months a f t e r t h e macroalgal accumul a t i on -and - decay event de sc r ibed above, but before t h e normal l y r e s i d e n t s p e c i e s had become f u l l y r e e s t a b l i s h e d . The C a a i t e l l a group conta ins s p e c i e s t h a t a r e well known ex - p lo i t e r s of o r g a n i c a l l y enriched o r otherwise d i s t u rbed environments (Grassl e and Grass le 1974, 1976; Nichols and Thompson 1985a) . The avai 1 abi 1 i t y of decaying organic ma t t e r , coupled with an absence of compet i to rs , may have con- t r i buted t o i t s temporary succes s .

Most o t h e r occasional spec i e s i r r u p - t i o n s , such a s t h a t of a r e n a r i a i n 1975 (F igure 21 ) , a r e not understood, a l - though some exp l ana t i ons can be hypothesized. Several d a t a s e t s , f o r example, show t h a t Macoma b a l t h i c a , sometimes absent f o r s eve ra l y e a r s a t a t ime, becomes abundant only when i t s l a rvae can s e t t l e in t h e r e l a t i v e absence of t he introduced amphi pod Ampel i s c a &- dita (F igure 26 ) . This f i nd ing sugges ts t h a t Macoma abundance may be cont ro l l e d l o c a l l y by t he presence of a l a r g e popula- t i o n of Ampelisca e i t h e r by d i r e c t consumption of s e t t l i n g clam l a r v a e o r t h e physical d i s r u p t i o n of l a r v a l s e t t l emen t (Ni chol s and Thompson 1985a) .

Other ape r iod i c changes may be mani f e s t a t i o n s o f spec i e s i n t e r a c t ions . 3.3 LONG-TERM TRENDS Some spec i e s common t o t h e bay benth ic community, such a s t h e c l ams Macoma ba l - The most pronounced change t h a t has t h i c a and MJGJ a r e n a r i a and t h e polychaete a f f ec t ed t h e benth ic community of San C a ~ i t e ? l a , dispf ay abundance p a t t e r n s t h a t Francisco Bay during t h e p a s t 140 yea r s a r e markedly d i scont inuous with time was t he i n t roduc t ion of spec i e s (Sec t ion (F igure 2 1 ) . Capi te l l a (commonly c a l l e d 2 . 3 ) . However, because q u a n t i t a t i v e C . c a p i t a t a , but a c t u a l l y comprising an s t u d i e s of t he benthos were not undertaken -

until the 195B's, well after the period of most introductions, it i s not possible to compare pre- and post-introduction benthic communi ties.

There is no indication from pub1 ished reports that there have been significant long-term changes in benthic community composition during the three decades since quantitative studies began, although such changes have undoubtedly occurred in the immediate vicinity of waste outfalls (as a result of changed salinity regime as well as the effect o f the waste flow itself;

Chapter 5). The absence of observable long-term changes at all other locations may be due, in part, to inconsistencies among the surveys in sampl i ng 1 ocation and time of year, sampl ing method01 ogy, species identification, data interpreta- tion, and discontinuous sampling through time within embayments (Nichols 1973). Qualitatively, the same common species names appear in all published species 1 ists for each area. Only consistent, long-term, bay-wide monitoring will allow us to detect the existence or lack of signi f i cant trends.

CHAPTER 4. CYCLING OF MATTER IN THE BENTHOS

4.1 INTRODUCTION

Ben th i c b i o l o g i c a l processes a r e i n - vo lved i n t h e p roduc t i on , supply , t rans fo rmat ion , and m i n e r a l i z a t i o n o f o r - gan ic m a t t e r i n e s t u a r i e s . To eva lua te t h e b i o l o g i c a l p r o d u c t i v i t y o f t h e b e n t h i c community and i t s r e l a t i o n t o f i s h e r y y i e l d , f o r example, we must have knowledge of many processes t h a t de te rmine t h e f a t e of o rgan ic m a t t e r as i t c y c l e s th rough t h e ecosystem. Reproduct ion, r ec ru i tmen t , growth, and m o r t a l i t y i n b e n t h i c macrofaunal p o p u l a t i o n s (Chapter 3 ) a re b u t a few o f many b i o l o g i c a l processes t h a t con- t r i b u t e t o biogeochemical c y c l e s . Pr imary p roduc t ion , ae rob i c and anaerobic r e s p i r a - t i o n , chemosynthesi s ( = chemoautotrophy) , and f e rmen ta t i on - - processes assoc i a t ed w i t h algae, b a c t e r i a , f u n g i , protozoans, and meiofauna - - a l s o c o n t r i b u t e t o t h e t u rnove r o f o rgan i c m a t t e r i n sediments. Other processes i n c l u d i n g sedimentat ion, g raz ing , f i l t e r feed ing , d e p o s i t feed ing , p reda t i on o f b e n t h i c i n v e r t e b r a t e s by f i s h and m i g r a t o r y b i r d s , ae rob i c and anaerobic m inera l i z a t i o n o f a1 1 k i nds o f o rgan i c ma t t e r , and t r a n s p o r t o f resuspended m a t e r i a l a l l c o n t r i b u t e t o t h e c y c l i n g o f o rgan i c m a t t e r between t h e sediment and water column. I n t h i s chap te r we cons i de r some o f t h e processes t h a t govern t h e cy - c l i n g o f m a t t e r i n t h e benthos.

4-2 SOURCES OF ORGANIC MATTER

The ma jo r sources o f o rgan i c m a t t e r t o t h e benthos a r e presumed t o be t h e same as t o t h e e s t u a r y i t s e l f : ( 1 f p l a n t m a t e r i a l (a lgae and vascu? a r p l a n t s j produced w i t h i n t h e es tuary , (2) 1 i v i n g p l a n t m a t e r i a1 and dead p a r t i cu1 a t e m a t e r i a l ( d e t r i t u s ) suspended i n t h e r i v e r

water and su r f ace r u n o f f t h a t f l o w i n t o t he es tuary , (3 ) d i s s o l v e d o rgan i c ma t t e r from a l l sources, and ( 4 ) sewage f rom waste- t reatment p l a n t s .

4.2.1 Vascular P l an t s

The marshes o f San Franc isco Bay and De l ta , because o f t h e i r g r e a t l y reduced s i z e f o l l o w i n g more than 130 years o f rec lamat ion , a r e p robab ly o n l y a m inor source o f o rgan i c m a t t e r f o r t h e nonmarsh benthos o f t h e bay. A twate r e t a l . (1979) est imated t h a t p r o d u c t i o n o f d r y vascu la r p l a n t m a t e r i a l i n t h e bay's t i d a l marshes i s about 1 x 105 t ons p e r y e a r . However, t h e amount o f o rgan i c m a t t e r washed i n t o t he bay f rom those marshes may be o n l y about 5% o f t h e amount produced by phy top lank ton i n bay wate r (A twate r e t a l . 1979).

Eelgrass, Zos te ra mar ina, i s a l s o found i n San Franc isco Bay, b u t i s ap- p a r e n t l y l i m i t e d t o t h e Cen t ra l Bay r e g i o n where s a l i n i t y i s h i g h e s t (U.S. F i s h and Wild1 i f e Se rv i ce and C a l i f o r n i a Department o f F i s h and Game 1979). Eelgrass beds wor ldwide form complex h a b i t a t s f o r as - soc i a t ed fauna and f l o r a and i n f l u e n c e t h e ben th i c community by s t a b i l i z i n g sediment, p r o v i d i n g s u b s t r a t e f o r ep iphy tes , produc- i n g o rgan i c ma t t e r , e x p o r t i n g d e t r i t u s , and a t t r a c t i n g p reda to r s such as crabs, shrimp, and skates (e.g., P h i l l i p s 1984). The disappearance o f ee l g rass f rom an a rea leads t o ex tens i ve changes i n sediment g r a i n s i z e , wa te r chem is t r y , c i r c u l a t i o n p a t t e r n s and tu rbu lence , and spec ies com- p o s i t i o n (Thayer e t a l . 1984). Nonetheless, s c i e n t i f i c s tudy o f San Franc isco Bay ee l g rass beds has been m i n i - mal s i nce t h e e a r l y s t u d i e s by S e t c h e l l (1929). Other t han a e r i a l observa t ions o f

t h e i r d i s t r i b u t i o n (U.S. Fish and Wi ld l i f e Service and Cal i f o r n i a Department of Fish and Game 1979), 1 i t t l e i s known about t h e s i z e of ind iv idua l beds, t o t a l s tanding s tock , seasonal and long-term f l uctua- t i o n s , e e l g r a s s bed fauna , and t h e q u a n t i t a t i v e c o n t r i b u t i o n of e e l g r a s s t o t he organic ma t t e r budget o f t he e s t u a r y . Recently, however, an ee l g r a s s t r a n s p l a n t p ro j ec t used in m i t i g a t i o n f o r t he l o s s of a bed dur ing a U.S. Army Corps of Engineers seawall r e p a i r p r o j e c t ( F r e d e t t e unpubl . ) has s t imu la t ed renewed i n t e r e s t in bay e e l g r a s s beds both with r e spec t t o mapping t h e i r d i s t r i b u t i o n and s tudying t h e i r ecology (S. Wyll i e Echeverri a , Cal i f o r n i a S t a t e Un ive r s i t y a t San Francisco; pe r s . comm. ) .

4.2.2 Benthic Macroalqae

There a r e , a t p r e sen t , 162 spec i e s of macroal gae known t o ex i s t i n San Francisco Bay ( Josse lyn and West 1985). The most widely d i s t r i b u t e d s p e c i e s a r e t h e green a lgae Enteromorwha c l a t h r a t a , E . i n t e s - t i n a l i s , E. l i n z a , Ulva anqus ta , l a c tuca , Cl adowhora s e r i c e a , and two red a lgae , Pol vsiphonia denudata and Anti thamnion kvl i n i i . Macroalgae a r e most commonly found growing i n hard bottom a rea s ( rock ou t c rops , coa r se sediments , and human-made s t r u c t u r e s ) i n t h e c e n t r a l and northern reg ions of t h e e s tua ry ( Josse lyn and West 1985). In summer, d r i f t i n g macroal gae (detached from growing su r f ace s ) occas iona l l y accumulate i n t h i c k mats in t h e i n t e r t i d a l zone (Nichols 1979; Josselyn and West 1985). The i r occurrence i s genera1 l y viewed, because of t h e i r smelly decay, a s a p u b l i c nuisance r a t h e r than as important product ion o f o rganic mat te r . Consequently, t h e main t h r u s t of research has been d i c t a t e d by t h e d e s i r e t o cont ro l nuisance blooms t h a t occur in some yea r s ( Jo s se lyn 1984; Josse lyn and West 1985). We do not know what t r i g g e r s t he se l oca l i z ed , ep i sod i c blooms of d r i f t macroalgae, nor do we know how much i s produced i n s i t u and how much accumulates by physical t r a n s p o r t and mixing processes .

Macroalgae a r e recognized as an impor tan t source of t he bay's o rganic mat te r , but t h e i r t o t a l con t r i bu t i on t o benthic primary product ion has not been assessed . Thus, t he importance of macroalgae as a source of food f o r benth ic

organisms of t h e bay i s a l s o l i t t l e under- s tood. The 1 a rge ly d e s c r i p t i v e ( S i l va 1979; Josse lyn and West 1985) and physiological (She1 lem and Josse lyn 1982) s t u d i e s of t h e bay 's macroalgae need t o be supplemented by f i e l d measurements t o ob- t a i n t h e necessary s p a t i a l and temporal e s t ima te s of na tu ra l product ion.

4 .2 .3 Phytoplankton

Phytoplankton abundances i n t h e bay a r e c o n t r o l l e d l a r g e l y by 1 i g h t ava i l ab i 1 i t y and v e r t i c a l mixing processes t h a t r e s u l t i n a sp r ing bloom i n South Bay and a summer bloom in Sui sun Bay (F igure 2 7 ) . Annual n e t product ion of phytoplankton in t h e p h o t i c zone v a r i e s from 95 t o 150 g C/m2 and i s h ighes t in South Bay where t u r b i d i t y i s lowes t , a l - though biomass i s h ighes t i n t h e entrapment o r nul l zone of Suisun Bay (Cloern e t a l . 1983; Cole and Cloern 1984). Resu l t s from severa l s t u d i e s (Cloern 1982; Hammond e t a l . 1985) suggest t h a t much of t h e phytoplankton produced in t h e water column s e t t l e s t o t h e bottom, where i t i s consumed by a v a r i e t y of o r - ganisms from b a c t e r i a t o 1 arge clams and worms.

Light and n u t r i e n t s (from t h e r i v e r s , waste- t reatment p l a n t s , and w i th in - e s tua ry r emine ra l i z a t i on ) a r e s u f f i c i e n t t o sup- p o r t much l a r g e r blooms o f phytoplankton than a r e t y p i c a l l y observed. Therefore , we might expect t h e occurrence of nuisance blooms of a lgae t h a t could d e p l e t e t h e oxygen supply in t h e water and kif l p lanktonic and benth ic animals . The l a c k of such nuisance b1 ooms i n San Francisco Bay has been a t t r i b u t e d , a t l e a s t in p a r t , t o benth ic graz ing (Sec t ion 2.5.1; Cloern 1982; Nichols e t a1 . 1986).

The coas t a l ocean i s a l s o a source of n u t r i e n t s f o r San Francisco Bay, pa r - t i c u l a r l y dur ing t h e summer upwell ing season (Conomos e t a1 . 1985). But, t o what degree t h e coas t a l ocean i s a source of plankton-derived o rgan i c ma t t e r i s unknown, a1 though n e r i t i c ( coas t a l ocean) diatoms a r e common i n t h e c e n t r a l p a r t of t h e bay (Cloern e t a l . 1985). Wolff (1977) showed t h a t o rgan i c d e t r i t u s from t h e coas ta l s e a was an important source of food f o r t he benthos of t h e Grcvel ingen Estuary (The Netherlands) before i t was converted t o a lake .

Figure 27. Contours of near-surface phytoplankton biomass (measured as chlorophyll) in San Francisco Bay on three occasians in 1980 (from Cloern et a!. 1985).

4 . 2 . 4 Benthic Bac te r ia and Microalsae

The primary producers on e s t u a r i n e sediments (excluding marshes, macroalgae, and s eag ra s s beds) a r e photosynthe t ic bac- t e r i a , diatoms, and bl uegreen a lgae (cyanobac te r ia ) . Photosynthe t ic b a c t e r i a , which produce s u l f u r r a t h e r than t he e a s i l y measured oxygen, occur under condi- t i o n s of anoxia e i t h e r in sediment o r in water , where both hydrogen s u l f i d e and l i g h t a r e p r e sen t . These b a c t e r i a can be a major primary producer i n s t r a t i f i e d br iny lakes and ponds which, because they do not mix v e r t i c a l l y , become anoxic a t some depth wi th in t h e pho t i c zone (Fenchel and Bl ackburn 1979). Carpel an (1957) noted t he presence of s u l f u r bac t e r f a in South Bay s a l t - evapo ra t i ng ponds. However, because t h e water in t h e s a l t ponds is not discharged i n t o t he bay, these b a c t e r i a a r e probably not a s i g - n i f i c a n t source o f o rganic ma t t e r f o r t h e bay.

L i t t l e q u a n t i t a t i v e information i s ava i l ab l e about t h e con t r i bu t i on o f microalgae (diatoms) t o t h e organic mat te r budget of t h e bay benthos. Recent s t u d i e s sugges t , none the less , t h a t ben th ic diatoms growing on t h e sediment s t i r facc thl-otighout

t he bay, t o g e t h e r with temporar i ly o r per - manently s e t t l e d phytoplankton, may represen t t h e most r e a d i l y avai 1 ab l e food resource f o r bottom organisms in t h i s shallow e s tua ry (Nichols and Thompson 1985a; s ee a l s o Chris tensen and Kanneworff 1985 f o r a p e r t i n e n t s tudy e l sewhere) . A 1-year survey of t he d i s t r i b u t i o n of ben- t h i c chlorophyll in bay sediments showed h ighes t l e v e l s of microalgal biomass (up t o 300 mg/m2 chlorophyll 3 a t some s t a t i o n s ) in t h e southernmost and nor th- ernmost ends of t h e bay, and t h e lowest l e v e l s (20 mg/m2) both i n San Pablo Bay (F igure 28) and i n t he deeper chan- ne l s . Limited by 1 i gh t a v a i l a b i l i t y , chlorophyll reaches higher concen t r a t i ons in i n t e r t i d a l and shallow sub t ida l ( l e s s than 5 m deep) sediments than in deep water sediments ( e . g . , 170 mg/m versus 50 mg/mz in Suisun Bay; Thompson e t a l . 1981).

Seasonal p a t t e r n s in benth ic p l an t biomass var ied from embayment t o embayrnent depending on 1 i g h t l e v e l s which a r e con- t r o l l e d by t h e t u r b i d i t y of inflowing freshwater and t h e t i d e - and wind-induced resuspension of s u r f i c i a l sediments (Nichols and Thompson 1985b). For example, maximum biomass i n South Bay was found in sp r ing , approximately co inc ident with t he phytoplankton bloom. The timing

Chlorophyll 5

200 1 , I - - Suisun Bay I/ f --- northern

South Bay

, - - San Pablo Bay E . ' - southern

South Bay

O M A M J J A S O N D J F

Figure 28. Average chlorophyll concentration in surface sediments at sites less than 5-m water depth; data from same stations as sediment data shown in Figure 10.

of the bloom coincided with the annual peak in so la r radia t ion a t low t i d e . Increased suspended sediment concentra- t ions , coincident with peak wind veloci t ies in May and June and peak t i d a l ve loc i t i e s in June and July a t the time of maximum s o l a r i r radiance (Figure 29), may 1 imit benthic microalgal biomass during l a t e spring and summer.

Maximum benthic chlorophyll biomass in Suisun Bay was not observed unt i l l a t e October. The Suisun Bay benthic diatom bloom consisted primarily of Thalassiosira d e c i ~ i e n s ( R . Laws, Univ. North Carolina; pers. comm.), the same species responsible for the major phytoplankton bloom in Suisun Bay during the previous month (Cloern e t a1 . 1985). This species has high sinking r a t e s (1.5 t o 6 m per day; Ball and Arthur 1981) and apparently resides a l t e r n a t e l y in the water column and in sediments depending on the degree of water-column mixing (Cloern e t a1 . 1985; Nichols and Thompson 1985b). The diatom c e l l s apparently s e t t l e t o the bottom following the autumn plankton bloom during a period of low r i v e r inflow and reduced t i d a l current and wind v e l o c i t i e s (Figure 29a, b; Nichol s and Thompson 1985a) .

I r T T' - r - 1-7 1

4 50 - i Maximum Ebb Velocity 4 in -

Figure 29. (A) Daily maximum ebb tidal velocity at the Golden Gate, (B) average monthly wind velocity at San Francisco International Airport located just south of the city of San Francisco, and (C) average monthly instantaneous irradiance at the time of low tide (from Nichols and Thompson 1985b).

the deeper water of Central and South Bays, where species t o l e r a n t of higher s a l i n i t y ( e - g . , Para1 i a sulcata and D i t v l um briahtwell i i ) were found (Laws 1983). The highest d i v e r s i t y among ben- t h i c diatom communities in San Francisco Bay was found in the sediments of the shallow margins of South Bay where there i s no major freshwater source. This a s - sembl age was dominated by es tua r ine benthic species ( e .g . , Nitzschia acuminata and &. p u s i l l a ) . Preliminary analysis of species d i s t r i b u t i o n s over one year showed t h a t species composition changes seasonally, pa r t ly because seasonally varying winds and t i d e s resuspend and mix sedimentary mater ia l , and thus influence the mix of benthic and planktonic forms found in the benthic diatom assemblage (Laws, unpubl . ) .

4.2.5 Mi croal qal Production

Elsewhere in the bay, the species Existing measurements of chlorophyll composition of benthic diatom communities concentration in surface sediments have varied with s a l i n i t y and water depth (Laws not been accompanied by systematic 1983, pers. comm. ) . Species d ive r s i ty in - measurements of benthic primary produc- creased with increasing sa l i n i t y toward t i o n , despi te the r e s u l t s from many

studies worldwide (reviewed by Parsons e t a l . 1984) t ha t demonstrate the importance of such measurements t o an understanding of net community production. The progres- sive buildup of diatom mats on in te r t ida l f l a t s of San Francisco Bay during l a t e winter and ear ly spring i s evidence of i t s potential importance here as well.

Because of the shallowness and per i - odic inflow and outflow of water, plankton production over an in te r t ida l zone may be small r e l a t i ve t o benthic production under both c lea r water (Pamatmat 1968) and tur- bid water (Hargrave e t a l . 1983). Furthermore, since the phytopl ankton present in the water column can cons i s t , in par t , of benthic diatoms t ha t are resuspended by waves and t i da l currents , the d i s t inc t ion between planktonic and benthic primary production in a shallow estuary can be an a r t i f i c i a l one.

To properly assess the r e l a t i ve importance of phytoplankton and benthic microalgae in San Francisco Bay, where the photic zone extends t o the bottom in a large b u t unknown f rac t ion of the to ta l area, the measurements of primary produc- t i v i t y will have t o be conducted from the in te r t ida l zone t o the midbay channels within each embayment. Understanding the quant i ta t ive re1 ation between natural l i gh t and benthic primary production in San Francisco Bay, where waves and t ida l currents repeatedly blur the boundary between benthos and water column, will be c r i t i c a l t o such investigations. One broad question concerns the e f fec t s of wind-generated sediment resuspension ( a dai ly occurrence in the summer) on photosynthetic r a t e s on the bottom as well as in the water column. Light transparency and the amount of l i gh t reaching the bottom are reduced during periods of resuspension, tending t o diminish benthic production. The loss of production on the bottom may, however, be compensated by the enhanced growth of "benthic" diatoms white they are suspended i n the water column. I f the diatoms grow a t l eas t as f a s t in suspension as on the bottom, and then s e t t l e t o the bottom during slack t i de s or windless periods, organic matter supply t o the bottom i s not impaired by sediment resuspension and tur- bidi ty . Even so, the r e l a t i ve importance of the benthos and the plankton as grazers would have t o be evaluated.

4 . 2 - 6 Other Sources of Orqanic Matter La the Benthos

Other sources of organic matter t ha t are potent ia l ly important t o the benthos, b u t tha t are poorly studied t o date , in- cl ude dissolved organic matter and de t r i tus . The input r a t e s and character of dissolved organic matter entering the bay are unknown. And, other than qua l i t a - t i ve descriptions of river-borne de t r i t u s (e .g . , Knight e t a l . 1980), information about the amounts and ro le of de t r i t u s (and i t s associated microbi a1 community) i s also very l imited. Further, no measurements of the supply of par t i cu la te organics t o the bottom, nor estimates of the r e l a t i ve importance of the two major sources of organic materi a1 s ( in ternal and external ) have been made.

4.3 RATE OF ORGANIC MATTER SUPPLY

Below the photic zone, the benthos i s dependent on the supply of organic matter from above, including s e t t l i ng plankton and i t s remains, d e t r i t u s transported in r ive rs , surface runoff, sewage treatment plant e f f luen ts , and d e t r i t u s mobilized by storm waves and shore erosion from sur - rounding marshes and t i de f l a t s , and carried by t ida l currents t o the open bay. The metabolic r a t e , energy flow, and productivity of the benthic community, and ultimately i t s capacity t o sustain a f ishery, depends upon the r a t e a t which t h i s organic matter i s supplied (Hargrave 1973; Pamatmat 1977). Needless t o say, the ra te of supply of organic matter t o the benthos of San Francisco Bay i s unknown.

While the re may be in te res t in measuring the r a t e of organic matter supply t o the benthos, i t cannot be measured direct ly with exis t ing methods (passive col lectors in the water column or on the bottom) because of the predominance of resuspension and horizontal advective transport processes associated with r i ve r discharge and t ida l currents . Furthermore, f i l t e r feeders such as clams and mussels apparently active1 y remove large quan t i t i e s of phytoplankton from within the water column. That i s , they are n o t necessari ly passive col lectors of se t t i ed pa r t i c l e s .

A combination of independent measures may be useful in estimating t o t a l

benth ic supply ( i . e . , summing t h e l o s s e s o f organic ma t t e r from the bottom - - ben- t h i c metabol ic ox ida t i on , bu r i a l r a t e , and r a t e of p reda t ion on benthos by demersal f i s h , p lus l o s s of o rganic ma t t e r with sediments leav ing San Francisco Bay). Meanwhile, we can only guess a t answers t o ques t ions t h a t involve t h e amount and f a t e of o rganic ma t t e r e n t e r i n g t he bay, such as (1) t h e t o t a l b io log i ca l p roduc t iv i t y of t he benthos, ( 2 ) t he capac i t y of t h e bay organisms t o decompose organic waste from domestic sewage e f f l u e n t s , and ( 3 ) whether t h e benth ic comm~~ni t y ' s f unc t i ons have been impaired by po: lu t ion .

4.4 FATE OF ORGANIC MATTER IN SEDiMENTS

Benthic energy flow and biogeochemi - ca l cyc l e s a r e l i nked t o t h e f a t e of organic d e p o s i t s i n t he bottom. Par t of t he s e t t l i n g organic ma t t e r i s inges ted d i r e c t l y by macrofauna, d i g e s t e d , and me- t abo l i zed t o carbon d iox ide , water , and d isso lved n u t r i e n t s such a s n i t r a t e s and phosphates. The uneaten and undigested f r a c t i o n e n t e r s t h e d e t r i t a l food web (Fenchel and Jorgensen 1977) where complex organic ma t t e r i s f u r t h e r transformed and mineral i zed by a v a r i e t y of metabol i c types of microorganisms.

Complex organic subs tances degrade as they pass through t h e metabol ic web (Figure 30). Whif e breaking down complex molecules, microbes syn thes i ze p r o t e i n s , po lysacchar ides , nucl e i c ac id s , and o t h e r matter whose complexity i s equal t o o r g r e a t e r than t h a t o f t h e i r s u b s t r a t e . The microbes a r e i nges t ed , d i g e s t e d , and metabol ized by s e l e c t i v e and nonse l ec t i ve depos i t f e ede r s (meiofauna and macrofauna). Microbes and higher forms of organisms a r e s i m i l a r i n metabol i z ing p a r t of t h e i r food i n t o smal le r molecules o r t h e mineral bu i ld ing blocks of o rganic mat te r , and r e syn thes i z ing p a r t i n t o complex molecules t h a t make up t h e i r r e spec t i ve biomass. S ince decomposition i s t he breakdown of dead organic mat te r , i t i s no t a microbial process a lone . The "decomposer" compartment in ecosystem models has no d i s t i n c t f unc t i ona l r e a l i t y 1 i ke primary producer, chemoautotroph, s u l f a t e reducer , e t c . The benth ic community as a whole i s a decomposer and mine ra l i z e r o f t he o rgan i c ma t t e r a v a i l - ab l e i n t he system.

The na tu ra l r a t e s of ben th ic microbi a1 processes in San Francisco Bay, which must be known f o r q u a n t i t a t i v e model ing of t h e sediment organic ma t t e r budget, have not been measured. Ins tead ,

C O ~ , PC?: O2 + Photoa~itotrophs SO:, NO?, NO, \ i 1 t h 0,,~03

Anaerobic Zone

Fermenters

,,, Ferrnentaiion Products /

Deniirifiers

so,

Figure 30. Relations among aerobic processes in the oxic surface sediment layer and anaerobic processes in the deeper ancxic layers. Acid fermentation produces organic acids, hydrogen, and carbon dioxide, v~hich are utifired in different anaerobic respiratory processes, producing reduced inorganic substances that are oxidized by chemoautotrophs.

work on San Francisco Bay sediment microbiology has been focused on d e n i t r i f i e r s (Oremland e t a1 . 1984; Mi l l e r e t a1. 1986), s u l f a t e reducers (Oremland and S i lverman 1979), and methanogens (Qremland 1981; Oremland and Polcin 1982; Oremland e t a l . 19821, with t h e fol lowing ob j ec t i ve s : ( 1 ) t o examine t h e biogenic o r i g i n of hydrocarbon gases i n sediments (Oreml and 1981 ; Vogel e t a1 . 1982) ; ( 2 ) t o c l a r i f y t h e i n t e r a c t i o n s between s u l f a t e reducers and methanogens (Oreml and and Polcin 1982; Oremland e t a l . 1982); ( 3 ) t o show t h e anaerobic degrada t ion of s p e c i f i c o rganic compounds (Smith and Oreml and 1983); ( 4 ) t o exp l a in t h e occurrence of methane in s u r f a c e waters (Oreml and 1979) ; and (5) t o i d e n t i f y t h e anaerobe 's na tu r a l energy and carbon sources (Oremland and S i 1 verman 1979) . These s t u d i e s demonstrate t h e involvement o f anaerobes i n various chemical t ransformat ions i n t he bay and g i v e us some of t h e necessary know1 edge f o r a ccu ra t e model i ng of s ed i - ment processes . For example, some methanogenic b a c t e r i a produce e thane , methane, e thene , propene, propane, and butane (Oreml and 1981 ; Vogel e t a1 . 1982). Because t h e s e ga se s can bubble out of t h e sediments (Oreml and and Si 1 verman 1979), t h e i r l o s s e s must be accounted f o r i n an accura te carbon budget.

The oxygen uptake by sediments has commonly been measured because of i t s per - ceived equivalence t o benth ic community metabolism and energy flow (Teal and Kanwisher 1 9 6 i ) . The r a t e of oxygen uptake has been found t o be r e l a t e d t o t h e r a t e of o rganic ma t t e r supply, tempera- t u r e , h y d r o s t a t i c p r e s su re , pH, t i d a l cyc le , die1 c y c l e , oxygen t ens ion , o rganic po l l u t i on , o rgan i c ma t t e r conten t o f sed i - ments, b a c t e r i a l count , and macrofaunal i r r i g a t i o n of t ubes and burrows. Some of these f a c t o r s a r e obviously i n t e r r e l a t e d ( Pamatmat 1977). The p a r t i cul a r depend- ence of benth ic oxygen consumption on phytoplankton product ion and subsequent sedimentat ion of o rganic ma t t e r t o t h e bottom i s now c l e a r (Hargrave 1973).

The only publ ished d a t a f o r San Francisco Bay (Hammond e t a1 . 1985) come from two s i t e s i n South Bay (Table 4 ) . Rates of oxygen consumption and carbon d ioxide product ion were h igher a t a s h a l - low s i t e (1.5-m water depth) than a t a deeper s i t e (14-m d e p t h ) . These r e s u l t s suggest a higher r a t e of o rgan i c mat te r depos i t ion a t t h e shal low s i t e . Ove ra l l , t he r a t e s f l u c t u a t e d s ea sona l ly by a f a c - t o r of 1 . 5 around an average of 27 mmol

Table 4. Rates of benthic oxygen uptake and carbon dioxide production in South Bay (Hammond et a!. 1985).

mmol ~ , / m ~ / d mmoi c0,/m2/d

Date T OC (k s t d . e r r o r ) (! s t d . e r r o r ) R q (=co2/02

Shallow s t a t i o n (1,5) Feb 19130 J u n Nov Feb 1980

Annual average

Deep s t a t i o n (14 m) Feb 1980 Jun Nov Feb 41981

Annual average

Not measured 43 0.9

16 i 3 0 . 6 14 ti 5 0.8 24 .t- 8

Not measured 33 + 1 1 . 5 16 rt 5 i.5 10 i 5 0.9 20 t 4

/m2/d, bud t h e i .5-m-deep l oca t i on showed a g r e a t e r seasonal amplitude than t h e 1 4 - m s i t e . The r a t e s ranged from 11 rnrnol/m2/d i n t h e f a l f / w i n t e r a t 14 m t o 46 mmol/m2/d in t he summer a t 1 .5 rn. These va lues a r e in t h e low t o middle p a r t of t he range (14 t o 95 mmol/m2/d) observed i n a v a r i e t y of coas ta l marine systems (Mixon 1981).

The r a t i o of moles CO, produced t o moles 0, consumed, known a s t h e r e s p i r a t o r y quo t i en t ( A Q ) i n animal metabol ism, i s a useful i n d i c a t o r of metabol i c a c t i v i t y , The ae rob i c ox ida t ion of f a t s , p ro t e in s , and carbohydra tes r e s u l t s in a value of 0 .7 , 0.85, and 1 , 0 , r e s p e c t i v e l y . Thus a range of 0 .7 t o 1 .0 sugges ts t h a t organic ma t t e r o f mixed composition i s e s - s e n t i a1 l y mineral i zed by aerobic r e s p i r a t i o n . Values of RQ g r e a t e r than 1 a r i s e when anaerobic r e s p i r a t i o n (deni t r i f i c a t i o n , s u l f a t e r educ t i on , e t c . ) produces CO, i n add i t i on t o t h a t which i s produced by ae rob i c r e s p i r a t i o n a t t h e sediment su r f ace . A va lue l e s s than 0 . 7 s i g n i f i e s t he uptake of oxygen by i no r - gani c chemical ox ida t ion r e a c t i o n s without a corresponding product ion of CO,, e : g . , s u l f i d e ox ida t i on and f e r r o u s - i r o n oxida- t i o n . The foregoing i n t e r p r e t a t i o n does not t ake i n t o account t h e r o l e of chemoautotrophs, which u t i l i z e both oxygen and carbon d ioxide t o produce organic mat- t e r (Pamatmat 1986). The r a t i o has been used as an i nd i ca t i on of aerobic-anaerobic bal ance i n benth ic systems ( Pamatmat 1984, 1986). Hammond e t a l . (1985) obtained values between 5.6 and 1.5 a t t h e i r two s i t e s in South Bay. The r a t i o s a t t h e i r shallow s i t e were l e s s than 1.0, while t h e 14-m depth showed a range of 0 .9 t o 1.5.

Hammond e t a l . (1985) compared t h e annual sediment oxygen uptake, o r i t s carbon equ iva l en t , wi th t h e es t imated annual phytoplankton product ion and concluded t h a t ben th ic b io log i ca l processes a1 t oge the r remineral i z e 70% t o 90% of p a r t i c u l a t e organic carbon produced by phytoplankton. These d a t a support t h e observat ion t h a t g raz ing by benth ic i nve r - t e b r a t e s i s a primary mechanism control 1 ing phytoplankton blooms in South Bay (&loe rn 1982). The oxygen-uptake, phytopl ankton-product ion comparison does not include t h e c o n t r i b u t i o n of benth ic primary product ion p lus o t h e r forms of o r - ganic ma t t e r t h a t e n t e r t he South Bay from su r f ace runo f f , s t reams, e f f l u e n t s from sewage t rea tment p l a n t s , and d e t r i t u s from surrounding marshes. I t i s important

t he r e fo re t o have an independent and pos- s i b l y d i r e c t measure of o rganic ma t t e r sedimentat ion t o t h e bottom. However, because s t u d i e s t o provide d i r e c t measurements of o rganic ma t t e r supply t o t h e benthos of San Francisco Bay have not been undertaken, we must f i n d o t h e r ways t o complete t h e benth ic budget of o rgan i c matter and improve our e s t ima te s of meta- b o l i c l o s s e s i n t he sediment .

4.6 BENTHIC NUTRIENT REGENERATiON IN SAN FRANCISCO BAY

The b io log i ca l p roduc t iv i t y of San Francisco Bay, a s e lsewhere ( s e e Ze i tzsche l 1980), i s c o n t r o l l e d i n p a r t by t h e i n t e r a c t i o n s between t h e benthos and t h e water column. As water depth i n - c r ea se s , ben th ic mine ra l i z a t i on decreases and metabol ic ox ida t i on by t h e plankton i nc rea se s , p r imar i l y because of t h e longer res idence time of o rgan i c p a r t i c l e s i n t h e water column (Hargrave 1973). In s h a l l ow e s t u a r i e s such a s San Francisco Bay, however, t h e benthos p l ays a dominant r o l e . The con t ro l l i n g i n f luence by t h e benthos can be measured in terms of ( I ) i t s r a t e of removal o f o rganic ma t t e r from t h e water column, ( 2 ) i t s r a t e of degrada- t i o n of s e t t l e d organic ma t t e r , and (3) i t s r a t e of r e l e a s e of primary n u t r i e n t s t o the ove r ly ing water .

Hammond e t a f . (1985) used i n s i t u f l u x chambers a t two s t a t i o n s t o measure changes i n concent ra t ions of radon, oxygen, ammonia, carbon d iox ide , s i l i c a , a1 kal i n i t y , n i t r a t e p lus n i t r i t e , and phosphate in t h e enclosed water ( e . g . , Table 4 ) . Pore-water p r o f i l e s of n u t r i e n t s and radon were a l s o determined. Calcu la t ions of ben th ic f l u x e s from t h e p r o f i l e s were c o n s i s t e n t with chamber measurements and i nd i ca t ed t h a t O,, C8, and n i t r a t e - n i t r i t e f l u x e s were t h e r e s u l t of r eac t i ons occur r ing in t h e t op few cen- t ime te r s of sediment , while t he f l u x e s of MH,, SiQ, , and a l k a l i n i t y were dr jven by r e a c t i o n s proceeding i n t h e e n t i r e 20- t o 40-cm sediment column. Seasonal and spa- t i a l d i f f e r e n c e s i n f l u x e s showed t h e e f f e c t s o f t empera ture , sp r ing phytoplankton bloom, and t h e i r r i g a t i o n of burrows through r e s p i r a t o r y a c t i v i t y o r locomotion of infauna. The f l u x e s of these 3 i s s o 9 v ~ d m a t e r i a l s i n Scath Say were s i m i l a r t o those measured i n o t h e r temperate e s t u a r i e s with the same l eve l of primary product ion. Smal I e r seasonal

amplitudes i n San Francisco Bay were a t - t r i b u t e d t o t h e re1 a t i v e l y smal I seasonal temperature range.

Mass balance c a l c u l a t i o n s f o r South Bay (Hammond e t a l . 1985) i nd i ca t ed t h a t about 65% of s i l i c a i n t h e annual phytoplankton primary product ion was recycled by t h e benthos. The s i l i c a f l u x could r ep l en i sh t h e s tanding s tock i n t he water column i n 17-34 days. Also , ben th i c n i t r i f i c a t i o n and d e n i t r i f i c a t i o n were shown t o conver t 55% of o rgan i c n i t rogen reaching t h e sediments i n t o n i t r ogen gas. Ammonia f l u x could r ep l ace s tanding s tocks i n t h e water column i n 2 - 6 days. All of these f i g u r e s demonstrate t h e q u a n t i t a t i v e importance of t h e benthos i n t h e biogeochemical c y c l e of t h e e s t u a r y .

4.7 MODELS OF ORGANIC MAUER BUDGETS OF ESTUARINE BENTHOS

muni c i pa1 sewage- t rea tment pl a n t s and c a r r i e d by s u r f a c e runoff d i r e c t l y i n t o t he bay, make up t h e t o t a l input t o t h e bay. From t h i s , t h e t o t a l amount metabo- l i z e d i n t h e water column and exported t o t he open ocean must be sub t r ac t ed t o ob- t a i n an e s t i m a t e of t h e amount t h a t s e t t l e s t o t h e bottom. The o rgan i c ma t t e r t h a t reaches t h e bottom i s d i s s i p a t e d by benth ic metabol ism, removed and exported by preda t ion and sediment e ro s ion , and removed from t h e biogeochemical cyc l e by buri a1 .

A summary of t h e known sources and s inks of o rgan i c ma t t e r f o l l ows.

Total bay i npu t = Plankton primary product ion

+ Macroal gal primary product ion

Our p r e sen t compari sons of e s t u a r i e s + B e n t h i c microa lga l primary a r e l im i t ed by t oo few known q u a n t i t a t i v e product ion r e l a t i o n s . Hargrave's (1973) empir ica l equat ion r e l a t i n g benth ic oxygen uptake t o + Eel g r a s s product ion plankton primary product ion and mixed l a y e r depth, + River-borne d e t r i t u s

b sediment 0, uptake (l/m2/yr) = a(C/Zm) , where a and b a r e cons t an t s , C i s n e t annual primary product ion i n g ~ / m 2 , and Z i s mixed-layer depth ( t h e t h i cknes s of the v e r t i c a l l y mixed water l a y e r ) , i s a s t e p towards q u a n t i t a t i v e modeling of ben th ic a c t i v i t y . For an e s t u a r y with d i v e r s e s o u r c e s of o r g a n i c c a r b o n , h o w e v e r , H a r g r a v e ' s model o f b e n t h i c oxygen consumption ignores many f a c t o r s ref ated t o t o t a l e n e r g y s u p p l y . For example, p reda t ion i s bel ieved t o be a s i g n i f i c a n t f a c t o r i n Chesapeake Bay (Kemp and Boynton 1981) and may be i n San Francisco Bay as w e l l . A model i n c o r p o r a t i n g a l l such f a c t o r s i s important.

A model combining a17 known f a c t o r s and p r o p e r t i e s and d e s c r i b i n g how they q u a n t i t a t i v e l y determine t h e ecology of t he benthos and San Franc isco Bay as a whole would be a va luab l e management t oa l . Kremer and Nixon (1978) have s e t an example f o r simul a t i n g t h e p r o p e r t i e s and processes occu r r i ng i n an e s t u a r y .

The sum o f a l l t h e o rgan i c ma t t e r coming from t h e va r ious sources d i scussed above, p l u s t h e amounts d i scharged by

+ Marsh-derived d e t r i t u s

t Sewage-derived d e t r i t u s

+ Sur face - runo f f -de r i ved d e t r i t u s

+ Dissolved o rgan i c ma t t e r from a17 sources

+ Matter e n t e r i n g t h e bay from t h e ocean

Benthic supply = t o t a l bay input

- PI ankton metabol ism

- Export t o t h e ocean

A t s teady s t a t e , Benthic supply = Benthic 1 osse s .

Benthic l o s s e s = Metabolic ox ida t ion by community

t Removal by migratory dernersal p r eda to r s

+ Export v i a e ro s ion of sediment

+ Removal by burial

+ Loss of gametes and larvae

+ Loss of dissolved substances

Many terms of the organic matter budget of the bay are unknown, including the character and ra tes of organic matter input to the benthos. Even in a study of an estuarine system for which much more detailed data on the par t i t ioning of o r - ganic matter are available (e .g . , Marshal l 1970), i t i s s t i l l an exceedingly d i f - f i c u l t task t o t r an s l a t e those data in to an understanding of , f o r example, the ab- solute yie ld of commercially exploitable species. Better knowl edge about the

dynamic re la t ion among the separate components of the estuary (benthic versus pelagic, l iv ing versus nonliving) i s es - sential i f we are t o answer a broad range of questions re1 ated t o f i sher ies produc- t ion, e f f ec t s of pol lut ion, capacity of the bay t o decompose organic wastes, and occurrence of nuisance blooms of macroalgae. For t he present, we have only separate pieces of comparative information from d i f fe ren t es tuar ies . The existence of data from other ecosystems and knowl edge of general pri nci pl es derived e l sewhere, whi 1 e he? ping us design re - search plans f o r future s tudies of the bay, do not provide the kind of spec i f i c deta i l we need t o predict important ecosystem responses in San Francisco Bay.

CHAPTER 5. ANTHROPQGENIC INFLUENCES

The San Francisco Bay Estuary and i t s d ra inage bas in , l i k e many e s t u a r i n e systems throughout t h e world, have been a f f ec t ed by human a c t i v i t y (Nichols e t a l . 1986). The bay a r e a has been populated by American Ind ians s i n c e a t l e a s t t he end of t h e l a s t g l a c i a l per iod , a1 though most remains of bay-area i n h a b i t a n t s p r i o r t o 5,000 yea r s ago have presumably been covered by t h e s e a (Atwater 1979). Unti l t h e a r r i v a l o f European c o l o n i z e r s , an e s - t imated 20,000 t o 25,000 Ind ians l i v e d in severa l hundred small vi 11 ages and depended on t he bay f o r a l a r g e propor t ion of t h e i r food (Bolton 1927; U.S. Fish and Wi I d 1 i f e Se rv i ce and Cal i fo rn i a Department of Fish and Game 1979).

Spanish s o l d i e r s and mi s s iona r i e s , f i r s t d i scover ing t h e bay in 1769, found a va s t complex of open-water bays and su r - rounding f r e s h - and s a l t w a t e r marshes with p l e n t i f u l game an imals , b i r d s , and f i s h . The t i d a l marshes alone covered an e s - t imated a r e a of about 2,200 km2 ( G i l b e r t 1917). This landscape changed a s t h e c u l - t u r e changed, bu t p a r t i c u l a r l y a f t e r t h e discovery of gold i n 1848 when Cal i f o r n i a was inundated wi th immigrants. Now, a l l t h a t remains of t h e abo r ig ina l c u l t u r e , which had changed 1 i t t l e with t he passage of m i l l e n i a , a r e a few of t h e more than 400 s h e l l middens ( t h e d e b r i s of t h e abor ig ina l d i e t c o n s i s t i n g 1 a rge ly o f s h e l l f i s h ) t h a t were mapped about 1900 (Nelson 1909, 1910) (F igure 31) . The r e s t n f t h e middens have 1 ong been buried o r e l iminated by urban and i n d u s t r i a l development. Sirnil a r l y , t h e e s tua ry has been changed by land rec lamat ion , over- f i s h i n g , and waste d i s cha rge wi th in t h e e s tua ry ; a g r i c u l t u r a l p r a c t i c e s i n the Central Val 1 ey ( f ede ra l Water Po l lu t i on Control Admini stratian 1963) ; hydraul i c gold mining i n t h e mountains {Gi lbe r t 1917); and management of r i v e r flow (Nichols e t a1 A 1986).

Human in f luence on t h e bay ecosystem i s seen most c l e a r l y a s change in t h e compos i t i on of t h e b i o t i c community, reduct ion o r e l im ina t i on of some of t h e bay's na tura l r e sou rce s , and d e t e r i o r a t i o n in t h e a e s t h e t i c and r ec r ea t i ona l value of

Figure 31. Distribution of indian shell middens and tidal marshes at about 1900. Most middens are now covered by urban development (map adapted d r ~ m Nelson 1909).

t he e s tua ry . The p o t e n t i a l agents For unwanted change a r e physical a l t e r a t i o n of t he bay's shore? i ne and bathymetry, over- e x p l o i t a t i o n of i t s r e sou rce s , i n t e r f e r e n c e wi t h t h e na tu ra l hydrologic cyc le , and d isposa l of human and i n - d u s t r i a1 wastes and dredge spo i l s .

5.5 EARLY PHYSICAL AND BlObOGICWL CHANGES

Rapid sedimentat ion of gold mining d e b r i s caused un in t en t i ona l shoal ing o f t he bay and i t s t r i b u t a r y s t reams and r i v e r s dur ing t h e per iod of hyd rau l i c mining in t h e S i e r r a Nevada Mountains between 1851 and 1884. A t i t s maximum use, hydrau l ic mining turned over t e n s of mi7 - 1 ions of cubic meters of gold-bearing mater ial annual ly ( G i l b e r t 1917). The mining r e s idue , c o n s i s t i n g of mud, sand, gravel , cobbles , and boulders , washed from the h i l l s i d e s and choked t h e c r eeks and r i v e r s of t h e Sacramento and San Joaquin Rivers . During succeeding decades, much of t h e mud and sand was f lushed ou t of t h e r i v e r s and i n t o San Francisco Bay ( G i l b e r t 1917; Atwater e t a l . 1979). By t h e end of t he 19th cen tu ry , 1 .0, 0.75, and 8 .25 m o f sediment had been depos i ted i n Suisun, San Pabl o, and Central Bays, r e s p e c t i v e l y , c r ea t i ng l a r g e shoal a r e a s , reducing t h e water volume of t h e bays, and a l t e r i n g c i r c u l a t i o n p a t t e r n s ( G i l b e r t 1917).

The s h o r e l i n e of t h e bay was a l s o g r e a t l y a1 t e r e d . The a r ea of t h e marshes p r i o r t o 1850 was es t imated a t about 2,200 km* ( G i l b e r t 1917). Leveeing and f i l l i n g of t he bay per imeter t o c r e a t e a g r i c u l - t u r a l , commercial, i n d u s t r i a1 and r e s i d e n t i a l land reduced t h e a r ea of t h e unleveed t i d a l marshes by about 95% (Atwater e t a l . 1979; Josse lyn 1983). Some of t h e leveed reg ions ( p r i m a r i l y a g r i c u l t u r a l l and ad jacent t o Suisun and San Pablo Bays and i n t h e Del ta , and s a l t evaporat ion ponds i n South Bay) r e t a i n some wetl and c h a r a c t e r i s t i c s ( "seasona l wetl ands") , and t hus provide va luable h a b i t a t f o r aqua t i c b i r d s .

The l o s s of t i d a l wetlands meant t h e e l imina t ion of much of t h e e s t u a r y ' s vas- c u l a r p l a n t primary product ion , a po ten t ia l source of food f o r benth ic o r - ganisms throughout t h e bay. The l o s s of wetlands has a l s o meant l o s s of migratory shorebird h a b i t a t , and with i t a l o s s i n thenumber of waterfowl using t h e bay (Skinner 1962). However, quan t i fy ing any

change i n t h e capac i t y of t h e bay t o produce ha rves t ab l e p r o t e i n , long a f t e r t h e change occur red , i s impossible . The only pos s ib l e b e n e f i t s t o t h e benthos of San Francisco Bay r e s u l t i n g from t h e near ly complete modi f ica t ion of t h e sho re l i ne a r e (1) t h e pos s ib l e reduc t ion i n shoreb i rd preda t ion because of t h e presumed reduc t ion i n shoreb i rd abundance (through hunting p re s su re and l o s s of h a b i t a t ) , and (2 ) t h e add i t i on of new h a b i t a t f o r some of t h e introduced spec i e s such a s t h e Japanese l i t t l e n e c k clam, Tapes phi1 ippinarum, through t h e cons t ruc- t i o n of l evees and seawal l s (McAll i s t e r and Moore 1982).

Contamination o f t h e bay by human and i n d u s t r i a l wastes was recognized as e a r l y as 1900 ( e .g . , Nelson 1909; Skinner 1962). As l a t e a s t h e mid-1950's, l e v e l s of water-col umn oxygen concent ra t ion a t o r near 0 mg/l were common in South Bay during summer (Pearson 1958; S t o r r s e t a1. 1966), with t h e r e s u l t t h a t few o r no animals were found i n South Bay s loughs (Brown and Cal dwel I Engineers 1954) .

The e f f e c t s of t h e i n t roduc t ion of spec ies on benth ic community s t r u c t u r e were marked: t h e new spec i e s a r e now c l e a r l y predominant in t h e community i n both abundance and biomass (Sec t ion 2 .3 ) . We can only guess now a t t h e na tu re of t h e ensuing i n t e r a c t i o n s and changes i n func- t i ona l r e l a t i o n s , ove ra l l b io log i ca l p roduc t iv i t y , and community e n e r g e t i c s t h a t occurred p rog re s s ive ly as one i n t r o - duced spec i e s a f t e r another became e s t ab l i shed .

5.2 [NTERFERENCE WfTH THE NATURAL HYDROLOGlC CYCLE

Seasonal p a t t e r n s of r i v e r flow and t o t a l annual flow a r e major f a c t o r s d e t e r - mining t h e bay's s a l i n i t y d i s t r i b u t i o n and pa t t e rn s of c i r c u l a t i o n and mixing (Ha l t e r s e t a1 . 1985). The s a l i n i t y of t h e bay f l u c t u a t e s g r e a t l y from season t o season i n response t o t h e w in t e r high-flow and summer low-flow p a t t e r n (Sec t ion l . a ) and between y e a r s i n response t o y e a r - t o - yea r d i f f e r e n c e s i n r a i n f a l l and runoff (wet versus d r y y e a r s ) . These f l u c t u a - t i o n s i n s a l i n i t y and i n o t h e r physicochemical a t t r i b u t e s of t he bay r e s u l t d i r e c t l y in marked tenlporal changes in a l l of t h e b io logica l communities o f t he e s tua ry (Cloern and Nichols 1985). In

winters and dur ing wet y e a r s , most e s - t u a r i n e benth ic spec i e s a r e r e s t r i c t e d t o t he p a r t of t h e bay west o f Carquinez S t r a i t because o f t h e i r i n t o l e r a n c e of f reshwater . The degree of displacement depends on t h e magnitude and du ra t i on of t he w in t e r - sp r ing f r e s h e t . In summer, when s a l i n i t y i n c r e a s e s , t h e e s t u a r i n e spec i e s reco lonize t h e p r ev ious ly vacated a r ea s . Despi te t h e t y p i c a l l y 1 arge seasonal and in te rannual v a r i a t i o n s in spec ies abundances and d i s t r i b u t i o n s , ben- t h i c community composition over t h e long term seems t o have remained s t a b l e (Chapter 3 ) .

Against t h e background of n a t u r a l l y varying r i v e r in f lows , d e t e c t i o n of t h e e f f e c t s o f f r e shwa te r impoundment (reducing t h e na tu ra l volume of r i v e r inflow) on t h e bay ' s benthos i s d i f f i c u l t . This i s t he case because t h e r e a r e no long-term bay-wide d a t a on spec i e s d i s - t r i b u t i o n s and abundances t h a t would al low us t o uncover d i r e c t a s s o c i a t i o n s with r i v e r flow.

The occasion of t h e 1976-77 drought along t h e west coas t of North America o f f e r ed a "wors t -case" example of t he re1 a t ion between reduced flows and balances among t h e aqua t i c communities of t he bay. During t h e drought , inf low from the Sacramento-San Joaquin River system was g r e a t l y reduced and t h e t y p i c a l summer phytoplankton maximum i n Suisun Bay was absent d e s p i t e g r e a t l y increased water c l a r i t y (reduced suspended sediment l o a d ) . Perhaps a s a consequence of t h e low phytoplankton biomass, zooplankton, shrimp, and l a r v a l s t r i p e d bass in Suisun Bay were a l s o found a t very low l e v e l s . Cloern e t a l . (1983) suggested t h a t t h e t yp i ca l summer phytoplankton maximum during t he per iod of extremely low summer flow ( l e s s than 100 m3/s) was moved upstream i n t o t h e deeper Sacramento River where 1 i gh t 1 imi t ed growth. Simultaneously, ben th ic spec i e s normally r e s t r i c t e d t o t h e more s a l i n e waters west of Carquinez S t r a i t migrated upstream i n t o Sui sun Bay and e s t a b l i shed dense popill a- t i o n s (Nichols 1985b). These populat ions may have s u f f i c i e n t l y grazed t he phytoplankton t o c o n t r i b u t e t o t h e decf i ne s o f t h e p e l a g i c consumers. From t h i s s cena r io , one can conclude t h a t during any prolonged per iod of reduced r i v e r flow, when Suisun Bay s a? i n i t y remains above z e r o dur ing h i n t e r , t h e dominant food web of Suisun Bay could

s h i f t from pe l ag i c t o benth ic and, as a r e s u l t , a f f e c t t h e pe l ag i c f i s h e r y y i e l d t h e r e . In c o n t r a s t , dur ing sp r ing of years with high r i v e r in f low, s tanding s tocks of phytoplankton, a t l e a s t i n South Bay, a r e h ighes t because t h e f reshwater su r f ace l a y e r t h a t p e n e t r a t e s i n t o South Bay enhances water column s t a b i l i t y t h a t favors a 1 a r g e r phytopl ankton bloom (Cl oern e t a1 . 1985).

The observed changes i n t h e food web of nor thern San Francisco Bay under pro1 onged cond i t i ons of reduced r i v e r flow, while t h e r e s u l t o f an extreme na tura l even t , a r e important in t h e con- t e x t of p roposa ls t o i nc r ea se r a t e s o f water d ive r s ion i n t h e f u t u r e ( e . g . , Meral 1982). The concern i s t h a t without some l i m i t s on t h e r a t e and t iming of i n t e r r u p - t i o n s of t h e flow of f reshwater t o t h e bay, changes i n p l a n t and animal com- munit ies l i k e t hose seen dur ing t h e 1976- 77 drought could occur dur ing f u t u r e d ry periods. Such changes, i f su s t a ined , might a f f e c t f i s h e r y r e sou rce s . While our presen t evidence f o r such a d i r e c t r e l a - t i o n in San Francisco Bay i s s can ty , l a r g e dec l i ne s i n f i s h ca t ches in many o t h e r e s - t u a r i e s have fo l l owed 1 a rge-sca l e impoundments of f reshwater (Rozengurt and Herz 1981) .

Increased f reshwater d ive r s ion may a1 so in f luence t h e chemical contaminat ion of t he e s t u a r y . During t h e 1976-77 drought y e a r s , t h e bottom d e p o s i t of t h e lower Sacramento River changed from sand t o mud, and increased i n oi 1 , grease , and metal conten t ( S i e g f r i e d e t a l . 1980). There i s evidence t h a t t h e f reshwater flows from t h e Sacramento and San Joaquin Rivers s i g n i f i c a n t l y a f f e c t t h e concentra- t i o n of contaminants in sediments and organisms e l sewhere i n San Francisco Bay: t he lowest concen t r a t i ons of s i l v e r i n clams c o l l e c t e d from South Bay were observed dur ing high-f low yea r s (F igure 32) . Although t h e mechanisms a r e no t y e t c l e a r , contaminants a r e more r a p i d l y a s s imi l a t ed by o r f lushed from t h e bay dur ing per iods of high r i v e r flow (Luoma e t a l . 1985). Fur ther , decreased r i v e r inf low t o t h e bay means t h a t waste water becomes a l a r g e r percentage of t h e t o t a l flow of water i n t o t he bay (Russel 1 e t a1 . 1982).

Another typjca! consequence of reduced r i v e r inf low t o e s t u a r i e s i s decreased sediment input and increased water t ransparency (Krone 1979). This

I I 1 - 1 . . . . I

500 1000 1500 2000 2500

River Discharge m3s-'

Figure 32. Relation between the winter maximum concentration of silver (average and 95% confidence limits) in Macoma balthica from the Palo Alto study site (Figure 4) and the rate of freshwater inflow from the Sacrarnento-San Joaquin River system during December (from Luoma et al. 1985; silver concentrations erroneously reported therein as milligrams per gram).

could be an important i s s u e i f , during periods of low r i v e r inf low, decreased t u r b i d i t y favored nuisance blooms of a lgae . As mentioned above, however, phytoplankton dec l i ned dur ing t h e 1976-77 drought per iod . Macroalgae, unaf fec ted by benthic f i l t e r f eed ing , might be expected t o pro1 i f e r a t e a s a r e s u l t of increased water c l a r i t y . Cur ious ly , however, no unusual macroal gal blooms occurred during t he drought y e a r s . What i s c l e a r from t h i s observa t ion i s t h a t while we may know how indiv idua l e s t u a r i n e p r o p e r t i e s f e . g . , sediment 1 oad, s a l t balance, r e s idence t ime, n u t r i e n t l oad ) w i l l change i n response t o changes in r i v e r inf low, we f ind i t d i f f i c u l t t o p r e d i c t ecosystem- 1 eve1 consequences.

The long-term e f f e c t of f u r t h e r i n - c reases i n f reshwater d ive r s ion on beninos production i s a l s o unc l ea r . An important t e s t of our understanding w i l l be t o determine whether t h e same s e t o f b i o l o g i - ca l condi t ions observed i n northern San Francisco Bay dur ing t h e drought y e a r s ( l a r g e benth ic i n v e r t e b r a t e biomass, reduced phytoplankton biomass), wi 11 r e c u r during t h e next drought per iod . The theory r a i s e s o t h e r ques t i ons a s wel l . I f t h e benthos becomes more prominent in northern San Franc isco Bay a s a r e s u l t of increased s a l i n i t y , w i l l a ben th ic food web rep1 ace t h e p r e sen t p lanktonic food web and r e s u l t in t h e d e c l i n e of pe l ag i c food spec i e s i n t h a t p a r t of t h e e s tua ry? Answers t o t h i s and r e l a t e d ques t ions a r e , a s y e t , beyond our reach .

5.3 EFFECTS OF POLLUTION

Approximately 30 municipal and 40 i n - d u s t r i a l was te - t rea tment f a c i l i t i e s and an add i t i ona l 100 sma l l e r i n d u s t r i a l p l a n t s d i scharge t r e a t e d waste i n t o San Francisco Bay, whi le more than 50 small l o c a l streams d i s cha rge un t r ea t ed waste from urban runo f f . Addit ional waste, 1 a rge ly from a g r i c u l t u r a l r eg ions , e n t e r s t h e bay in t he flows from t h e Sacramento and San Joaquin Rivers (Nichols e t a l . 1986). The bay annual ly r ece ives 5,500 t ons of o i l and grease and 438 t ons of o t h e r pol - l u t a n t s (372 tons of which a r e heavy meta l s ) from i n d u s t r i a l and domestic sewage-treatment p l a n t s ( C i t i z e n s f o r a Be t t e r Environment 1983). Although t h e d a t a a r e extremely l i m i t e d , t h e amounts of heavy meta l s from r i v e r inf lows and s u r - f ace runoff flowing un t r ea t ed i n t o t h e bay a r e est imated t o be twice a s high a s t h a t i n t reatment p l an t e f f l u e n t s (Russel 1 e t a l . 1982).

Most p o l l u t a n t s discharged i n t o es- t u a r i e s end up i n p a r t i c u l a t e farm through adsorp t ion , compl e x a t i on, and prec i pi t a - t i o n . Incorpora t ion of p o l l u t a n t s i n sediment d e p o s i t s l e a d s t o concen t r a t i ons t h a t a r e much higher than i n t he over ly ing water (Meff e t a l . 1978). The pos s ib l e d e l e t e r i o u s e f f e c t s o f contaminant-bearing sediment on t h e benthos and organisms t h a t feed on t h e benthos a r e a major concern f R i sebrough e t a? . 1 9 7 7 ) .

Cal i f o r n i a S t a t e agenc ies have been s tudying ways of determining local and

regional e f f e c t s o f waste d i scharges i n t o San Francisco Bay (Johns and Bachman 1982). The subs tances of g r e a t e s t concern have been petroleum hydrocarbons and heavy metals because samples of clams and mus- s e l s from t h e bay have shown some o f t h e h ighes t body burdens of t he se subs tances i n organisms sampled from coas t a l waters nationwide (Luoma and Cloern 1982).

Past e f f o r t s t o determine t he e f f e c t of waste contaminat ion on t h e b i o t a of t h e bay have been l imited l a r g e l y t o l oca l s t u d i e s of contaminant concen t r a t i ons i n individual organisms (Risebrough e t a1 . 1977; Luoma and Cloern 1982; Luoma e t a1 . 1985). With t h e i nc r ea s ing pub1 i c awareness and concern about contaminat ion and i t s e f f e c t s , g r e a t l y expanded programs a r e being proposed. The S t a t e of C a l i f o r n i a has e s t ab l i shed t h e non-profi t Aquatic Habi ta t I n s t i t u t e t o monitor and e v a l u a t e t he e f f e c t s of p o l l u t a n t d i scharge on San Francisco Bay (Ca1 i f o r n i a S t a t e Water Resources Control Board 1982). The National Oceanic and Atmospheric Administrat ion (NOAA) of t he U.S. Department of Commerce, as p a r t o f i t s long-term "National S t a t u s and Trends Program," i s c o l l e c t i n g sediments and bot - tom f i s h a t t h r e e s t a t i o n s a t each of fou r s i t e s in San Francisco Bay annual ly t o measure concent ra t ion of a v a r i e t y of contaminants (National Oceanic and Atmospheric Administrat ion 1986). This program wi 1 l be expanded t o inc lude c o l - l e c t i o n s of bottom f i s h , sediments , and b iva lves between t h r e e and s i x t imes per year f o r 2 y e a r s a t a number o f s i t e s throughout t h e bay t o measure t r a c e contaminant concen t r a t i ons and t o conduct bioassay experiments ( E . R . Long, National Oceanic and Atmospheric Adminis t ra t ion , S e a t t l e , MA; pe r s . camm. ) . Other agenc ies a r e planning add i t i ona l pol l u t an t - r e1 a t ed s t u d i e s (D.J. Baumgartner, U.S. Environmental P ro t ec t i on Agency, Newport, OR, p e r s . cornrn.; 5.U. Palawski , U.S. Fish and Wild1 i f e Se rv i ce , Sacramento, CW, yers . comm. ; S. E . Anderson, San Franci sco Bay Regional Water Qua1 i t y Control Board, Oak1 and, Ch, pers . comm. j .

5.3.1 Methods o f Evaluat ion

Two approaches have been employed t o study t h e e f f e c t o f p o l l u t i o n on benth ic organisms: t h e f i e l d survey and t h e 1 aboratory b ioassay .

F ie id populat ion survey a ~ g r o a c h . The r e s u l t s o f numerous surveys o f bay benthos dur ing t h e pa s t t h r e e decades, designed t o show the e x t e n t of changes t o t he b io t a near waste o u t f a l l s and harbors , have been of on ly l i m i t e d use in d e f i n i n g t he e f f e c t s of p o l l u t a n t d i scharge on ben- t h i c communities. Early s t u d i e s ( e . g . , F i l i c e 1959) demonstrated t h e dep re s s ive e f f e c t o f un t r ea t ed i n d u s t r i a l and domes- t i c waste on t h e d i s t r i b u t i o n and abundance of r e s i d e n t spec i e s . More r ecen t ly , some loca l e f f e c t s o f sewage s p i l l s (Cloern and Oremland 1983), o i l s p i l l s (Chan 1972, 1974), and poorly t r e a t e d i n d u s t r i a l d i s cha rges (Luoma and Cl oern 1982), which cause 1 ocal contami na- t i o n of i nd iv idua l organisms and occas iona l ly t h e l o c a l e l iminat ion of spec ies popula t ions , have been d i s t i n - gui shed. Fu r the r , nea r ly a1 1 r ecen t surveys i n harbors and near o u t f a l l s a1 so r epo r t t h e prevalence of animals t y p i c a l of d i s t u rbed envi ronrnents e l sewhere, such as o p p o r t u n i s t i c s p e c i e s of t h e polychaete genus C a ~ i t e l l a (e .g . , Figure 3 3 ) . There a r e , however, no d a t a t h a t sugges t a p rogress ive change i n spec i e s composition and re1 a t ive abundance among spec i e s during t h e p a s t t h r e e decades even though the amounts of wastes a r e presumed t o have s t e a d i l y increased because of popula t ion and i n d u s t r i a l growth (Nichols 1973). I t i s not c l e a r whether t h i s l a c k of pe r - ceived change means t h a t t h e r e has a c t u a l l y been no e f f e c t from p o l l u t i o n , t h a t p o l l u t i o n - r e l a t e d change has gone un- no t iced , o r t h a t we a r e unable t o d i s t i n g u i s h p o l l u t i o n - r e l a t e d change from the sometimes opposing e f f e c t s o f na tu r a l f a c t o r s .

There i s much ev idence from s t u d i e s elsewhere t h a t sediment contaminants may a f f e c t reproduct ion , growth, o r su rv iva l of i nd iv idua l s . Yet such e f f e c t s a r e a1 - most never d e t e c t e d i n q u a n t i t a t i v e populat ion surveys i n San Francisco Bay because t h e p o t e n t i a l l y important sources of v a r i a t i o n i n populat ion s i z e among sam- p l i ngs a r e numerous and d i f f i c u l t t o s epa ra t e . I t i s impossible t o d e t e c t , f o r example, whether observed seasonal va r i a - t i o n s in t h e i n v e r t e b r a t e popula t ions on a South Bay mudfl a t (Nichol s and Thompson 1985a) a r e due t o seasonal v a r i a t i o n s i n contaminant i npu t s from a nearby sewage t reatment p i a n t ( s e e Thonlpson e t a:. 1984, Luoma e t a1. 1985), t o na tu ra l physical d i s turbance of t h e sediment ( e , g . , windwave e r o s i o n ) , t o p r eda t i on , o r t o

in terspecif ic in t nificance of contamination t o popul a t i ons (as organisms or thei fec t s can be (Nichols e t a l . 1

.eractions. Thus the s ig - Com~ari ng poll uted versus control chronic, low-level s i t e s . One approach t o assessing e f fec t s

§an Francisco Bay benthic of waste eff luents i s t o compare benthic opposed to the individual community s t ructure (species occurrences, r t i s sues , in which e f - abundance, biomass, d ivers i ty , s imi la r i ty seen) remains uncertain indices, animal -sediment in teract ions) a t 986). an eff luent discharge s i t e with t ha t of a

Figure 33. Distribution and abundance of Capifella species from results of many quantitative surveys summarized by Hopkins (1986).

s i t e t h a t i s known t o be nea r ly i d e n t i c a l except f o r t h e absence of a p o l l u t a n t source. In a t y p i c a l example, samples c o l l e c t e d each season from Cas t ro Cove ( a s i t e contaminated with o i l , chemical , and domestic waste) were compared wi th samples from Gall inas Cove and t h e Corte Madera Ecological Reserve (F igu re 4 ) , s i t e s with s i m i l a r physical c h a r a c t e r i s t i c s , t o determine d i f f e r e n c e s i n community and populat ion i n d i c e s (CH2M-Hill 1982). As might be expected, t h e r e were s i m i l a r i t i e s and d i f f e r e n c e s i n community s t r u c t u r e among t h e t h r e e s i t e s . Some s t a t i o n s a t t h e contaminated Cas t ro Cove s i t e were found t o have fewer s p e c i e s ; a g r e a t e r abundance of C a ~ i t e l l a s p p . , S t r eb l o sp io benedic t i , and Pol ydora 1 i a n i ; fewer ep iben th i c c r a b s , shrimp, and f i s h ; and g r e a t e r m o r t a l i t y and h ighe r body burdens of hydrocarbons i n t h e marsh-dwell ing mus- s e l s than t h o s e from t h e con t ro l s i t e s . However, t h e r e s u l t s do no t n e c e s s a r i l y r ep re sen t t h e e f f e c t s of p o l l u t i o n a1 one. The l a r g e f l u c t u a t i o n s i n numerical abundance of i nd iv idua l spec i e s from one sampling d a t e t o another s t r o n g l y suggest t h e importance of o t h e r sources of v a r i a - t ion . Di f fe rences between s i t e s could have r e s u l t e d from d i f f e r e n c e s i n (1) sediment e ro s ion , resuspens ion , and depos i t i on t h a t would, i n t u r n , a f f e c t primary product ion and t h e food supply t o t h e benthos, a s well as reproduct ion , l a r - val r ec ru i tmen t , and mortal i t y ; ( 2 ) f reshwater i n t r u s i o n and res idence time over t h e mudflat and i t s p o s s i b l e e f f e c t on reproduct ion and m o r t a l i t y of ben th ic organisms; and (3) type , occurrence, and magnitude of p r eda t i on .

Numerous s i m i l a r s t u d i e s worldwide, although conducted us ing t he bes t a v a i l - ab l e procedures and p r a c t i c e s , have f a i l e d t o show unequivocal e f f e c t s of chronic nonle tha l contaminat ion o f ind iv idua l s (as i n Johansson e t a l . 1986) o r ben th ic populat ions because o t h e r f a c t o r s a r e e i t h e r over1 ooked, o r cannot be con t ro l 1 ed under na tu ra l f i e l d cond i t i ons . Sub1 e tha l e f f e c t s on reproduct ive capac i t y , reproduct ive success , growth, and behavior can probably be conc lu s ive ly demonstrated only through r i go rous ly con t ro l 1 ed exper i - r e n t s i n which other f a c t o r s t h a t cause s i m i l a r e f fec ts i n t h e f i e l d a r e con- t r o t led o r e: iainated,

Tissue-contaminant survey a p p ~ r o a c h . On t h e grounds t h a t t h e p o l l u t a n t conten t of t i s s u e s i n d i c a t e s t h e inc idence and

re1 a t i v e concen t r a t i ons of the substances i n t h e i r environment, mussels have been used worldwide as " s e n t i n e l organisms" f o r monitoring pol 1 u t a n t s i n coas t a l waters (Goldberg e t a l . 1978; Stephenson e t a l . 1979; National Academy of Sciences 1980; Goldberg 1986). However, t he use of body burdens as i n d i c a t o r s of p o l l u t i o n and s t r e s s t o t h e organism i s complicated by many f a c t o r s (Luoma e t a1 . 1985). T issue burdens of s i l v e r i n t h e clam Macoma ba l - t h i c a , f o r example, a r e h igh ly dynamic (F igure 3 4 ) , varying between seasons a s much a s f i f t y f o l d from t h e combined e f - f e c t s of ( 1 ) s ea sona l ly f l u c t u a t i n g metal load i n s u r f a c e runo f f , ( 2 ) varying spa- t i a l d i s t r i b u t i o n of meta l s i n t h e sediment, ( 3 ) an i n t e r a c t i o n between metal concent ra t ion and organism growth, and ( 4 ) an e f f e c t o f f reshwater inf low on metal b ioava i l abi 1 i t y through i t s e f f e c t on sediment-water chemistry o r r e s idence time of water ove r t h e mudflat (Thomson-Becker and Luoma 1985). Elevated t o l e r a n c e s t o t r a c e metals have been observed in popula- t i o n s of Macoma b a l t h i c a from metal- contaminated l o c a t i o n s in San Francisco Bay (Luoma e t a l . 1983), implying t h e importance o f adapt ive f l e x i b i l i t y t o t h e surv iva l o f some popula t ions . On t h e o the r hand, s t u d i e s near a South Bay sewage o u t f a l l i n d i c a t e t h a t phys io logica l s t r e s s caused by t r a c e metal contaminat ion occurs even in h igh ly adaptab le b iva lves during per iods when metal a v a i l a b i l i t y i s h ighes t (Johansson e t a l . 1986).

Body 1 e s i o n s , i n t e r n a l hi s topa thol ogi - cal abno rma l i t i e s , and high incidence of

Figure 34. Concentrations of silver in Macoma balthicafrorn the Palo Alto study site (from Luoma et al. 1985).

p a r a s i t e s and d i s e a s e s i n s t r i p e d bass caught in San Francisco Bay may be i nd i ca - t i o n s of p o l l u t i o n e f f e c t s on f i s h (Jung e t a1 . 1984). Although s i m i l a r h i s - topathol og ica l abnormal i t i e s have been repor ted in benth ic i n v e r t e b r a t e s i n the New York Bight s ludge d isposa l s i t e s (Rosenfield 1976), s i m i l a r a f f l i c t i o n s of ben th ic i n v e r t e b r a t e s from San Francisco Bay have not been r epo r t ed .

Laboratory bioassav versus f i e l d =- p l inq aimroach. B i o a s s a y ~ a r e con t ro l l ed experiments i n which t e s t organisms, under s t a t i c o r flow-through cond i t i ons , a r e subjected t o d i f f e r e n t l e v e l s o f par- t i c u l a r p o l l u t a n t s ( e . g . , Marine Bioassay Laborator ies 1984) . Because of method01 ogica l c o n s t r a i n t s , t h e t e s t con- d i t i o n s a r e o f t e n unna tura l f o r t he organisms ( e . g . , infaunal worms, clams, and c ru s t aceans held i n water without sediment o r held i n sediment t h a t i s u n - n a t u r a l l y c lean and devoid of o t h e r organisms), thus e l iminat ing pos s ib ly impo r t an t spec i e s i n t e r a c t i o n s . Experiment du ra t i ons a r e u sua l l y t o o s h o r t ( a few days t o a few weeks) t o d e t e c t chronic e f - f e c t s on a l l l i f e s t a g e s . Moreover, t e s t s have been appl ied t o on ly a few s e l e c t e d spec ies known t o be amenable t o l abo ra to ry experimentat ion, but whose responses may be q u i t e d i f f e r e n t from those of r e s i d e n t spec ies . F i n a l l y , one subs tance a lone may not produce t h e same r e s u l t s a s combina- t i o n s of subs tances , because of s y n e r g i s t i c o r a n t a g o n i s t i c e f f e c t s . Thus, i t i s not c e r t a i n , even in c a r e f u l l y designed s t u d i e s ( e . g . , McIntyre 1977) t h a t observed sub l e tha l o r l e t h a l e f f e c t s under bioassay cond i t i ons wi 1 l a1 so occur in t h e f i e l d . For t h e s e r ea sons , most s t ud i e s of p o l l u t a n t e f f e c t s i n San Francisco Bay have used t h e f i e l d approach (Nichol s 1973; CH2M Hi 11 1982).

Recent ly, b i oassays (exposure o f four t e s t organisms i n fou r s e p a r a t e procedures t o na tura l sediment from t h r e e t e s t s i t e s in San Francisco Bay) were combined with sediment chemistry measurements and i n - faunal community ana lyses ("sediment qua1 i t y t r i a d " ; Long and Chapman 1985; Chapman e t a l . 1986) t o t e s t t h e e f f i c a c y of such a program f o r use i n t h e U.S. Department of Commerce na t iona l coas t a l / e s tua r ine envi ronmentaf monitoring program ("National S t a t u s and Trends Program" ; National Oceanic and Atmospheric Administrat ion 1986). A1 though t h e s p e c i f i c causes of faunal d i f f e r e n c e s

among t h e s i t e s sampled wi th in t h e e s tua ry were not c l e a r l y determined, t he r e l a t i v e importance of anthropogenic f a c t o r s a t each s i t e (sediment contaminat ion, d e j e t e r i o u s e f f e c t s of sediments on t e s t a n ~ m a l s j could be i n f e r r ed from t h e combined t r i a d r e s u l t s : a waterway ad jacent t o t h e Ci ty of San Francisco was c l e a r l y the most pol lut ion-degraded s i t e , an open water s i t e in San Pablo Bay was t h e l e a s t degraded, and an Oakland o u t e r harbor s i t e was degraded t o an in te rmedia te degree. Chapman e t a1 . (1986) concluded t h a t a1 1 t h r e e measures (sediment chemis t ry , s e d i - ment bioassay, community a n a l y s i s ) a r e " . . . neces sa ry t o determine t he presence and measure t he degree of contamination and of synop t i ca l l y measured bi 01 ogi c a l e f f e c t s a t each s t a t i o n and s i t e . "

F ie ld bioassav. One v a r i a n t of t h e bioassay approach i s der ived from t h e f a c t t h a t organisms s t r e s s e d by p o l l u t a n t s o r high temperatures t y p i c a l l y show reduced capac i ty f o r growth and reproduct ion (Bayne e t a1 . 1982). The approach i n - volves exposing t e s t organisms in t h e f i e l d t o known environmental p o l l u t a n t s . Subsequently, t h e t o t a l amount of inges ted energy and t he f r a c t i o n r e t a ined by t h e organisms f o r somatic growth and amete production ( = scope f o r growth ~ S F G ] ; Warren and Davis 1967) i s measured in t h e labora tory . This combined approach has been used in San Francisco Bay focusing on pol 1 u t ion g rad i en t s (us ing mussels, Martin e t a1 . 1984), o r thermal s t r e s s g r a d i e n t s a t power p l an t e f f l u e n t s i t e s (us ing clams, Foe and Knight 1985b).

In p r i n c i p l e , t h e r a t i o n a l e behind SFG has m e r i t , but t h e methods used in San Francisco Bay s t u d i e s ( t h e l abo ra to ry measurements o f r e s p i r a t i o n and i nges t i on and t he s t a t i s t i c a l c a l c u l a t i o n s of SFG) can be c r i t i c i z e d f o r t h e l a ck o f pol l utant-body-burden da t a t h a t could be c o r r e l a t e d with p o l l u t a n t s a c t u a l l y present i n t he f i e l d and, t h u s , t h e lack of evidence t h a t d i f f e r e n c e s in SFG were indeed caused by p o l l u t a n t s o r s t r e s s . (Unfortunately, even when body burdens s f p o l l u t a n t s a r e known, one i s s t i l l no t s u r e whether observed i nc rea se s in body burdens of pol 1 u t a n t s and demonstrated lowering in SFG a r e r e l a t e d . ) Another source o f concern i s t h a t t h e t r a n s p l a n t a - t i o n of tes t crganisms t o and from pol lu ted o r nonpolluted s i t e s i t s e l f had an e f f e c t on SFG ( e . g , , i n t h e case of mussels, from Tomafes Bay ou t s ide San

Francisco Bay to San Francisco Bay; Martin et a1 . 1984)- Finally, if the results of SFG experiments were indeed valid for the test organisms, it does not necessarily f0170~ that the results apply to other species in the benthic community. Some species thrive in polluted harbors, perhaps through genetic plasticity (Luoma 1977) and/or through constant recruitment from outside the affected area.

5.3.2 Sewase-Induced Nutrient Enrichment

An important consideration in the management of estuaries is the degree to which they are affected by eutrophication and the often-associated decrease in bottom-water oxygen content. In many estuaries, elevated nutrient inputs from sewage-treatment plants and runoff result in nuisance blooms of phytopl ankton and macroalgae (e.g., Wi 1 kinson 1963; Sawyer 1965; Soulsby et al. 1978). Widespread macroalgal blooms have occurred in San Francisco Bay (Section 4.2.2) and, in the one instance when benthic samples were being collected simultaneously, caused mass mortality of infauna by cutting off oxygen supply to the sediment (Section 3 .2 .1 ) . However, a relation between enhanced macroal gal product ion and sewage- derived nutrient enrichment of the bay has not been demonstrated.

Waste nutrient-stimulated phytoplankton blooms that deplete dissolved oxygen, while important in many locations (e.g. Chesapeake Bay; Officer et al. 19841, also do not occur in San Francisco Bay despite high rates of waste-derived nutrient inputs (37 x 103 tons/yr nitrogen, 13 x lo3 tonslyr phosphorus; Russell et a1. 1982). Nutrient levels in South Bay are high each summer, par- ticul arly because wastewater from treatment plants is the major source of freshwater during summer and water residence time is high (Conomos et al. 1979). There have been no overt signs of eutrophication, however. One difference between San Francisco and Chesapeake Bays is the greater phytoplankton production in the latter (Peterson et al . 1985), leading to higher rates of bottom-water and sediment oxygen uptake (range of 8 to 106 mmo? O,/ m" / din Chesapeake Bay [ Kemp and Soy~ton 19811, versus !I to 46 i n Ssn Francisco Bay [Hamand et a7. 19851). The greater depth and water column stabil ity o f Chesapeake Bay are also majsr factors

contributing to summer bo'ttom-water anoxi a.

Although accidental discharges of raw sewage occasional Iy cause 1 ocal occurrences of oxygen depletion in San Francisco Bay (e. g. ? Cl oern and Oreml and 1983), the bay is generally well oxygenated throughout the year due to its shall ow depth, and wind- and t ide-i nduced mixing that keeps the water in close equilibrium with the atmosphere (Chapter 1; Hartman and Hammond 1985). Further, benthic grazing may significantly control the size of phytoplankton populations (Section 2.5. I ) , thus preventing the accumulation of critically 1 arge biochemical oxygen demand (Nichols et a1 . 1986). Cloern et a?. (1985) have shown that the most intense blooms are concentrated in the shallow areas of both the northern and southern ends of San Francisco Bay, where active grazing within the photic zone by the shallow-water benthos would be expected to be most intense. The limiting effect of wind-generated turbidity and vertical mixing upon the amount of available light for photosynthesis may also be a factor in preventing l arge phytopl ankton blooms (Cole and Cl oern 1984).

5.3.3 Effect of Pollution on Benthic Community Metabol i sm

The size of microbial and faunal populations in sediments and the activity of the total community as measured in terms of sediment oxygen uptake generally increase as the supply of organic matter to the bottom increases. Polluted waters with high organic loading show relatively high rates of oxygen consumption (Stein and Denison 1966; Pamatmat et a1 . 1973; Smith et a1 . 1974). On the other hand, the presence in sediments of noxious chemicals that affect respiration should be reflected by low benthic community metabol ism. Nonetheless, even grossly polluted areas such as the New York Bight sludge disposal site show high rates of oxygen uptake (Thomas et al. 19761, undoubtedly due to the amount of organic material being deposited there.

We do not know if the pollutants in San Francisco Bay sediments inhibit benthic com3u9;ty metabo!Ss~. A possible way of detecting such an effect indirectly might be to compare the San Francisco Bay data of Wammond et a1 . (1985) and Cole and

Cloern (1984) with Hargrave's (1993) em- p i r i c a l equa t ion re1 a t i ng benth ic oxygen consumption t o plankton primary product ion and mixed l a y e r depth (Sec t ion 4 .9) . The oxygen uptake a t t h e deeper s t a t i o n of Hammond e t a l . (19851, where annual ne t primary product ion i s 150 g carbon/m2 (Cole and Cloern 1984) and t h e e n t i r e 14-m deep water column i s well mixed, i s p red ic ted by t h e equa t ion t o be 120 l i t e r s 0,/m2/yr. By comparison, t h e annual average r a t e of ben th i c oxygen consumption ca l cu l a t ed from ac tua l measurements was 130 1 i t e r s O,/m2. I t would seem, t h e r e - f o r e , t h a t San Franc isco Bay does not d i f f e r from t h e o t h e r ecosystems i n regard t o t h e r e l a t i o n between benth ic metabolism and plankton primary product ion . Such a comparison i s tenuous, however, because we cannot r u l e ou t t h e p o s s i b i l i t i e s t h a t (1) Hargrave's (1973) equa t ion may have i n - cluded r e s u l t s from ecosystems a f f e c t e d by po l lu t i on , and ( 2 ) t h a t any i n h i b i t o r y e f - f e c t by p o l l u t a n t s on San Franc isco Bay benth ic community metabolism i s masked by an enhancing e f f e c t r e s u l t i n g from t h e u n - measured supply of o rgan i c ma t t e r represen ted by d e t r i t u s d e r i wed from such sources as sewage, wet1 ands, and benth ic mi c roa l gal product ion.

5.4 SEDIMENT BUDGET AND DREDGING

Each y e a r , l a r g e q u a n t i t i e s o f mud and sand a r e c a r r i e d i n t o San Francisco Bay from the dra inage bas in . This materi a1 has h i s t o r i c a l l y r ep re sen t ed a nuisance i n t h e maintenance of navigable channels and harbors . On t h e o t h e r hand, t h e r e a r e concerns about t h e e f f e c t s o f t he removal and depos i t i on of t h e dredged mater ia l on t h e bay 's l i v i n g r e sou rce s .

5 .4.1 Es t imates o f t h e Sediment Budqet

Although annual suspended sediment input t o San Francisco Bay v a r i e s with t h e r a t e of inf low from t h e two major r i v e r s , a long-term average i s e s t ima ted a t 8 x 106 m3 (Krone 1979). Est imates o f t h e f r a c t i o n of t h i s t o t a l t h a t i s discharged t o t h e ocean vary widely (4%, G i l b e r t 1917; 6%, Conomos and Peterson 1977; 50%, Krone 19791, demonstrat ing how 1 i t t l e we understand t h e bay 's sediment budget. Typica l ly , much of t h e w in t e r sediment load i n t he Sacramento-San Joaquin Rivers s e t t l e s ou t i n San Pablo Bay. IR summer,

wind waves and t i d a l c u r r e n t s e rode t h e previous1 y depos i t ed sediment and r e d i s t r i b u t e i t over a wider a r ea of northern San Franc isco Bay. In South Bay t h e shal low reaches seem t o be exper ienc- ing ne t e ro s ion , while t h e deeper channels a r e f i l l i n g ( F u l l e r 1982).

A t o t a l o f about 7 .6 x 186 m3 o f sediment i s dredged annual ly t o main ta in navigat ion channels i n San Francisco Bay (Sus t a r 1982). Thus, t h e average t o t a l amount o f sediment dredged from t h e bay each year i s about equal t o t he average annual sediment i npu t est imated by Krone (1979). Such an e q u a l i t y sugges ts t h a t , t o t he degree t h a t new sediment e n t e r i n g t he bay i s depos i ted o u t s i d e t h e s e chan- n e l s i . . , on t h e shal low s h o a l s ) , dredged mater i a1 i s sediment t h a t i s simply moving (by means of t i d a l , g r a v i t a - t i o n a l , and wind-driven water c i r c u l a t i o n ) from one p lace i n t h e bay t o another . Because d i sposa l o f most o f t h e dredged sediment occurs a t t h r e e open water s i t e s wi th in t h e bay (one s i t e a t t he western end of Carquinez S t r a i t , one near t h e southwestern end of San Pablo Bay, and one near Alca t raz I s land i n Cent ra l Bay; Fong e t a1 . 19821, i t i s a1 so probable t h a t some of t h i s r e c i r c u l a t i n g sediment i n - c ludes sediment t h a t has been dredged before.

5 . 4 . 2 E f f e c t s o f Dredsins on t he Benthos

The environmental e f f e c t s of dredging and d isposa l o f dredged sediments have been widely reviewed (O'Neal and Sceva 1971; Morton 1977; U.S. Army Corps o f Engineers 1977; DiSalvo 1978; Hirsch e t a l . 1978). The Corps o f Engineers has developed procedures f o r a s se s s ing t h e poss ib le impacts o f proposed new dredging in San Francisco Bay (Fong e t a f . 1982).

A t yp i ca l s c e n a r i o f o r dredging and i t s impacts i s a s fo l lows . During t h e course of dredging a s well a s t h e subsequent dumping, t h e water becomes t u r b i d with resuspended s i l t and c l a y , and d i s - solved oxygen i s consumed (JBF S c i e n t i f i c Corporation 1975; U.S. Army Corps o f Engineers 1976), a l though t h e e f f e c t s a r e usual f y g r e a t e r dur ing d i spasa l than dur ing dredging (3.S. Army Corps of Engineers 1976). The formation of a t h i c k suspension of dredged sediments ea l l ed f l u i d mud smothers some spec i e s but no t

others (Diaz and Boesch 1977). The resulting turbidity is re1 atively short- lived and probably no worse than the natural turbidity caused by winter river discharge, wind waves, and tidal currents. Laboratory studies of the effect of sediment suspensions on mussel s , cl ams , worms, and crustaceans {Peddicord et a1 . 1975) show that the mud-dwelling invertebrates would not be harmed by field suspensions noted during actual dredging operat ions in the bay (U.S. Army Corps of Engineers 1976). The depression of dissolved oxygen concentration is small and brief, probably because the bulk of the sediment rapidly sinks to the bottom before all the reduced substances can be oxidized. Advect ion and mixing quickly restore equilibrium conditions.

The dredged bottom, as well as the dumped deposit, are usually recolonized rapidly (McCauley et a1 . 1977). Moreover, the areas of dredging and deposition at any one time are small fractions of the total area of the estuary. Thus, the in- flux of organisms from the surrounding undisturbed areas can be rapid. Additionally, benthic communities normally subject to wave scour, high turbidity, and sediment redeposition rapidly recover from dredging and sediment disposal because the residents are rapidly r$produci ng oppor- tunistic species with short 1 ife cycles (01 iver et a1 . 1977). Because many of the species in San Francisco Bay remain reproductively active for much of the year (Section 3. I . ] ) , they can quickly colonize a newly exposed sediment surface. As a resuf t, San Francisco Bay benthos can be expected to be as resilient as that in other estuaries (Boesch et al. 1976).

5.4.3 Effects of C-ininat,ed Dredqed Sediments --- on Orqan i sms

Resuspension o f sediment, enriched relative to the overlying water, with a large variety of substances including waste chem~cals, could cause harm not only to benthos, but to plankton as well. However, resuspensisn of sediment deposits can remove as well as liberate substances, depending upon pH, oxidation-reduction level, re1 a t i v e concentrations in sediment and water, and ion-exchange capacity - - factors t h a t influence chemical processes such as acid-base balance, precipitation- di ssotution, complex formation, oxidation- reduction, and adsorption reactions (lee

1970). Sorption and release o f substances depend on complex dynamics invo7ving (1) diffusion of ions within sediment, (2) reactions in interstitial water, (3) hurnic binding forces, f 4) organi c/i norgani c coo:]- plexes, (5) nutrient mobilization, (6) reactions at the sediment-water interface, (7) mobility of cations from the sediment, and (8) water-sediment exchange reactions (Lu and Chen 1977).

San Francisco Bay sediments subject to dredging are contaminated with oil and grease discharged by refineries and other industrial plants (Citizens for a Better Environment 1983) and from urban runoff (Stenstrom et a1. 1984). These contaminants include numerous natural and petrol eum-derived hydrocarbons; fats, oil, and waxes of both natural and anthropogenic origin; fat-sol uble materials such as the polynuclear aromatic compounds DDT and PCB; and elemental sui - fur. Such substances differ in biodegradability as well as short- and long-term toxicity. Determining the effects of contaminated dredge spoils is usually difficult.

Shuba et a1 . (1978) concl uded from an extensive study of highly contaminated sediments from Puget Sound, Long Island Sound, New York Harbor, James River, and Mississippi River, that toxicity of contaminated sediments to test organisms in the laboratory does not positively indi- cate the same toxicity in the field. Hughes et al. (1978), in a comparative study of benthic and epibenthic species population density and community composition at a dredge disposal site and a control site in Elliott Bay, Puget Sound, Washington found that differences between sites could not be attributed to dredge spoils alone because many other factors (e.g., species migrations) were not considered in the sampling design.

In laboratory studies, mussels, clams, crabs, and snails from San Francisco Bay showed only minor uptake from sediment contaminated with oil and grease (DiSal vo et a1 , 1977). Anderl inS et al. (1975), in an effort to measure the biological uptake of sediment contaminants (primari ly heavy metal s) suspected of being mobil ired during dredging and disposal, compared body burdens of transpl anted mussel s and sediment macrofauna in dredge and disposal sites and in control sites. The organisms showed only

small changes in average metal concentra- 15.o~-- t ions .

I

In summary, studies t o date of the biological e f fec t s of dredging and dredge spoil disposal and the tox ic i ty of contaminants in the dredged material in San Francisco Bay, as el sewhere, have shown the following: (1) measured damage i s apparently limited in duration and area affected; ( 2 ) while toxicants in sediments are accumulated by infauna and other organisms, and these substances cause s t r e s s and behavioral changes during bioassay experiments, there i s no c lea r evidence to date tha t populations and communities have been adversely affected (e .g . , that recovery i s not complete); and ( 3 ) because d i f fe ren t species show d i f fe ren t e f fec t s from the same concentrations of toxicants, the only r e a l i s t i c experiments that apply t o a specif ic estuary are those involving resident species and t h e i r responses to pollutants occurring there .

5 . 4 . 4 Effects of Channel Dredqinq on Sa l t Intrusion

San Francisco Bay, 1 i ke other shallow estuar ies where shipping i s an important ac t iv i ty , requires maintenance dredging of midbay channels and harbors t o counteract the constant deposition of sediment. Increasing ship s i z e often necessitates fur ther deepening of channels.

Channel deepening has important implications fo r c i rcu la t ion and mixing of bay waters in the northern reach between San Pablo Bay and the Delta. In par- t i cu l a r , channel deepening in northern San Francisco Bay enhances upstream saltwater intrusion, thereby exacerbating the e f - fects of reduced r i ve r inflow. Case h i s to r ies of channel dredging to allow passage of deep-draft vessel s (e.g. , Rotterdam Harbor, van der Burgh 1968) and modeling s tudies (e .g . , Festa and Hansen 1976) have demonstrated t h a t increases in channel depth by a few meters can enhance gravitational c i rcula t ion and increase by many kilometers the upstream extent of saltwater intrusion (Figure 35). Increased saltwater intrusion has obvious consequences fo r agr icul ture in the western area of the Delta by threatening freshwater supplies and contaminating the soil with s a l t s . Such changes eventually resul t in 1 ong-term l and-use changes (Hackney and Yalverton, in press) .

0 20 40 60 80 100 120

Distance tkrn)

Figure 35. Relation between the depth of the river-estuary channel and the extent of landward intrusion of saltwater (0.05~100) under constant flow, from model results (adapted from Festa and Hansen 1976).

Increased sa1 twater intrusion a1 so leads to a1 tered species d i s t r ibu t ions tha t can have important secondary e f fec t s on the bay ecosystem. Hill and Kofoid (1927) recognized tha t i t was the combination of channel deepening and low r iver flows during the periods of 1913-14 and 1919-20 that led t o the spread of sa l ine bottom water in northern San Francisco Bay; t h i s , in turn, permitted the upstream migration of the introduced marine wood-boring shipworm Teredo naval i s . The invasion of t h i s pest species caused rapid and widespread destruction of the wood pi1 ings in bridges and piers i n the northern bay and Delta. Increased saltwater intrusion a1 so encouraged the upstream migration of estuarine benthic f i l t e r feeders into Suisun Bay during the 1976-77 drought, which resulted in a temporary s h i f t from a primarily pelagic food web supporting important f i she r i e s such as the s t r iped bass, to a benthic food web of l esse r economic significance (Sections 3.2.1, 5 . 2 ) .

Although i t i s not possible t o separate the e f fec t s of r ive r f l o w reduc- t ions and channel deepening on saf twater inirusicn, t h 2 r e su l t s fron s tud i es elsewhere suggest tha t the l a t t e r e f fec t cannot be ignored in discussions of the estuary9 s sag t bal ance.

CHAPTER 6. SHELLFISHERlES

The s h e l l middens t h a t do t t ed t h e sho re l ine of San Francisco Bay u n t i l t h e beginning of t h e present century (F igure 31) provided v i s i b l e evidence of t he importance of s h e l l f i s h t o t h e abor ig ina l i nhab i t an t s of t h e bay area before t he a r - r i v a l of Spanish s o l d i e r s and miss ionar ies (Nel son 1909). Composed 1 a rge l y of t h e bay mussel, Mytilus e d u l i s , and t h e bent - nosed clam, Macoma nasuta , i n t he northern p a r t of t h e bay, and the na t ive o y s t e r Ostrea l u r i d a i n t h e southern p a r t , t h e -- she l l middens were t h e res idences , r e fuse heaps, and bur ia l grounds of a c u l t u r e dependent t o a l a r g e degree on loca l shel l f i sh. Large-scale harves t ing of s h e l l f i s h by t h e post-Gold Rush s e t t l e r s continued i n t o t h e e a r l y yea r s of t h e present century u n t i l t h e s h e l l f i s h beds became fouled by human and i ndus t r i a1 wastes. Today t h e r e i s hope t h a t shel 1 f i s h e r i e s w i l l once again become prominent in San Francisco Bay.

6.1 EARLY HISTORY OF BAY SHELLFlSHERlES

6 . 1 , l Oysters

J . E . Skinner , in h i s review of t h e h i s to ry of San Francisco Bay's f i s h and wild1 i f e resources (19621, pointed out t h a t t h e bay "undoubtedly possesses t h e g r e a t e s t po t en t i a l o f any area in t h e S t a t e [Cal i f o r n i a ] f o r shel l f i s h c u l t u r e . " To t h e immigrants of t h e 185O's, t h e broad expanses of i n t e r t i d a l and shallow sub- t i d a l mudflats seemed ideal f o r s h e l l f i s h growing. Unfortunately, t h e na t ive spec ies were, f o r t h e most p a r t , not favored: "Native o y s t e r s [Ostrea l u r ida l , with t h e i r small s i z e , r a t h e r dark meat, and s t rong , coppery f l a v o r , d id not appeal t o e a s t e r n e r s accustonied t o t h t larger, whi te r , and mi lder oys t e r s " ( B a r r e t t 1963). Thus, although t h e n a t i v e o y s t e r was commercially harvested in San

Francisco Bay, no at tempt was made t o c u l - t i v a t e i t t h e r e (Bonnot 1935, Ba r r e t t 1963). The same spec i e s was imported by sh ip from Shoalwater Bay, Washington (now Will apa Bay), beginning in 1850, because i t was succes s fu l ly cu l tu red t h e r e . This e n t e r p r i s e , known a s t h e "Shoalwater Trade," provided most of t h e o y s t e r s f o r San Francisco u n t i l t h e l a t e 1 8 6 0 ' ~ ~ a l - though o y s t e r s from o the r P a c i f i c coas t l o c a t i o n s , e . g . , Mazatl an o y s t e r s from Mexico, were a l s o imported during t h i s period .

With t h e completion of t h e t ranscon- t i n e n t a l r a i l r o a d in 1869 came the opportuni ty f o r growing o y s t e r s in San Francisco Bay on a l a r g e s c a l e . The in - t roduct ion of t h e e a s t e r n o y s t e r s , Crassos t rea v i r q i n i c a (Sect ion 2 . 3 ) , c rea ted an indus t ry t h a t , by t h e 1 8 9 0 ' ~ ~ became the most important f i s h e r y in Ca l i fo rn i a . A t i t s peak in 1899 t h e i n - dus t ry produced near ly 3 x l o 6 1b of meat per yea r (Skinner 1962; Ba r r e t t 1963). Because t h e ea s t e rn o y s t e r never reproduced in commercial numbers in t he bay, t h e indus t ry depended on t h e con- t inuous import of e a s t e r n seed oys t e r s . Despite t h i s o b s t a c l e , San Francisco Bay remained the P a c i f i c coas t c e n t e r of e a s t - ern o y s t e r growing f o r many y e a r s .

Most of t h e o y s t e r beds were loca ted in t h e shallows of South Bay (F igure 36 ) ; t h e low s a l i n i t y and t h e high r a t e s of s i l t a t i o n in win ter ( p a r t i c u l a r l y during t h e period of hydraul i c mining; G i lbe r t 1917) apparent ly precluded good oys t e r growth and surv iva l in t h e northern pa r t of t h e bay. The beds were fenced with c lo se ly spaced s t a k e s t o keep out preda tors (Ba r r e t t 1963).

The f i r s t s i gns of problems i n t h e bay's oys t e r i ndus t ry appeared about 1900, a s t he o y s t e r s grew more s lowly, became t h i n and watery, and o f t e n were u n f i t f o r

Figure 36. Location of former oyster beds (Barrett 1963).

s a l e (Bonnot 1935). Observers a t the time (Nelson 1909) a t t r i b u t e d t h e d e t e r i o r a t i o n of t he oys t e r s t o t h e untreated human and indus t r i a l wastes being discharged i n t o the bay. By 1910, seed oys t e r s were no longer being imported from t h e East coas t , and by 1935 t h e oys t e r indus t ry in San Francisco Bay had c o l l apsed (Bonnot 1935; Skinner 1962). Bonnot concluded t h a t "Port ions of San Francisco Bay a re f r e e from sewage but g r e a t a r eas a r e contaminated and must be avoided. In c lean

areas where na t ive oys t e r s develop t o commercial s i z e , some e f f o r t may be made t o improve na tura l condi t ions but no g r e a t amount of time o r energy should be spent in San Francisco Bay u n t i l s a n i t a r y condi- t i ons improve" (Bonnot 1935).

While t h e l i v e na t ive oys t e r f e l l i n to d i s f avor , i t s s h e l l s a i d not . The ancient depos i t s of s h e l l material and assoc ia ted mud provided a ready source of t he ma te r i a l s used t o make cement

(calcium, magnesium, s i l i c a , a1 uminum, i ron , e t c . ) a s well as l i ve s tock and poul t ry feed (Hart 1966). Between 1924 and 1966, l a r g e - s c a l e dredging of t h e she l l depos i t s , l a r g e l y loca ted in South Bay (Figure 91, removed an est imated 30 x lo6 tons of s h e l l s (Hart 1966). The p rac t i ce cont inues t o t he present on a smaller s c a l e .

6.1.2 Clams and Mussels

The s h e l l d e p o s i t s in t h e Indian middens around t h e bay suggest t h a t t h e bay mussel, Mvti 1 us edul i s , was abundant enough in t h e e a r l i e r cen tu r i e s (Nelson 1910) t h a t a s much a s one - th i rd of t h e harvest was c a r r i e d upstream t o t h e v i l - 1 ages of t h e Sacramento-San Joaqui n River Delta (Cook 1946). In t h e upper, more recent l a y e r s of t h e s h e l l middens, t h e bent-nose c l am, Macoma nasuta , becomes prominent. Whether t h e gradual s h i f t from M ~ t i l u s t o Macoma r e s u l t e d from a change in t h e i r r e l a t i v e abundance o r a change in aboriginal food preference i s not known.

The Gold Rush immigrants did not con- s i d e r t he se n a t i v e spec i e s worthy of l a r g e - s c a l e commercial exp lo i t a t i on within the bay. Nonetheless , t h e bent-nosed clam, dug in l a r g e numbers i n South Bay by Chinese shrimp f i shermen, was common in the San Francisco markets in t h e decades following the Gold Rush (F i she r 1916). The bay mussel, Mvti 1 us edu1 i s , a1 so con- t r i b u t e d s i g n i f i c a n t l y t o t h e t o t a l mollusk landings from the bay in t h e l a t e 1800's (Skinner 1962). The acc identa l i n - t roduct ion of t h e e a s t e r n s o f t - s h e l l clam, & a rena r i a , sometime between 1869 and 1874 (Carl ton 1979a), led t o i t s gradual replacement of na t ive spec ies in t h e marketplace (F i she r 1916) and cont r ibuted t o a g r e a t l y expanded mollusk f i s h e r y . Fencing of t h e clambeds t o prevent preda- t i on by rays and f lounders g r e a t l y enhanced t h e sof t - she1 1 clam harvest (Bonnot 1932a). A t t he peak of t h i s f i she ry i n t h e 1888's and 1890's , between 1 and 3 m i l l i o n I b of meat were har - vested annual ly (Skinner 1962). The harvest gradual ly decl ined t h e r e a f t e r : between 1916 and 1935 i t ranged from 100,000 t o 300,000 1b p e r y e a r , then f e l l o f f rap id ly . By 1949 t h e ca tch was n e g l i - g ib l e ; and records were not kept t h e r e a f t e r (Skinner 1962).

The decl ine in t h e clam f i s h e r y was a t t r i b u t e d t o increas ing labor c o s t s t o

harvest t h e clams and t h e po l lu t i on o r f i l l i n g of clam beds (Bonnot 1932a; Skinner 1962; Wooster 1968a). Bonnot (1932a) noted t h a t some of t h e clam beds were "abandoned due t o i n d u s t r i a l wastes which a r e dumped i n t o t h e bay." During t h a t same yea r (1932) t he Ca l i fo rn i a S t a t e Board o f Publ i c Health e s t ab l ished a permanent quarant ine on clams in San Francisco Bay "by reason of sewage pol l u - t i o n . . . and consequential danger of typhoid f eve r and gas t ro -en t e r i t i s" (excerpt from Minutes of May 28, 1932). The general qua ran t ine was 1 a t e r rescinded (1934) and replaced with a quarant ine t h a t cavered only a few s p e c i f i c pol l u t ed loca - t i o n s within t he bay. In 1945 t h e o r ig ina l qua ran t ine was put i n t o t h e Cal i f o r n i a Department of Publ i c Health ad- m i n i s t r a t i v e code (apparent ly i n ignorance of the 1934 r e s c i s s i o n ) ; i n 1953, a t t h e request of a clamming company t h a t wished t o dredge f o r clams in t h e middle of t h e bay, t h e cod i f i ed quarant ine was i t s e l f rescinded (Jones and Stokes Assoc ia tes , Inc. 1977). Today, no general quarant ine of s h e l l f i s h i s in e f f e c t .

The Japanese 1 i t t l e n e c k clam, Tapes phi l iopinarum, a c c i d e n t a l l y introduced t o t h e west coas t o f North America with Japanese oys t e r s sometime in t h e 1930's and 1940's, was discovered in San Francisco Bay in 1946 (Carl ton 1979a). This spec ies t h r ived and became t h e focus of spor t harves t ing t h a t cont inues t o t h e present .

6 .1.3 Crabs

A t t he time of t h e Gold Rush, t h e market o r Dungeness c r ab , Cancer mas i s t e r , was i n c i d e n t a l l y co l l ec t ed from San Francisco Bay in f i s h ne t s . In t h e 1860's, c rabs caught i n t he bay were marketed in San Francisco (Dahlstrom and W i l d 1983). The bay's c r ab f i s h e r y dec l ined t h e r e a f t e r because t he c rabs were small and abundance was t o o low t o support t h e f i s h e r y ; by 1880 t h e f i s h e r y was forced o f f sho re (Dahlstrom and Wild 1983). The of fshore f i s h e r y remained an important indus t ry un t i l 1960 when a p rec ip i tous and permanent dec l ine occurred. The d e c l i n e is var ious ly a t t r i b u t e d t o a change i n ocean c? imate i . e . , increased water tempera ture an i n t e n s i f i e d currents! , predat ion by ha tchery- reared s i l v e r salmon Oncorhvnchus k i su t ch , and pol 1 u t ion (Wild and Tasto 1983). Some juven i l e s s t i l l use t h e bay a s a nursery and feeding ground.

6.1.4 Shrimp

Bay shrimp, Cranqon franciscorum, C. nisricauda, and C. nisromacul a ta , were f i r s t exploited by I ta l ian seine fishermen in 1869. These fishermen were soon put out of business by Chinese shrimp f i sher - men employing ancient Chinese techniques that included use of fine-meshed nets (Bonnot 1932b; Skinner 1962). The larger specimens were sold in local markets, but the bulk of the catch was dried and shipped to China (Bonnot 1932b). The loss of many juveniles of commercial f i sh species in the Chinese shrimp nets resulted in the imposition of closed seasons, r e s t r i c t i ons of the industry to limited areas of the bay, and l imita t ions on the amount exported (Bonnot 1932b). Despite the l imi ta t ions , the catch in 1929 exceeded 3 x lo6 1 b, then declined owing t o a lack of su i tab le markets. The fishery was revived on a small scale in 1965 t o supply ba i t fo r sportfishermen (Smith and Kato 1979).

6.2 PRESENT STATUS OF BAY SWELLFlSHERlES

6.2.1 Sport Harvestinq of Mollusks

Despite the poss ib i l i ty of contamina- t ion from wastes (par t i cu la r ly during winter when urban runoff increases and sewage treatment plants occasionally overflow) and the lack of o f f i c i a l authorization, sport harvesting of she l l f i sh from the bay's in te r t ida l beds continues (McAll i s t e r and Moore 1982). The primary focus of sport clamming in the bay i s the Japanese 1 i t t leneck clam, Tapes phi1 ippinarum, a1 though arenaria, Mvtilus edul is , and a variety of much less common species are taken as well. While Tapes i s collected primarily as food, a large percentage i s used as bai t by fishermen.

In 1967, Wooster (1968a, b) conducted the only known baywide survey of in te r - t idal she l l f i sh beds. He ident i f ied the major beds, including f i ve native oyster beds, and determined the abundance of individual species in each. He estimated a to ta l abundance of 21 x lo6 adult MJM, Tapes, and other assorted species i n beds baywide, an abundance suf f ic ien t to support 2 x 106 person-days of recreational shell f ishing per year.

Recent surveys of the most promising of the bay's she l l f i sh beds (Sutton 1978; Sutton and Jefferson Assoc. Inc. 1981; McAllister and Moore 1982) demonstrate the great potential fo r shel l f i s h harvesting i n the bay as well as the present importance of t h i s source of food t o some bay area residents. Large numbers of Tapes and occasionally are found in d i sc re te in te r t ida l beds, pa r t i cu la r ly along the eastern and western margins of central South Bay in the narrow band of rock, cobble, and broken concrete riprap along the base of dikes, p ie r s , and breakwaters (Figure 37). In other words, an "introduced" hab i ta t , in areas tha t formerly were marshes or open mudflats, provides the appropriate substra te fo r the introduced mollusk species t ha t const i tu te the bay's only clam f ishery. Much l e s s i s known about subtidal shel 1 f i sh popul a- t ions , a1 though various sampling e f fo r t s have shown tha t South Bay contains Tapes populations tha t might be commercially exploited (McAllister and Moore 1982).

6.2.2 Commerci a1 Harvestinq of Crustaceans

Although there i s no longer a Cancer maqis tercrab f ishery in the bay, two -

Figure 37. Breakwater af boulders, braken concrete, and cabbie that provides habitat and refuge for Tapes philippinarum and My8 arenaria.

o the r commercial c rus tacean f i s h e r i e s opera te i n t he bay: t h e b a i t shrimp and b r ine shrimp f i s h e r i e s . The bay shrimp, Cranqon franciscorum, C . n iq r i cauda , and C . niqromacul a t a , a r e comrnerci a1 l y f i shed - with beam t r awl s , p r imar i l y in Suisun and San Pablo Bays and t h e extreme south end of South Bay, t o provide b a i t f o r s t r i p e d bass and s turgeon s p o r t f i s h i n g (Frey 1971; Smith and Kato 1979). The small s i z e of t he se shrimp appa ren t ly l i m i t s t h e i r usefu lness a s food f o r human consumption.

The b r ine shrimp, Artemia s a l i na , i s abundant in t h e shal low diked ponds bor - der ing South Bay where s a l t i s produced by s o l a r evapora t ion . This s p e c i e s t h r i v e s under t h e hypersal i n e cond i t i ons of t h e s a l t ponds, and 250 t o 375 t ons a r e ha r - vested per yea r t o provide food f o r aquarium f i s h (Bay Conservat ion and Development Commission 1986). In addi - t i o n , b r i ne shrimp eggs from t h e s a l t ponds a r e shipped worldwide t o be hatched and used as f i s h food and f o r use i n labora tory research .

6.3 THE FUTURE OF BAY MOLLUSK FISHERIES

Although o y s t e r s have not been grown commercially i n t h e bay f o r many y e a r s , recent f i e l d t e s t s by t he Cal i f o rn i a Department of Fish and Game (McAl l i s te r and Moore 1982) and by t h e Morgan Oys te r Campany (unpubl . ) have shown t h a t o y s t e r s suspended above t h e bottom on racks would grow well enough t o permit t h e r e e s - tabl ishment of an o y s t e r i ndus t ry (Bay Conservation and Development Commission 1986). The major o b s t a c l e s t o commercial oys t e r growing i n t h e bay seem t o be (1) devef oping a s u f f i c i e n t l y 1 arge market f o r bay o y s t e r s t o r e t u r n t he investment r e - quired t o cover l a n d a c q u i s i t i o n and opera t iona l c o s t s , and ( 2 ) meeting h e a l t h s tandards with regard t o t i s s u e contamina- t i o n . Oysters grown commercially i n t h e bay would r e q u i r e depu ra t i on - -ho ld ing t h e o y s t e r s i n a c o n t r o l l e d c l ean -wa te r en-

v i roornent u n t i l cont an~i nants a r e reduced t o acceptab le l eve l s . Such hol ding f a c i l i t i e s a r e common worldwide wherever o y s t e r s a r e grown ad j acen t t o urban a reas (Jones and Stokes Assoc. , Tnc. 1977).

6 .3 .2 Clams

Commercial ha rves t i ng of clams from bay mudflats i s appa ren t ly i n h i b i t e d by high l abo r c o s t s a s soc i a t ed wi th d igg ing . Moreover, t h e l im i t ed s i z e o f e x i s t i n g beds would preclude 1 a rge - sca l e ha rves t - ing . Sport harves t ing i s expected t o cont inue d e s p i t e t he l a ck o f o f f i c i a l au tho r i za t i on (McAl l i s te r and Moore 1982).

Recommendations f o r enhancing t he spo r t shel 1 f i s h e r y f o r T a ~ e s phi7 i ~ p i n a r u m inc lude p lan t ing of hatchery-produced seed clams and en la rg ing t h e clam h a b i t a t by covering po t en t i a l 7y s u i t a b l e i n t e r t i d a l mudflats with an app rop r i a t e mix of cobble, g r a v e l , and shel 1 mater i a1 s (McAll is ter and Moore 1982).

6 .3 .3 The Threat of Po l lu t i on

Contamination of bay water , bottom sediments , and organisms by wastes remains t h e major concern prevent ing o f f i c i a l ap- proval of she1 1 f i sh ha rves t i ng . Great s t r i d e s have been made dur ing t h e p a s t 20 years in r e so lv ing many water qua1 i t y problems. The opera t ion of modern sewage t reatment f a c i l i t i e s around t h e bay has led t o t he near e l im ina t i on of incidences of low d isso lved oxygen, and t h e reduc t ion of col i form (human waste) b a c t e r i a t o very low l e v e l s i n most l o c a t i o n s dur ing most o f t he year . Occasional t rea tment p lan t ma1 func t ions do, however, sometimes cause contamination of some s h e l l f i s h beds. Contamination with v i r u s e s and with t r a c e organic and inorganic m a t e r i a l s i n i n - d u s t r i a l wastes p e r s i s t s and r ep re sen t s a po t en t i a l t h r e a t t o people who r egu l a r ly e a t bay s h e l l f i s h (Jones and Stokes Assoc. , Inc. 1977). Therefore, t he Gal i f o r n i a Department o f Heal t h Serv ices does not o f f i c i a l l y permit she l l f i s h i n g except under occas iona l 1y au thor ized , s t r i c t 1 y c o n t r o l l e d cond i t i ons as r e - quested by ? ocal governments.

CHAPTER 7. MANAGING BENTHIC RESOURCES

7.1 INTRODUCTION

We have described in t h i s p rof i l e the soft-bottom benthic environment in San Francisco Bay and have defined, where pos- s i b l e , the important features and processes tha t l ink the benthos with the r e s t of the es tuar ine ecosystem and with humans. I t i s c lea r tha t the benthos i s an important component of the estuary and i s a resource tha t has measurable economic value. The soft-bottom habi ta ts of estuar ies are places where both l iv ing and nonl iving organic matter accumulates (Chapter 4 ) and subsequently becomes food for diverse bottom-living primary consumers from bacteria to clams (Chapter 2 ) . The inconspicuous clams, worms, and small crustaceans l iv ing in the mud a t the bottom of the bay are a major source of food fo r abundant and diverse predators ( f i s h , sharks, rays, shrimps, crabs, and shorebirds) during a t l e a s t some part of the predators' l ives (Chapter 3 ) . Humans have a1 so exploited the productive bottom of the bay by harvesting both the primary consumers (c l ams, oysters) and secondary consumers ( f i s h ) . The potential fo r renewed mollusk f i she r i e s in the future (Chapter 6) has stimulated renewed in te r - e s t in the bay's protection and management (e .g . , McAllister and Moore 1982; Bay Conservation and Development Commi ssion 1986). We have also used macroinvertebrates , because of t he i r general ly sess i l e 1 i f es ty le , as measures of the degree to which the estuary shows evidence of human a l t e ra t ion (Chapter 5 ) . I n shor t , the value of the benthos t o an estuarine ecosystem i s much greater than i t s d i rect monetary value.

Concerns about the present condition of the estuary and about the potential for further change and possf ble deter iorat ion in i t s aes thet ic and economic values need t o be translated into good management pol ic ies and practices. However, because

of the divergent uses of and conflict ing demands on the bay, decisions are d i f - f i c u l t . Useof the bay as a s i t e fo r waste disposal conf l i c t s with the use of the bay as a source of food ( f i s h , clams). Use of former wetlands fo r garbage dumps and commercial developments conf l i c t s with aes thet ic and recreational values and eliminates wi ld l i fe habi ta t . In order t o develop appropriate policies and practices tha t can resolve such conf l i c t s , i t will be necessary, f i r s t , t o educate managers and users ( the public) about the recrea- t ional , economic, and aes the t ic values of the estuary, Second, i t will be necessary t o overcome the obstacles ( l imita t ions of s c i en t i f i c understanding, th rea t s posed by human ac t i v i t i e s , the lack of c lea r management pol i c ies and objectives, and the limited financial support for scien- t i s t s , educators, and resource managers) that prevent us from protecting and enhancing bay resources and maximizing the human benefits obtained from them.

7.2 PUBLIC PERCEPTIONS, USES, AND CONCERNS

Cit ies bordering the bay have his- t o r i cal l y 1 ocated t he i r refuse dumps near the perimeter of the bay. Additional debris col lects a t the edge of the bay by t i de and wind action. As a r e su l t , a v i s i t o r approaching the bay finds a d i s - turbed, often unat t ract ive s ight a t most points of access. Broken bo t t l es (a few dating to the previous century and thus providing modern archeological treasures fo r bot t le co l lec to rs ) , cans, refuse from fishing and pleasure boats, and automobile t i r e s (Figure 38) l i t t e r the shore. In par t icular , that portion of the mud bottom of the bay v i s ib le a t low t i de (about 15% of the surface area o f the bay, much of which i s muddy and d i f f i c u l t t o wa? k oa, and thus frequented by only a small number of clamdiggers) has been viewed as an eyesore and a smelly nuisance t o be Fil led

7.3 SCIENTIFIC BASIS FOR MANAGEMENT

7 . 3 . 1 Present Knowl edqe

Figure 38. A typical bay view (photograph courtesy of D.R. Hopkins).

and put. t o a more "use fu l " purpose. For tuna te ly , wi th in t he pas t two decades t h a t a t t i t u d e has been changing ( e . g . , Bay Conscrvat ion and Development Cornmi s s i on 1983).

Although most o f t he land above high water i s s t i l l fenced p r i v a t e o r publ ic land, ongoing e f f o r t s t o develop bayfront t r a i l s and parks a r e g r e a t l y expanding pub1 i c access . Addi t i o n a l l y , a growing number of pub1 i c educat ional f a c i l i t i e s loca ted around the shore of t he bay f e a - t u r e d i sp l ays and t r a i n i n g programs about thc natura l h i s t o r y of the bay and s u r - rounding a rea ( f o r l oca t i on maps of t he se f a c i l i t i c 5 , s e e Ray Conservation and Devclnpment Commission and I n s t i t u t e f o r Human Environment 1981). These f a c i l i t i e s & r e increas ing pub1 i c awareness of t he bay, i t s var ious h a b i t a t s , and b i o t i c com- rr~trni i .ies,

iherc i s publ ic concern t h a t f i s h and s h e l l f i s h , although s t i l l abundant in t h e bay, may not be s a f e t o e a t . Furthermore, there i s concern t h a t cant inued d isposa l of wastes as well a s increased d ive r s ion o f Freshwater away from t h e e s tua ry may lead t o unwanted changes o r dec l i ne s in the bay's b i o t a . Dealing wi th these cnn- cerns e f f e c t i v e l y r equ i r e s t h a t pol i cy makers and t h e pub1 i c have an app rop r i a t e leve l o f s c i e r t t i f i c understanding,

In t h e preceding s i x chap t e r s we have summarized t h e r e s u l t s o f severa l decades of ben th ic r e sea rch and monitor ing. In summary, we have a good general under- s tanding of many q u a l i t a t i v e a spec t s of benthic ecology. We know how individual benthic spec i e s a r e d i s t r i b u t e d around the bay, we have some idea of t h e i r general ecology, and we presume t h a t we know what they e a t and who e a t s them (Chapters 2 and 3 ) . We know t h a t t he benthos minera l izes organic waste, consumes microalgae perhaps t o t h e ex t en t t h a t i t c o n t r o l s nuisance qrowth, r e t u r n s e s s e n t i a l n u t r i t i v e ma te r i a l s t o t h e water column, and provides a major source of food f o r f i s h and aqua t ic b i r d s . We a l s o know t h a t t he benthos i s s e n s i t i v e t o human a c t i v i t i e s such as waste d i sposa l p r a c t i c e s (Chapter 5 ) . With t h i s background, we can draw t e n t a t i v e , qua1 i t a t i v e conclusions about probable r e l a t i o n s ( o r l ack of r e l a t i o n s ) between human a c t i v i t i e s and changes in the benth ic environment.

I t i s apparent in near ly every chap- t e r of t h i s p r o f i l e , however, t h a t t h e r e a r e major gaps i n our understanding. Our knowledge of t h e benthos i s 1 imited l a rge ly t o macrofauna (we know almost nothing about t he micro- and meiofauna of San Francisco Bay). Moreover, d e t a i l e d understanding of t h e macrofauna i t s e l f i s lacking in many a r ea s . We have very l i t t l e q u a n t i t a t i v e understanding of many of t h e phys ica l , chemical, and b io logica l processes t h a t determine t h e na tu re of t he benthic community a t any s i t e . I n par- t i c u l a r , we have only q u a l i t a t i v e understanding of t h e importance of physical processes !e .g . , f reshwater inf low, water c i r c u l a t ~ o n and mixing, p a t t e r n s of temperature and s a l i n i t y v a r i a t i o n s ) t o observed v a r i a t i o n s in t he d i s t r i b u t i o n and abundance of benth ic macrofaunal animals. Achieving q u a n t i t a t i v e under- s tanding i s c r i t i c a l i f we a r e t o c o r r e c t l y a n t i c i p a t e t h e e f f e c t s on t he benthic environment o f , f o r example, proposed development p r o j e c t a l t e r n a t i v e s .

Ue know l i t t l e about t he pathways and r a t e s of o rganic ma t t e r inputs t o t h e benthos and about what o r how f a s t t he animals e a t . We a l s o have l i t t l e s p e c i f i c

knowledge of the rate of p reda t i on by other invertebrates, fish, or birds on benthic species, and of the importance of predation relative to other sources of invertebrate mortal i ty. We do not know how critical the abundance of benthic invertebrates is to consumer populations such as fish. We do not know to what degree contaminants affect benthic populations or the consumers of those populations. Finally, we do not know if the benthos of the bay is changing with time as a result of increasing human infl uence.

Nonetheless, these kinds of information are critical to rational management of important benthic resources and of the estuarine system as a whole. Knowledge gained from other estuaries helps us to gain insight into San Francisco Bay processes and problems, but again, only in a qualitative sense. Management of an individual estuary such as San Francisco Bay requires quantitative understanding developed in that estuary.

7.3.2 Hindrances to Increased Under- standinq

The 1 imitations of our knowledge of benthic processes, like most other estuarine processes of the bay, stem largely from an historic reluctance to invest significant financial and human resources toward their study. This reluctance derives, in turn, from (1) the lack of public appreciation that the estuary, 1 i ke any natural resource, requires careful management to insure continuing benefits, and (2) the lack of substantial commercial fisheries that would focus attention on and f i nanci a1 investment in the estuary's 1 iving resources.

Among the specific factors that contribute to our lack of scientific understanding of the bay's benthic ecology are the following. First, there have been very few in-depth studies of the factors that regulate reproduction, growth, feeding, and mortality. Such studies would, for example, allow us to distinguish between the factors (e.g., physical disturbances, habitat character, biologi - cal interactions, food availabil i ty, predation) that affect abundances and di s - tributions of benthic species. Such knowledge is necessary if we wish, for example, to distinguish the effects of

pollutant loadings on shellfish growth, reproduction, and survival, or to enhance the productivity of bay shellfish.

The lack of in-depth studies is, in large part, a reflection of institutional priorities. Most governmental agencies that are concerned with the bay and its resources are not established to conduct basic research. They are, rather, resource management or regulatory in nature. The local institutions that strongly support basic research are few, and of these, the two largest (Stanford University and the University of California at Berkeley) have historically not been active in bay studies: with a few exceptions their aquatic scientists have not used San Francisco Bay as a primary study area (Hedgpeth 1979). A direct result is the lack of in-depth doctoral studies that are so important to the advancement of knowledge in any local area. Scientists affil iated with other local academic and research institutions who could address some of the unanswered questions have difficulty finding the necessary financial support for such studies.

Second, there is a lack of long-term, bay-wide monitoring that would provide quantitative evidence that the bay's benthic community is (or is not) changing over time. This is the case because few governmental agencies and academic institutions have been able to maintain consistent, on-going bay programs of any kind. The only two long-term benthic studies are limited to a single region of the bay (California Department of Water Resources 1986) and a single site (Nichols and Thompson 1985a). The first i s a re- quired monitoring program conducted by the Ca? ifornia Department of Water Resources as part of its permit to divert water from the Sacramento-San Joaqui n river system for irrigation. This program has ccn- sisted of semiannual benthic sampl ing at 11 stations in Suisun Bay and Delta between 1975 and 1979, and monthly sampling at 5 stations in the same area since 1980 (see California Department of Water Resources [I9863 for the most recent annual data report). The second study is a research investigation of the factors that contribute to short- and long-term change in the b ~ n t h i c cornunity at three statfans on one intertidal mudflat in South Bay (Chapter 3; Nichols and Thompson 1985a). The new Aquatic Habitat Institute

populations are being affected by human activities (Nichols et a i . 1986). Therefore, delays in implementing the studies necessary to prove or disprove cause and effect only delay further the imp1 ementation of rneani ngful corrective actions. In particular, we require in- depth studies that focus on well -defined problems (e.g., how much and by what mechanisms the contamination of small clams near waste outfalls affects the resident fish or bird species that feed upon them) in which the questions that are asked can be answered through field and 1 aboratory investigations.

Other issues requiring detailed study include (1) the role of the sediment (with its associated microbi a? community) in determining the levels of water column constituents (e.g., nutrients, waste contaminants); (2) the rates of sediment transport and deposition in various parts of the bay, how these rates are affected by dredging (both removal and disposal ) , and how these rates affect benthic species di stri but ions and abundances; and (3) the re1 ative importances of ri ver-borne detritus, sediment microbes, microalgae, and meiofauna as food for invertebrate species in various parts of the bay.

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-- - 4. TRk and SuMItia

The Ecology of t he Soft-Bottom Benthos of San Francisco Bay: A Community Prof i 1 e

i

7. Authotls) A Pwforming Organization Rapt. No.

Frederic H . Nichols and 9. p.fformin~ Or#anizatlan Name sod Addr*ss

U.S. Geological Survey 345 Middl ef i e l d Road San Francisco S ta te Universi t v :-- Men10 Park, CA 94025 P.O. Box 855

Tiburon, CA 94920

12. s rorlng Org~nhatlbn Name a d Address -7:: 1 l w i d -red

n. Department of the In t e r i o r Fish and Wildlife Service - idational Wet1 ands Research Center

----. - - - - - 1 . -- 15. Supplemmtey Notes

-- 16. Abstract (Limn: ZOO words)

Benthic species composition in San Francisco Bay r e f l e c t s the highly variable environment and t he predominance of introduced species. Species abundances vary grea t ly with season, re f lec t ing both i n t r i n s i c (reproduction/mortal i t y ) and e x t r i n s i c (sal in i t y , sedimentation, wind) fac tors . Larger year-to-year var iat ions appear associated with cl imatic pa t te rns and unusual c l imat ic events.

F i l t e r feeders predominate, with growth in some species linked t o the a v a i l a b i l i t y of microalgae. They may prevent the growth of nuisance algal blooms. Benthic invertebrates a r e , in t u r n , food fo r f i s h , aquatic birds , and humans.

Sediments and organisms a r e contaminated with wastes, b u t e f f e c t s a t the population level (declines in abundance) o r community level (changes in species composition) a r e not e a s i l y dis t inquished from natural v a r i a b i l i t y . Permanent e f f ec t s of freshwater diversion or dredging on benthic community s t ruc tu re have not been detected.

She l l f i sh harvest ing, once commerically prominent, i s r e s t r i c t ed t o spor t s digging o. two introduced clam species . The renewal of commercial oyster growing, now being considered, requires resolut ion of contamination issues.

The fu ture management of the e s tua ry ' s benthic resources depends on increased awareness of the need t o protect and enhance these resources, on increased commitments t o estuarine research, and on improved s t r a t e g i e s f o r overcoming human-induced problems.

benthos pollution es tuar ies sediments food chains she1 l f i s h

b. identlfieirn/Opcn.Ended Terms

benthic community dynami cs introduced species estuarine fauna San Francisco Bay estuary management

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The Ecology of the Soft-Bottom Benthos of San Francisco ... · Biologica1 Report 85(7.19) September...

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