Biological Services Program

FWS/OBS-81/15

May 1981 1

THE ECOLOGY OF INTERTIDAL
OYSTER REEFS OF THE SOUTH
ATLANTIC COAST: A COMMUNITY PROFILE

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Fish and Wildlife Service

U.S. Department of the Interior

The Biological Services Program was established within the U.S. Fish
and Wildlife Service to supply scientific information and methodologies on
key environmental issues that impact fish and wildlife resources and their
supporting ecosystems. The mission of the program is as follows:

t To strengthen the Fish and Wildlife Service in its role as
a primary source of information on national fish and wild-
life resources, particularly in respect to environmental
impact assessment.

• To gather, analyze, and present information that will aid
decisionmakers in the identification and resolution of
problems associated with major changes in land and water
use.

• To provide better ecological information and evaluation
for Department of the Interior development programs, such
as those relating to energy development.

Information developed by the Biological Services Program is intended
for use in the planning and decisionmaking process to prevent or minimize
the impact of development on fish and wildlife. Research activities and
technical assistance services are based on an analysis of the issues, a
determination of the decisionmakers involved and their information needs,
and an evaluation of the state of the art to identify information gaps
and to determine priorities. This is a strategy that will ensure that
the products produced and disseminated are timely and useful.

Projects have been initiated in the following areas: coal extraction
and conversion, power plants; geothermal , mineral and oil shale develop-
ment; water resource analysis, including stream alterations and western
water allocation, coastal ecosystems and Outer Continental Shelf develop-
ment, and systems inventory, including National Wetland Inventory,
habitat classification and analysis, and information transfer.

The Biological Services Program consists of the Office of Biological
Services in Washington, D.C., which is responsible for overall planning and
management. National Teams, which provide the Program's central scientific
and technical expertise and arrange for contracting bioloaical services
studies with states, universities, consulting firms, and others, Regional
Staffs, who provide a link to problems at the operating level; and staffs at
certain Fish and Wildlife Service research facilities, who conduct in-house
research studies.

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FWS/CCS-81/15
May 1981

THE ECOLOGY OF INTERTIDAL OYSTER REEFS OF THE
SOUTH ATLANTIC COAST: A COWUNITY PROFILE

by

Leonard f". Bahr
William P. Lanier
Louisiana State University
3aton Rouge, Louisiana 70803

Project Officer

Wiley V,. Kitchens

National Coastal Ecosystens Team

U.S. Fish and Wildlife Service

1010 Gause Boulevard

Slidell, Louisiana 70458

Performed for

National Coastal Ecosystems Team

Office of Biological Services

Fish and Wildlife Service

U.S. Department of the Interior

Washington, D.C. 20240

DISCLAIMER

The findings in this report are not to be construed as an official
U.S. Fish and Wildlife Service position unless so designated by other
authorized documents.

This report should be cited:

Bahr, L. M., and W. P. Lanier. 1981. The ecology of intertidal oyster
reefs of the South Atlantic coast: a community profile. U.S. Fish
and Wildlife Service, Office of Biological Services, Washington,
D.C. FWS/OBS-81/15. 105 pp.

PREFACE

This oyster reef comnunity profile is
the second in a developing series of pro-
files of coastal habitats. The purpose of
this profile is to describe the structure
and ecological function of intertidal oys-
ter reefs in the salt niarsh estuarine eco-
systeni of the Southeastern United States.
The intertidal oyster reef habitat, as
described here, is classified by Cowardin
et al. (1979) as occurring in the Carolin-
ian province, in the euhaline estuarine
system, in the intertidal subsysterri, in
the reef class, and in the riollusk sub-
class, v/ith the eastern oyster Crassostrea
vi rqinica as the dominance type.

This profile provides a handy refer-
ence which synthesizes the voluminous sci-
entific literature on oysters and focuses
on aspects of the less-studied oyster reef
community. The profile also points out
some of the many deficiencies in the cur-
rent level of understanding of the oyster
reef subsystem and of the entire estuarine
ecosystem. If additional research efforts
are thereby initiated, this profile vji 1 1
have been a success. (The observant read-
er will notice that in many instances
where quantitative data were not avail-
able, extrapolations from other communi-
ties or educated judgments, or both, were
necessary. )

The information in the profile will
be useful to environmental managers, re-

source planners, coastal ecologists, ma-
rine science students, and interested lay-
men who wish to learn about the oyster
reef community and its role in the coastal
ecosystem. The format, style, and level
of presentation should make this report
adaptable to a diversity of needs, from
the preparation of environmental assess-
ment reports to supplementary reading
material in college marine science
courses.

This profile proceeds from a descrip-
tion of the estuarine setting (Chapter 1),
to a discussion of oyster biology (Chapter
2), to a characterization of the oyster
reef per se (Chapter 3), to a discussion
of the development and role of the reef
system in the coastal ecosystem (Chapter
4). Chapter 5 is a summary of the role of
the oyster reef as expressed in three con-
ceptual models, and Chapter 6 includes a
brief synopsis of the first five chapters,
along with implications for management.

Any questions or comn:ents about or
requests for this publication should be
directed to:

Information Transfer Specialist
iJational Coastal Ecosystems Team
U.S. Fish and l.'ildlife Service
NASA-SI idell Computer Complex
ICIC Cause Boulevard
SI idell, LA 70458

CONTENTS

Page

PREFACE iii

FIGURES vii

TABLES viii

ACKNOWLEDGMENTS ix

CHAPTER 1. COMMUNITY PROFILE BACKGROUND AND OBJECTIVES; DESCRIPTION

OF THE COASTAL SETTING 1

1.1 Introduction and Objectives 1

1.2 General Characteristics of the South Atlantic Bight ... 3

1.3 Estuarine Producers 8

1.4 Estuarine Consumers 10

CHAPTER 2. FUNCTIONAL OYSTER BIOLOGY AND AUTECOLOGY 17

2.1 Taxonomy and Evolution 17

2.2 Oyster Reproduction and Development 20

2.3 Oyster Feeding, Digestion, and Assimilation 24

2.4 Stresses on Oyster Populations: Natural and Cultural. . . 28

2.5 Energy Summary 32

CHAPTER 3. OYSTER REEF DESCRIPTION AND SYNEC0L06Y 37

3.1 General Reef Description 37

3.2 Reef -Associated Macrofauna 42

3.3 Reef Community Energetics 48

3.4 Reef Predation 53

3.5 Colonial Aspects of the Reef Community 55

CHAPTER 4. OYSTER REEF DEVELOPMENT, DISTRIBUTION, PHYSICAL EFFECTS,

AND AREAL EXTENT 57

4.1 Reef Development 57

4.2 Distribution of Oyster Reefs in the Marsh Estuarine

Ecosystem 58

4.3 Physical Effects of Oyster Reefs on the Marsh-

Estuarine Ecosystem 61

4.4 Areal Extent of Oyster Reefs in the Coastal Ecosystem . . 62

CHAPTER 5. CONCEPTUAL MODELS OF THE INTERTIDAL OYSTER

REEF COMMUNITY 65

5.1 Objectives and Level of Resolution 65

5.2 Regional Level Conceptual Model 71

5.3 Drainage Unit Level Conceptual Model 71

5.4 Reef Level Conceptual Model 74

CONTENTS (continued)

Page

CHAPTER 6. SUMMARY AND MANAGEMENT IMPLICATIONS AND GUIDELINES .... 79

6.1 Summary and Oyster Reef Significance 79

6.2 Management Implications and Guidelines 82

REFERENCES 84

APPENDIX: OYSTER BIOENERGETICS 93

VI

FIGURES

Number Page

la The study area (South Atlantic Bight) extends from Cape

Fear, North Carolina, to Cape Canaveral, Florida 2

lb Tidal characteristics of the Atlantic and Gulf of Mexico

coasts 2

2 Sedimentary regions of estuary 6

3 A comparison of primary productivity for different kinds

of ecosystems 9

4 Model of energy flow in the Georgia salt marshes 12

5 Trophic spectrum of an estuarine community (Lake
Pontchartrain Estuary, Louisiana) 15

6 The distribution of Crassostrea virqinica 19

7 Anatomy of the oyster (Crassostrea virqinica) and diagram
showing the correct method of measuring the height, length,

and width of oyster shells 21

8 Transverse section of the dorsal part of an adult
Crassostrea virginica 22

9 A schematic representation of the rhythmic nature of the
feeding process and extracellular and intracellular
digestive mechanisms in oysters 25

10 Effects of turbidity on pumping rate 27

11 Effects of crude oil extract on Mytilus edulis carbon
budgets calculated for 100-mg mussels held at 31 /oo
salinity under summer conditions (15° C,215 ug C/liter). . . 31

12 Summary of energy flow through intertidal reef oysters ... 35

13 Diagrammatic section through oyster reef illustrating
relative elevation with respect to mean tidal levels and
corresponding fouling pattern on piling 38

14 Several generations of oysters (£. virqinica) growing
vertically on muddy bottom of Altamaha Sound, Georgia ... 39

15 Seasonal oxygen consumption of reef community 49

16 Seasonal energy partitioning estimates for the entire

reef community 52

17 Typical distribution of oyster reefs in small tidal

creeks 60

18 Comparison of two systems of concentrated consumers whose
survival depends on strong flows that bring in fuels and
oxygen and outflow wastes: (a) reef of oysters and
other marine animals characteristic of many estuaries;

(b) industrialized city 66

19 Three hierarchical levels of oyster reef organization. ... 67

20 Reef distribution in a single drainage basin, the Half

Moon River Estuary, Wilmington Island, Georgia . 68

21 Recent and historical reef distribution in the Duplin River
Estuary, Sapelo Island, Georgia 69

22 Regional level conceptual model and explanation of

symbols 72

23 Drainage unit level conceptual model 73

24 Reef organization conceptual model 75

vii

FIGURES (continued)

Number Page

A-1 Age-dependent annual production of soft tissue, shell

organics, gonad output, and respiration in an oyster .... 95
A-2 Seasonal variation in water temperature affecting oyster

reefs in South Carolina 95

A-3 Seasonal changes in size -frequency distribution of reef

oysters in Georgia 99

A-4 Seasonal changes in intertidal oyster size -frequency

distribution in South Carolina 100

A-5 Reef oyster height frequency relationship and cumulative

biomass curves 102

A-6 Schematic representation of percentage distribution of

potential food expressed in kilocalories for 1-year period

in 1 m^ of subtidal Crassostrea gigas population 104

TABLES

Number Page

1 General effects of man-induced (cultural) stress on

oysters 29

2 Pounds of meat and ex-vessel value (dollars) of oysters
harvested in four South Atlantic States from 1973-1975 . . 33

3 Macrofauna found in Georgia oyster reefs 43

4 Mean annual frequency distribution of reef macrofauna . . 45

5 Ranked biomass of 16 major oyster species or groups of
species and proportion of total macrofaunal biomass ... 45

6 Ranking of macrofaunal metabolic dominance based on

biomass 51

7 Community respiration in aquatic systems 54

8 Time scales relating ecosystem processes and components at
the three conceptual levels of oyster reef organization

and function 70

A-1 Conversion factors for oyster biomass units (intertidal

oysters) 98

A-2 Comparison of two sets of oyster reef energy parameters

collected within the study area 103

vn 1

ACKNOWLEDGMENTS

During the construction of this pro-
file it was necessary to request inforina-
tion from a variety of individuals, all of
whom were generous with their time and
suggestions. An incomplete list of those
who helped includes: Clay Adams, Jim
Bishop, Norman Buroker, Elgin Dunnington,
Skipper Keith, Kel Lehman, Bob Reimold,
and Tony Reisinger. Special thanks are
also due to Joy Bagur, Pauline Jolly, and
Francisco Ley, who assisted in the compi-
lation of the reference material; and to
Carolyn Lusk and Josie Williams, who
typed the manuscript.

The draft manuscript was reviewed for

its scientific content by Ed Cake, John
Hall, James Kirkwood, Stuart Stevens, Jim
Stone, Martha Young, and Tim Sipe. All
reviews were extremely helpful. Gaye
Farris and Elaine Bunce edited the manu-
script and were assisted by the efforts of
typists, Elizabeth Krebs and Daisy Single-
ton, and illustrator, Graham Golden.

Finally we would like to acknowledge
the unselfish assistance of Wiley Kitch-
ens, who ably administered this project.
Factual errors or faulty conclusions are,
of course, the sole responsibility of the
authors.

IX

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This view of the intertidal zone at Sapelo Island, Georgia, shows the position of
oyster reefs relative to the surrounding marshes and mudflats. Photo by Leonard
Bahr, Louisiana State University.

CHAPTER 1

COMMUNITY PROFILE BACKGROUND AND OBJECTIVES;

DESCRIPTION OF THE COASTAL SETTING

1.1 INTRODUCTION AND OBJECTIVES

Oysters occupy a unique status among
marine and estuarine invertebrates. As a
group, they are the most widely studied
and thus best known of all these animals,
primarily because of their universal
socioeconomic value. Some oyster species
are prized for their flavor and high qual-
ity protein; some are valued for their
pearls. Oyster shell calcium carbonate
has long been used as a building material;
e.g., "Tabby" houses of oyster shell were
once common in coastal Georgia and South
Carolina. Oyster shells are fed to chick-
ens and are even the source of supplemen-
tary calcium in tablets for humans. Oys-
ters of various kinds have been cultured
for centuries, so, in a sense, some spe-
cies qualify as domestic animals.

Much of the information gathered
about oysters has been collected by sci-
entists, but a significant amount has been
collected by observant laymen, natural-
ists, and aquaculturists. The objectives
of most of those observations, however,
were to learn to grow more oysters in
given areas faster and with fewer losses.
In the vast oyster literature, there are
relatively few "pure" ecological studies
that treat the oyster objectively as an
ecosystem component. For example, animals
associated with oysters are usually
referred to as "pest" species, as coyotes
are to sheepherders. But just as no orga-
nism is autonomous, and all organisms
operate within the framework of ecosys-
tems, so the oyster's importance extends
beyond its socioeconomic value.

The primary objective of this commu-
nity profile is to describe the function
of one species of oyster in a portion of
its habitat. More specifically, we present
a profile of a community associated with,
dependent on, and dominated by the Ameri-
can or eastern oyster, Crassostrea virgin-
ica (Gmelin). The study area comprises

the coast of the South Atlantic Bight be-
tween Cape Fear, North Carolina, and Cape
Canaveral, Florida, (Figure la), as dis-
cussed in Section 1.2.

Because the range of the American
oyster extends over a wide latitude (from
20° N to 54° N), the ecological conditions
encountered are diverse and the "oyster
community" is not uniform throughout the
range (see Section 2.2). The present de-
scription applies primarily and specifi-
cally to those populations of oysters and
associated organisms occurring in the in-
tertidal zone in the Southeastern United
States. In some portions of its range,
particularly in the area being described
(which has a large tidal range), the oys-
ter builds massive, discrete reefs in the
intertidal zone.

The vertical elevation of intertidal
oyster reefs above mean low water is max-
imal within the central Georgia coastal
zone, where mean tidal amplitude exceeds
2 m (2.2 m [7.2 ft] at Sapelo Island, ap-
proximately at the center of the South
Atlantic Bight). Approximate isopleths or
contours of the tidal range along the
Atlantic and gulf coasts are indicated in
Figure lb. Local areas experience tidal
variation because of local hydrologic
effects. The most extensive contiguous
oyster reefs occur in the South Carolina
coastal zone. Oyster reefs diminish in
size and significance south of Georgia and
north of South Carolina, but there are in-
tertidal patch reefs in northeastern
Florida and southern North Carolina. In-
formation reported in this document is
applicable to reefs from Cape Fear,
North Carolina, to Cape Canaveral, Flor-
ida, except as noted in the text.

The term oyster reef often is inter-
changed loosely with other terms for local
estuarine areas inhabited by oysters,
including oyster bar, oyster bed, oyster
rock, oyster ground, and oyster planting.

DIURNAL TIDE
One high water and one low water each
tidal day (about 24 hours, 50 minutes)

SEMIDIURNAL TIDE
Two nearly equal high waters and two
nearly equal low waters each tidal day

MIXEDTIDE

Two unequal high waters and/or two
unequal low waters each tidal day

Corange lines connect
points of equal tide
range. Numerals Indicate
the mean maximum
semimonthly spring tide'
ranges in feet

Direction of tide pro-
gression

Figure 1. (a) The study area (South Atlantic Bight) extends from Cape Fear,
North Carolina, to Cape Canaveral, Florida, (b) Tidal characteristics of
the Atlantic and Gulf of Mexico coasts (adapted from U.S. Geological Survey
1970).

Throughout this document, oyster "reefs"
are strictly defined as "the natural
structures found between the tide lines
that are composed of oyster shell, live
oysters, and other organisms and that are
discrete, contiguous, and clearly distin-
guishable (during ebb tide) from scattered
oysters in marshes and mud flats, and from
wave-formed shell windrows." Intertidal
reefs, as defined here, are also distinct
from natural and planted subtidal oyster
populations.

Ecologists' opinions differ as to
whether benthic communities (and some
other communities) exist as tightly inter-
active and interdependent systems of orga-
nislns, or whether such communities are
merely loose, chance associations to which
member species belong solely by geographic
accident. A proponent of the former argu-
ment long ago chose the oyster community
as an example of a biocoenosis, or inter-
active community (Mobius 1883). Whether or
not some species that occur in the oyster
reef community are dispensable, the Ameri-
can oyster is the "keystone" species (or
indispensable) in the sense intended by
Paine (1959) when he coined the term.

Specific objectives of this report
are as follow: (1) to synthesize a state-
of-the-art systems view of the oyster reef
community in the study area from existing
literature; (2) to address the effects of
various potential cultural and natural
perturbations on the oyster reef subsys-
tem, including pollution effects, physical
alterations to the estuary, and natural
changes; (3) to condense the above infor-
mation into conceptual ecosystem models
constructed at a level understandable by a
variety of readers, including those inex-
perienced in using ecological models.

The American oyster is the quintes-
sential or most typical estuarine animal.
It can tolerate a wide range of salinity,
temperature, turbidity, and oxygen ten-
sion, and therefore is adapted to the pe-
riodic and aperiodic changes in water
quality that characterize estuaries. Some
physiological and anatomical reasons for
its adaptive plasticity are described in
Chapter 2, which treats the autecology of
the oyster. Other aspects of the success
of the intertidal oyster are related to
its colonial lifestyle and mutual inter-
dependence and cannot be comprehended from

information gathered for individual oys-
ters. Chapter 3 is devoted to a discus-
sion of the entire reef community. Chap-
ter 4 discusses the reef's role in the
coastal ecosystem and Chapter 5 presents
three models expressing the reef's role.
Chapter 6 summarizes the other chapters
and gives implications for management.

This chapter's remaining sections de-
scribe the specific estuarine environment
of the oyster reef community. They in-
clude the physical, chemical, and biolog-
ical settings.

1.2 GENERAL CHARACTERISTICS
OF THE SOUTH ATLANTIC BIGHT

The geographic area on which this
profile primarily focuses is the portion
of the South Atlantic Bight, extending
along the southeastern coast of the United
States between Cape Fear , North Caro-
lina, and Cape Canaveral, Florida. This
section of the southern coastal plain ex-
hibits a continuum of change in coastal
morphology, but is characterized by exten-
sive lagoon-marsh systems and estuaries
bound at their eastern extent by barrier
island complexes. The morphology of coast-
al barrier island systems and extent of
the lagoon-marsh are the results of a com-
plex interplay of physical and biological
processes.

In general, this area can be consid-
ered a mixed-energy coast (Hayes 1975)
since coastal processes and morphologies
are determined by the varying influence of
both waves and tides. Wave and tidal con-
ditions in this area are largely a func-
tion of the changing profile of the inner
continental shelf (Hayden and Dolan 1979;
Hubbard et al. 1979). Average wave heights
decrease from a maximum of 1.2 m (4 ft)
along the North Carolina coast to a mini-
mum of 0.1 m (0.5 ft) along the central
Georgia coast (Hubbard et al. 1979). Where
the shelf is broad, nearshore wave heights
are reduced through frictional loss caused
by shoaling on the ocean floor shelf.

Shelf width, combined with the arcu-
ate shape of the coastline, also influenc-
es tidal range. The southern coast of
North Carolina is classified as a micro-
tidal coastline (Davies 1964), with semi-
diurnal tides that range between 0 and 2 m

(0-6.5 ft). Tides at ^lasonboro Inlet on
the southern coast of North Carolina range
from 1.2 m (4 ft) to 1.4 m (4.5 ft) for
mean and spring conditions, respectively
(Vallianos 1975). Wind and wave processes
are the principal forces dictating coastal
morphology in microtidal coastal systems
(Hayes 1975). Barrier islands in North
Carolina tend to be long and narrow, and
they contain relatively few tidal inlets.
Lagoon-marsh systems are usually narrow
(1.5 km or 0.6 mi), shallow, and densely
vegetated (Cleary et al. 1979).

Farther south in South Carolina and
Georgia, the coastal system has been clas-
sified as mesotidal (Davies 1964), having
a tidal range between 2 and 4 m (6.5 and
13 ft). This coastline is characterized
by short (20 to 30 km or 12 to 19 mi) bar-
rier islands, with a wider central portion
and narrow ends broken by numerous tidal
inlets. In response to the higher tidal
range, larger areas of lagoon-marsh are
broken by extensive and complex networks
of tidal drainage channels. Tidal inlets
between barrier islands tend to be rela-
tively deep (>10 m or 34 ft) and are
flanked by extensive bars and spits.

Estuaries and lagoons with associated
marsh, mudflat, and tidal drainage net-
works compose the dominant habitat of the
American oyster, £. virginica, in the
Southeastern United States. The term estu-
ary from the Latin aestus, meaning tide
(Schubel 1971), has been defined in vari-
ous ways. Geologists tend to accept the
strictly physical interpretation of Prit-
chard (1967), who defined an estuary as "a
semi-enclosed coastal body of water which
has a free connection with the open sea
and within which sea water is measurably
diluted with fresh water from land drain-
age." A broader, more ecological defini-
tion proposed by Cowardin et al. (1979) is
"deep-water tidal habitats and adjacent
tidal wetlands which are usually semi-
enclosed by land, but have open, partially
obstructed, or sporadic access to the open
ocean and in which ocean water is at least
occasionally diluted by fresh water runoff
from the land." In this paper we define
estuaries even more broadly to include all
the ecological subsystems that interact to
form the coastal marsh-estuarine ecosys-
tem. In other words, to quote Odum et al.
(1974), "It is the ecosystems rather than

the estuarine waterbodies that are dis-
cussed ...here.

Pr.
waterbod
types

'itchard (1967) subdivided estuarine
)dies into four geomorphological

„^ , (1) drowned river valleys; (2)

fjord-type estuaries; (3) bar-built estu-
aries; and (4) estuaries produced by tec-
tonic processes. All southeastern coastal
plain estuaries fall into either the bar-
built or the drowned river valley estua-
rine types.

General Estuarine Hydrography

Water circulation patterns are of
primary significance in determining the
physical and chemical conditions of the
estuarine ecosystem. Water circulation
strongly influences salinity, but it also
directly influences sedimentation pat-
terns, turbidity, temperature, and nutri-
ent conditions. Estuaries with signifi-
cant riverine sources of low salinity
water are distinctly different in form and
hydrographic character from those without
such sources (Oertel 1974).

Classifications of estuarine water
circulation patterns are based largely on
the relative magnitude of either riverine
or tidal influence (Ketchum 1951; Stommel
1951; Pritchard 1955, 1967, 1971; Bowden
1967) in conjunction with the geomorphol-
ogy of the estuarine basin (Schubel 1971).
Estuaries with large riverine sources of
fresh water show a well-defined vertical
salinity stratification. Fresh water over-
rides higher density salt water and forms
an upper, freshwater layer. The entrain-
ment of salt water from the lower layer
into the upper, freshwater layer through
eddy diffusion results in the mass move-
ment of the saline bottom layer into the
estuarine basin (Schubel 1971). This
mechanism creates the salt-wedge type es-
tuary as described by Pritchard (1971). A
partially mixed estuary occurs when the
tidal flow is sufficiently strong to pre-
vent the river from dominating the circu-
lation pattern (Schubel 1971). Turbulence
generated by the movement of the saline
bottom layer results in increased vertical
mixing and moderate salinity stratifica-
tion (Pritchard 1967). Many southeastern
estuaries with relatively large freshwater
sources (e.g., Altamaha and Ossabaw Sounds
in Georgia and Charleston Harbor in South

Carolina) fall into this second, partial-
ly mixed classification at least season-
ally.

Most estuaries in the study area are
classified as vertically homogeneous
(Pritchard 1967, 1971; Schubel 1971),
where tidal mixing is the dominant physi-
cal process. These systems receive fresh
water primarily though local precipitation
via tidal creek drainage systems particu-
larly during spring floods. Sapelo Sound,
Georgia, and the lagoon-marsh complex ad-
jacent to North Inlet, South Carolina
(Finley 1975), are two examples of verti-
cally homogeneous systems. Lagoon-marsh
complexes in southern North Carolina are
not fed by major streams (Cleary et al.
1979); therefore, they can also be consid-
ered vertically homogeneous.

In estuaries not directly influenced
by large riverine sources, estuarine cir-
culation patterns are largely determined
by tides, wind, and by the water storage
capacities of lagoon-marsh complexes
(Oertel 1975). The lagoon-marsh complexes
in Georgia, for example, are extensive and
average 6,5 to 7.5 km (4.0 to 4.6 mi) in
width. These areas store large volumes of
water during high tide, and during tidal
drainage they contribute significantly to
water circulation and nutrient exchange
within the estuarine ecosystem. These
large lagoon marshes generally occupy a
major portion of the watershed of the es-
tuarine basins, and therefore direct rain-
fall is the major source of freshwater to
these sytems (Tom Williams, Clemson Uni-
versity, Georgetown, South Carolina; pers.
comm. )

Estuarine Sedimentation

The origin of sediments in estuaries
and the processes that affect their dis-
tribution and deposition have been the
subject of extensive research and scien-
tific debate for over 25 years (Guilcher
1967). Estuarine sedimentation patterns
are complex and influenced by tidal cycle,
wind direction and duration, waves, sea-
sonal riverine flooding, water storage
capacity of lagoon-marsh complexes, and
sediment availability. The biological
animal-sediment interactions (bioturba-
tion) and chemical factors are also impor-
tant (Howard 1975). These factors may vary

continuously in space, time, and intensity
(Oertel 1974).

The processes of sedimentation can
best be understood if the estuarine system
is divided into three parts, based on gen-
eralized physical and hydrographic charac-
teristics: (1) the lower sound and inlet
entrance; (2) the middle region of the es-
tuary, including the main rivers feeding
the sound; and (3) smaller tidal creeks
draining the marsh complex. Naturally oc-
curring oyster reefs can be found in each
of these main zones in the study area. The
three estuarine sedimentation zones are
illustrated in Figure 2.

The area of the lower sound and inlet
entrance is influenced primarily by marine
processes. Wind-wave and tidal ly generated
currents exert the greatest influence in
the lower sound, creating a relatively
high energy sedimentary system. Where a
sufficient sediment supply is present,
this area is characterized by medium- to
coarse-grained and commonly cross-bedded
sands. Where the lower sound is less in-
fluenced by strong tidal currents, bottom
sediments consist of a mixed medium- to
fine-grained muddy sand. These sands be-
come progressively finer grained and in-
terbedded, or mixed with mud farther in-
land. This is particularly common in estu-
aries without fluvial sources of coarser-
grained sediment. Near the mouth of the
sound, influence of the adjacent shoreface
is indicated by the increasing grain size
and higher energy bedforms, sand ripples,
etc. (Mayou and Howard 1975). Sandflats
and mudflats frequently characterize the
intertidal margins of the lower sound.

In estuarine systems characterized by
large riverine freshwater input, the ver-
tically stratified lower sections of the
estuaries become natural traps for fine-
grained sediment (Schubel 1971). Fine-
grained sediment transported in the upper
freshwater layer frequently will settle
into the lower saline layer and then be
carried back inland. Suspended sediment
may, therefore, be transported back and
forth many times within the lower section
of an estuary before it is finally depos-
ited (Postma 1967).

The middle region of the estuarine
sedimentary environment includes the

sssm

SCALE

:/

2 km

ZONE 1

ZONE 2

ZONE 3

0
0

0
0

MARSH

LOWER SOUND AND INLET ENTRANCE

UPPER SOUND AND MAIN RIVER MOUTHS

MAIN RIVERINE FRESH WATER SOURCE

TIDAL CREEKS

UPLAND

Figure 2. Sedimentary regions of estuary.

uppermost portion of the sound and the
main rivers feeding the sound. This zone
is influenced by both marine and riverine
processes. Bottom sediments in the upper
reaches of the estuary are characteristi-
cally muddy sands or interbedded fine-
grained sands and muds. Farther inland,
if the river transports a significant
amount of coarse-grained material, bottom
sediments contain a decreasing percentage
of mud (Dorjes and Howard 1975). Turbid-
ity levels are generally higher in this
zone (the middle region) during all por-
tions of the tidal cycle (Day 1951; Howard
et al. 1975). These higher turbidity lev-
els in part reflect the fact that tidal
currents (especially ebb currents) attain
the highest velocities in the middle re-
gions of the estuary before they are
slowed in the open sound. The importance
of turbidity to oyster populations will be
explained in Section 2.3.

The complex network of smaller tidal
creeks that drain extensive areas of salt
marsh forms the third division of the es-
tuarine sedimentary environment. Tidal
creeks exhibit highly sinuous channel pat-
terns; laterally migrating point bars on
the convex inner sides form depositional
banks. The concave outer banks of tidal
creeks are areas of net erosion, where
water currents attain their highest veloc-
ities. This estuary zone can be classi-
fied as a low-energy, sedimentary environ-
ment. Current velocities in tidal creeks
depend on the extent of marsh drainage
area. Fine-grained mud-silts and, less
frequently, fine sands are the most common
bottom sediments. Despite the relatively
fine grain size of bottom sediments in
tidal creeks, the bottom includes all gra-
dations, from extremely soft and organi-
cally rich to hard mud and clay (Galtsoff
and Luce 1930). The degree of bottom sed-
iment consolidation is a function of the
interaction between depositional and ero-
sion forces. Hard mud bottoms form in
areas where tidal creeks erode into con-
solidated marsh sediment.

Physico-Chemical Environment

The chemical environment of the estu-
arine ecosystem is strongly influenced by
local hydrography. The three general divi-
sions (Figure 2) of the estuarine system
used in the discussion of sedimentation

also provide a convenient framework for a
discussion of the chemical environment.

In the study area, estuaries are
characterized by highly variable lateral
and vertical salinity gradients. Within
any particular estuary, however, salinity
trends are best described by the degree of
vertical mixing taking place between fresh
and saline water masses. Three relatively
well-defined salinity zones exist in the
majority of estuarine systems: (1) a
stable, well-mixed, and marine-dominated
lower zone; (2) an unstable intermediate
zone where large changes in the vertical
salinity gradient occur with each tidal
cycle; and (3) a stable upper region domi-
nated by riverine fresh water influence
(Howard et al. 1975). The juxtaposition of
these three zones depends upon the inter-
action and relative magnitude of riverine
and tidal influences. In the lower sound
and inlet entrance, corresponding to zone
1, mean salinities are high, ranging from
approximately 20 °/oo (parts per thousand)
to 32 °/oo, and the water column tends to
remain well mixed throughout the tidal
cycle. In estuaries receiving large river-
ine inflows, the well-mixed, high-salinity
zone may be displaced seaward several kil-
ometers (Oertel 1974). The upper sound in
the vicinity of the river mouths is influ-
enced by both marine and riverine process-
es. Salinity in this region varies, rang-
ing from 5 °/oo to over 20 °/oo, and
strong vertical salinity gradients are
common. Upstream of the river mouths
(zone 3), salinities reflect riverine in-
fluence. The water column remains well
mixed at all times, and salinities vary
from 0 °/oo to 10 °/oo. Salinity varia-
tions in marsh tidal creeks correspond to
that of the tidal water mass flooding the
marsh. As might be expected, these values
are lowered significantly during periods
of local precipitation in the marsh and
resultant runoff from adjacent uplands.

In general, thermal mixing of estua-
rine water masses occurs rapidly (Oertel
1974). Hence, over most of the lower
sound, vertical temperature gradients in
the water column are not pronounced
and are subject to daily fluctuations
(Oertel 1974). In summer, lower tempera-
ture ocean waters have a cooling influence
on the estuary. Water temperatures in
marsh creeks are slightly higher during

ebb tide, the result of solar heating in
the marsh during the tidal excursion over
dark sediments with low albedo (reflec-
tance).

Dissolved oxygen concentrations gen-
erally increase from the upper, riverine-
dominated portion of the estuary to the
lower sound and inlet. This pattern close-
ly parallels that of salinity. Howard
et al. (1975) found that during the summer
dissolved oxygen values ranged from 4 to 6
microliters/liter for a portion of the
Ossabaw Sound, Georgia. These relatively
low values may reflect the consumption of
oxygen during the oxidation of organic de-
tritus in suspension in the upper section
of the estuary. Frankenberg and Wester-
field (1968) reported that the dissolved
oxygen levels in estuarine waters in
coastal Georgia were extremely sensitive
to sediment disturbance; during the summer
the oxygen demand of a single milliliter
of disturbed sediment could deplete the
dissolved oxygen contained within 986 ml
of water.

Oertel (1976) described large tempo-
ral and spatial variations in turbidity in
estuarine waters. These variations relate
to riverine input, local resuspension of
bottom sediments by tidal scour and waves,
and trapping of fine-grained sediments in
the lower portions of estuaries (Schubel
1971). Turbidity is greater in the upper
reaches of the estuarine system than
either farther upstream in the source
river or farther seaward. This zone has
been termed the "turbidity maximum" by
Schubel (1968). Oertel (1976) found sus-
pended sediment concentrations in the up-
per Wassaw ranging from 9.6 mg/liter to
585.6 mg/liter, averaging 46.6 ng/liter.
Higher levels of turbidity were measured
during spring tides. In tidal creeks, tur-
bidity increases significantly during per-
iods of local rainfall when the marshes
are exposed at low tide (Settlemyre and
Gardner 1975). Oertel (1976) found a con-
sistent inorganic-organic ratio in sus-
pended sediments in the upper estuary,
averaging 70% inorganic material and 30%
combustible organic detritus.

1.3 ESTUARINE PRODUCERS

The estuary is perhaps best known
ecologically for its typically high net

primary productivity. The productivity of
estuarine systems relative to other eco-
systems is illustrated in Figure 3. A de-
tailed explanation of the high annual net
productivity in southeastern estuaries was
presented by Schelske and Odum (1962).
They listed five essential factors: (1)
tidal currents; (2) abundant nutrients;
(3) rapid turnover and conservation of
nutrients; (4) three separate groups of
producers; and (5) year-round productiv-
ity. Factors 4 and 5 ensure that primary
production occurs throughout the year;
therefore, energy and nutrient sources are
optimally exploited and net production is
maximized. The three primary producers
discussed by Schelske and Odum (1962) are
emergent macrophytes, phytoplankton, and
benthic algae. Another group recently has
received scientific attention: chemosyn-
thetic bacteria (Howarth and Teal 1979).
Each group is briefly discussed below.

Emergent Macrophytes

The marsh-estuarine complexes within
the study area are characterized by broad
expanses of salt marshes dominated by two
marsh grass species which compose a major
portion of the annual primary production
of these systems. These are the saltmarsh
cordgrass (Spartina alterniflora) and the
black needlerush (Juncus roemerianus).
Spartina is dominant overall, and large
continuous stands of this plant occur be-
hind the barrier islands (Pomieroy and
Wiegert 1980). The annual production cycle
of these marshes peaks in late summer,
followed by a long period of decay and
gradual export of dead vegetation (detri-
tus) into waterbodies or incorporation
into peat deposits within the marsh.

In terms of overall primary produc-
tion, the emergent macrophytes are consid-
ered to contribute a major portion of par-
ticulate carbon to the estuarine ecosys-
tem. Pomeroy and Wiegert (1980) reported
that Spartina production makes up 79% of
the particulate organic matter annually
produced by the entire marsh estuarine
ecosystem. Spartina also produces dis-
solved organic matter that leaches into
the water column during each tidal inunda-
tion. This leachate is thought to contri-
bute significantly to the total carbon
budget of the estuarine ecosystem (Turner
1978).

5 4
>.

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I 2

>

T3
O
O.
>

E
a

5 to 15 .

/is

Mm

/

/

1.5 to 5

z/

^*^

X).3 to 1.5

.^^'

1 to 1.5

0.3

-jT

,-

0.3

1

i^ ^

„.^

^A

-miWiihUiMa

t^jg^^^j -J- —?-,-;

^^^^^^

Desert Dry agriculture Moist

Estuarine Coastal Open ocean

Figure 3. A comparison of primary productivity for different kinds of ecosystems
(adapted from Teal and Teal 1969).

Estimated annual net production by
emergent nacrophytes in the study area has
been reported at 980 gC/mVyr, when pro-
rated for the entire marsh estuarine sys-
tem (Pomeroy and Wiegert 1980). This num-
ber does not include leachate, however,
making it a conservative estimate.

It should be noted that some contro-
versy exists regarding the paradigm that
emergent macrophytes are the primary
source of particulate carbon in coastal
ecosystems in the South Atlantic Bight.
Arguments have been advanced (Haines 1976,
1977) that perhaps production by phyto-
plankton is more significant than that of
emergent macrophytes. Counterarguments
and hypotheses by Peterson et al. (1980)
provide alternative interpretations of
Haines' (1976, 1977) studies. Until more
definitive research resolves this contro-
versy, the paradigm is still viable.

Phytoplankton

The major phytoplanktonic producers
in a "typical" estuary in Georgia were
listed (Pomeroy and Wiegert 1980) as pela-
gic diatoms (and occasional benthic pen-
nate diatoms swept up from the bottom into
the water column), dinoflagellates and
green flagellates. Their combined produc-
tion rate was estimated as 125 gC/m-^/yr
(Pomeroy and Wiegert 1980) when prorated
for the entire marsh water surface (water
comprises about one-third of this area).

Benthic Algae and Epiphytes

The principal primary producers in
the marsh sediments are benthic pennate
diatoms. These organisms migrate verti-
cally in the sediment, depending on the
tidal stage and light conditions. They
are often clearly visible on exposed creek
banks as a golden sheen on the brown mud.
Pomeroy and Wiegert (1980) reported that
benthic algae account for about 11% of
total net primary production in a marsh
estuarine system in the study area, or
134 gC/m^/yr, prorated for total estuarine
area.

Another group of primary producers in
the marsh-estuarine ecosystem is the com-
munity of epiphytic algae that inhabits
the culms or stalks of marsh grass. This
diverse community is not readily apparent

but attracts grazers, especially the gas-
tropod Littorina irrorata. In terms of
production rates, the epiphytic community
is relatively unimportant compared to
Spartina alterniflora (Pomeroy and Wiegert
1980).

Mixotrophic

Chemosynthetic Bacteria:
and Photolithotrophic

Two groups of anaerobic microbial
organisms inhabiting sediments within the
salt marsh-estuarine system are the mixo-
trophic sulfate-reducing bacteria and the
photolithotrophic bacteria, which have re-
cently received scientific attention. The
abundance of sulfate in salt marsh sedi-
ments makes this ion the obvious substi-
tute for oxygen as the electron acceptor
in the anaerobic respiration of many mi-
crobes. These organisms use dissolved
organic matter as an energy source. Sul-
fate reduction is now recognized as an
extremely important process in the salt
marsh estuary (Fenchel and Riedl 1970;
Howarth and Teal 1979). As sulfate is
reduced (primarily by a bacterial group
known as Desulfovibrio), the resulting
sulfide diffuses upward. Its reducing
"power" is subsequently used along with
light as the energy source to fix atmos-
pheric carbon dioxide by anaerobic bacte-
ria. The release of the resulting organic
matter from salt marsh sediments is prob-
ably augmented by tidal flushing and may
be quite significant along creek banks.

A major implication of this overall
process is that the initial carbon source
for the sulfate reducers is leachate from
the roots of macrophytes. Thus, the wet-
land macrophyte production is ultimately
the source of this (unknown) amount of
extra organic carbon that goes into the
ecosystem.

1.4 ESTUARINE CONSUMERS

The following description of the con-
sumers of the salt marsh estuarine ecosys-
tem in the study area is necessarily in-
complete because it describes only those
groups of organisms that are considered
dominant, functionally significant, or
that directly affect the oyster reef com-
munity. These are bacteria, benthic in-
fauna, zooplankton, nekton, and terres-
trial consumers.

10

Bacteria

Two basic principles relate to the
consumption of the net energy produced
annually in the marsh-estuarine ecosystem.
The first principle is that most energy
produced by the dominant primary producer
in the system (Spartina alterniflora) is
not consumed directly by grazers. Instead,
at least 90% (perhaps 95%) either leaches
into the water column from living and dead
plants as dissolved organic matter, or
through various processes enters the sys-
tem as detritus. Both forms of this or-
ganic matter are then attacked by micro-
scopic decomposers or ingested directly by
macroconsumers.

The second major principle of energy
consumption in the salt marsh is that the
decomposer community (aerobic and anaer-
obic) is large, diverse, and extremely
active, consuming about 50% of the total
energy flowing through the ecosystem, as
shown in Figure 4 (Teal 1962). The decom-
poser community of the estuarine ecosystem
can be divided conveniently into two
groups: (1) aerobic heterotrophs (bacteria
and fungi) which utilize inorganic matter
in standing dead grass stalks, the water
column, and aerobic sediments; and (2) an-
aerobic bacteria in anoxic (oxygen-poor)
sediments. The activity of the aerobic
group enhances the nutritive quality of
both particulate and dissolved organic
matter for the larger consumers. Particu-
late organic matter is colonized by the
aerobic heterotrophs as it is gradually
fragmented into detritus. Its nutritional
value is enhanced by increasing the rela-
tive nitrogen composition of the particu-
late organic carbon (POC), as shown by
Odum and de la Cruz (1967). This can be
symbolized as follows: POC + O2 + NH4+ -^
bacterial POC-N + CO2. Dissolved organic
carbon (plant leachates, etc.) can be as-
similated by micro-heterotrophs and also
converted into POC-N. Some aerobic bac-
teria are also critical elements of the
nitrogen cycle, as discussed below.

Anaerobic decomposers function in a
variety of roles in the salt marsh ecosys-
tem. They are essential to the geochemical
cycles that release plant nutrients in a
continuous stream to the primary produc-
ers. The nitrogen cycle is especially im-
portant because evidence to date indicates

that nitrogen is the limiting nutrient in
the salt marsh (Valiela and Teal 1979).
Since the decomposition of cellulose is
nitrogen-limited (Pomeroy and Wiegert
1980), the decomposition of the large
standing stock of organic matter in the
system results in a competition for nitro-
gen between decomposers and primary pro-
ducers.

Four groups of bacteria are involved
in the nitrogen cycle. One group in the
sediments (nitrogen fixers) converts atmo-
spheric nitrogen to nitrate and nitrite
(N2 -* NC3 -+ NO2-); another group (the de-
nitrifiers) reduces nitrates and nitrites
to atmospheric nitrogen. A third group
(ammonifiers) converts dead tissue into
ammonia. A fourth group (nitrifiers) oc-
cupies the thin, oxidized layer around
Spartina roots and converts ammonia from
anaerobic sediments into nitrates directly
usable by the plant.

The anaerobic zone in salt marsh-
estuarine sediments extends upward almost
to the sediment surface because of the
enormous oxygen-depleting capacity (chemi-
cal oxygen demand) of these sediments. The
metabolic activity of anaerobic bacteria
is responsible for this oxygen demand.

Benthic Infauna

Other organisms in estuarine sedi-
ments include metazoan animals larger than
bacteria but so small that studying them
and documenting their functions are diffi-
cult. This group is called the meiofauna,
and although it contains various phyloge-
netic groups and trophic positions, its
overall role apparently is that of a tro-
phic intermediary between bacteria and
macroconsumers. Nematodes and other meio-
fauna appear to be major processors of
bacterial tissue, and they are an impor-
tant component of the food of many so-
called deposit feeders (Sikora 1977; Bell
and Coull 1979). Intertidal biomass of
nematodes in creek banks in the study area
has been measured at 6.4 g ash free dry
weight (afdw)/ m^ (Sikora et al. 1977).

Larger benthic organisms (macroben-
thos) in salt marsh estuaries are usually
divided into epibenthos and macro-infauna.
Because oysters are epibenthos, we will
omit further discussion of epibenthos

11

RECYCLING

Kcal/m2/vr

Figure 4. Model of energy flow in the Georgia salt marshes (adapted from Teal
1962).

12

until later. Macro-infauna are often di-
vided into two functional groups, deposit
feeders and suspension feeders. Theories
have been developed to explain why often
the two groups appear to be mutually ex-
clusive in local areas (Rhoads and Young
1970; Levinton 1972).

Suspension feeders include clams and
sone tube-dwelling polychaetes (worms).
Deposit feeders are often more motile, and
some workers even include in the group
those quasidemersal nektonic organisms
that burrow into the bottom to feed, e.g.,
grass shrimp. Kany polychaetes and gas-
tropods (snails) are also deposit feeders.
Another major category of the estuarine
macrobenthic community is the predators,
including some gastropods, turbellarians
(flatworms), nemertines (round worms), and
echinoderms (starfish).

Deposit feeders and demersal nekton
are important in reworking the sediments
by burrowing and plowing (bioturbation).
This activity redistributes organic matter
and other nutrients to the water column
and introduces oxygen into the sediments.
For example, one mullet can rework 45 m^
of bottom area per year (Pomeroy and
Wiegert 198G).

Conversely, suspension feeders (in-
cluding oysters) filter particles from the
water column and then deposit organic miat-
ter in the form of feces on the sediment
where it becomes available to the decom-
posers. Krauter (1976) estimated that salt
marsh macrobenthic organisms (in the marsh
proper) deposit 1,709 g dry wt/m-^/ yr,
which is 455 g of organic matter. He also
calculated that 53% of the marsh's annual
primary production could be processed
through the feeding mechanisms of these
organisms.

Zooplankton

Estuarine animals living suspended in
the water column generally are classified
as zooplankton if they are either so small
or such weak swimmers that they are trans-
ported passively by water currents. The
mobility of zooplankton typically is lim-
ited to vertical migrations in the water
column; for example, a daily migration
from the surface to bottom waters and back
again is a commonly observed pattern among

many forms. By altering their vertical
elevation in the water column, zooplank-
ters can use variations in food supply and
use water movements in estuaries for dis-
persion by "riding" parcels of water mas-
ses as the latter traverse an estuary.
For example, some species of zooplankton
follow the salinity wedge on the bottom as
the wedge progresses landward, or the sur-
face layers of freshwater as they move
seaward.

Zooplankton often are divided into
holoplankton and meroplankton. Holoplank-
ton spend their entire life cycles in the
water column while meroplankton spend only
their larval stages above the bottom.
Holoplankton include microzooplankton,
such as copepods and rotifers; and macro-
zooplankton, like euphausiids, ctenophora
and other jellyfish. Meroplankton include
larval finfish and decapods; and a large
contingent of the larvae of many macroben-
thic animals, including many polychaetes,
barnacles, clars and mussels, and, of
course, oyster larvae.

The functional importance of zoo-
plankton in the estuarine ecosystem is
partly expressed by a high turnover rate
of planktonic species, by large popula-
tions, and by the very small average size
of individual members. These three fac-
tors ensure that zooplankton process a
large amount of the organic materials
available in some estuaries, much of which
represent the conversion of phytoplankton
into the tissue of higher consumers. The
zooplankton community as a group largely
depends on phytoplankton as a carbon
source, and thus tends to be more impor-
tant (abundant) in estuaries dominated by
phytoplankton, rather than in those where
macrophyte production is of primary impor-
tance. The carbon pathway from phytoplank-
ton to zooplankton to higher consumers is
a significant trophic link in all estua-
ries, however, including those in the
study area.

Although the oyster larvae are mem-
bers of the zooplankton community, they
are extremely vulnerable to predation by
plankton feeders, including members of the
macroplankton group, such as ctenophores.
Some years ago in the New Jersey oyster
grounds, oyster spatfall (larval recruit-
ment) was reduced during years of large

13

ctenophore populations (Nelson 1925). He-
roplankton usually compose a greater por-
tion of the zooplankton community during
summertime when many clams, mussels, oys-
ters, barnacles, crabs, polychaetes, and
other benthic organisms are spawning. This
input of living protein from the bottom
into the water significantly increases the
food supply of filter-feeding animals,
both nektonic and epibenthic suspension
feeders. Many of the latter probably can-
nibalize larvae of their own kind.

Nekton

The active swimmers in the estuary
are divided into pelagic and demersal nek-
ton. The pelagic nekton feeds in the
water column, either on phytoplankton and
detritus, on zooplankton (including oyster
larvae), or on other nektonic forms. The
bottom feeders or demersal nekton feed on
adult benthos, including oysters and their
associates. Darnell (1961) reported the

feeding habits of some typical estuarine
nekton (Figure 5).

Terrestrial Consumers

The other major group of consumers
characteristic of the marsh-estuarine sys-
tem is the large, diverse collection of
"terrestrial" or land-based consumers.
This group comprises insects and other
small arthropods, including some fiddler
crabs; pulmonate gastropods, especially
Littorina irrorata; birds; reptiles (even
alligators); and mammals, such as the rice
rat, mink, otter, and raccoon. The spe-
cific members of this group that directly
impinge on the oyster reef community are
discussed in Chapter 3. The total biomass
of terrestrial consumers, including the
active primary consumers (plant hoppers
and grasshoppers) that graze Spartina di-
rectly, was estimated at 1 g C/m2 (Pomeroy
and Wiegert 1980).

- ••---- M, *^

--'-^.T-v^-*;''

h^'W

.^^•-"W^.

^ %==■

^c; --

i-L^ -^ »:^ **

'2:

•fM-

A view of the estuarine environment in which oyster reefs occur in coastal South
Carolina. Photo by South Carolina Wildlife and Marine Resources Department.

14

FOOD
CATEGORIES

TROPHIC SPECTRUM OF ESTUARIME COMMUNITY

CONSUMER SPECIES (NEKTON!

I < £

li|

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_) UJ uj CL "J -

m o: o. (A > <

2 o < 5 o
< _i I < <

w u. « o -

— ■ -■■■■■

MACROBOTTOM
ANIMALS

MICROBOTTOM
ANIMALS

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IMIHII
ll-l-hl —

-I - - - -

ZOOPLANKTON

PHYTOPLANKTON

M

VASCULAR PLANT
MATERIAL

l-l

ORGANIC DETRITUS
AND UNDETERMINED
ORGANIC MATERIAL

Mlim-

— -■ — "

Figure 5. Trophic spectrum of an estuarine community (Lake Pontchartrain
Estuary, Louisiana) (adapted from Odum 1971 after Darnell 1961).

15

This photograph depicts individual reef oysters occurring at the mean
low water mark. Note the vertical orientation. Photo by Rhett Talbert,
University of South Carolina.

16

CHAPTER 2
FUNCTIONAL OYSTER BIOLOGY AND AUTECOLOGY

This chapter summarizes the salient
information on oyster biology, especially
that relating to the functional position
of the oyster in the estuarine ecosystem.
Each aspect of oyster biology discussed
here is presented as an aid to understand-
ing this functional role.

A number of excellent treatises on
oyster biology, including the monograph on
the American oyster by Galtsoff (1964),
preclude the necessity for another exten-
sive treatment. Readers interested in
more detail on subjects discussed here
should refer to Galtsoff (1964) or other
references cited in the chapter.

2.1 EVOLUTION AND TAXONOMY

The oyster evolved long ago from an
ancestral mollusk into a highly reorga-
nized and in some ways simplified form.
The major evolutionary steps involved are
summarized below as they were recon-
structed by Yonge (1960):

(1) lateral compression of the body

(2) extension of the mantle to the
margins of the shell

(3) division of the shell into
halves (valves) separated by
a noncalcareous ligament

(4) fusion of pallial muscles to
form paired adductor muscles

(5) reduction of head and develop-
ment of labial palps

(6) development of cilia on (paired)
gills, and development of a gill
feeding function in addition to
their respiratory role

(7) probable reduction of metabolic
requirements over that of ances-
tral forms

(8) loss of foot and byssus in the
adult life stage

(9) loss of anterior adductor muscle

(10) rounding of the body

(11) development of a horizontal
orientation with the left valve
down in the adult form

The currently accepted formal classi-
fication of the American oyster is pre-
sented below, accompanied by the major
morphological and ecological characteris-
tics that apply to each category. There
is currently some controversy about the
classification of some oyster genera and
species, and descriptors are not standard-
ized, so that different workers have used
shell morphology, geographical range,
reproductive behavior, and larval shell
morphology to classify oysters. New tools
of biochemical genetics offer hope of
resolving some of the controversial ques-
tions in oyster taxonomy.

For this report, the American oyster
will be classified according to Abbott
(1974) as follows:

Class Bivalvia (Pelecypoda)
Order Pterioida
Family Ostreidae
Genus Crassostrea
Species virginica

Each taxon will now be described
briefly.

Class Bivalvia

This class includes clams, mussels,
scallops and oysters. Some general char-
acteristics are (1) a shell divided into
two valves hinged dorsal ly by a ligament
of conchiolin and connected by one or two
adductor muscles; (2) a shell usually
consisting of three layers: an outer
organic horny matrix (conchiolin), a mid-
dle prismatic layer, and an inner nacreous
or pearly layer; (3) a laterally com-
pressed body; (4) either a small head or
none at all; (5) a wedge- or hatchet-
shaped foot (if present), (6) a mantle
extending to the margins of the shell and
forming a large mantle cavity, containing
ciliated gills (ctenidia) that function in
feeding, pumping, and respiration; (7) a
crystalline style that releases amylase
for starch digestion.

17

Order Pterioida

The order Pterioida is one of four
orders of bivalves, each distinguished by
the structure of its gills, and includes
pearly and winged oysters, scallops, and
the true oysters. These orders are char-
acterized by paired gills that are greatly
lengthened (compared to the ancestral
type) and folded back on themselves to
form four demibranchs interconnected by
tufts of cilia. The mantles in these tnol-
lusks have taken over the sensory function
of the molluskan head, including some
visual or light-sensing capacity.

Family Ostreidae

This family includes a large number
of edible and nonedible oysters. They are
generally restricted to shallow coastal
waters between 44° S and 64° N (Galtsoff
1964). Oysters have unequal valves with
no hinge teeth except in the prodissoconch
or larval shell. In all but their larval
stages, oysters have completely lost their
byssus (attachment filaments) and foot and
have retained only the posterior adductor
muscle, which is kidney- or crescent-
shaped.

Genus Crassostrea

The oysters included in this genus
are characterized by extremely variably
shaped (ecomorphic) shells, depending on
the substrate and current regimes of the
habitat in which the oysters grow. Mem-
bers of the genus Crassostrea are anatom-
ically distinct from their counterparts in
the genus Ostrea, in that Crassostrea are
somewhat larger at maturity, with a deeper
cupped left valve on which they ordinarily
rest. ^ They also possess a distinctive
asymmetrical space between the right
mantle and gill plates, known as the
promyal chamber. The promyal chamber is
important because it probably permits
greater pumping rates, an advantage in
silt-laden water (Ahmed 1975). This cham-
ber also functions in the reproductive
success of this genus. Eggs of Crassos-
trea species are small ( -x. 40 y) and are
released directly into the water, rather

Note, however, that reef oysters are usu-
ally oriented vertically with both left
and right valves pointed upward.

than being incubated within the mantle
cavity, as those of the genus Ostrea. The
promyal chamber allows for higher release
velocity for eggs and is important for egg
dispersal.

The production of free-living plank-
tonic larvae is critical to members of the
genus Crassostrea because it promotes ge-
netic exchange over wide areas. Oyster
larvae have been documented to travel at
least 50 km (30 mi). Quayle (1969) and
Stenzel (1971) estimated that they could
disperse up to 1,300 km (800 mi).

Probably the most important charac-
teristic of the genus Crassostrea, which
has permitted almost worldwide distribu-
tion, is its ability to tolerate wide
ranges of salinity, turbidity, tempera-
ture, and oxygen tension.

The morphology has changed little
since the oyster arose during the Triassic
period about 190 million years ago. The
genus Crassostrea arose during the Creta-
ceous period (T35 million years ago)
(Stenzel 1971). Representatives of this
genus characteristically occur in turbid
estuaries with soft ■ bottoms in the Indo
Pacific area, Eurasia, Africa, and North
and South America.

Crassostrea virqinica

The Eastern or American oyster (£.
virginica) is the species that builds the
intertidal reefs focused on in this re-
port. This species is distributed along
the entire east coast of North America,
from the Gulf of St. Lawrence in Canada to
Key Biscayne, Florida, to the Yucatan and
the West Indies; and it has been reported
even in Brazil (Gunter 1951). Figure 6
(from Ahmed 1975) illustrates this 8,050-
km (5,000-mi) range. Crassotrea virqinica
prevails over this immense range because
of its tolerance to low temperature (Sten-
zel 1971).

Physiological, ecological, and bio-
chemical data indicate that £. virqinica
has several distinct physiological races
(Loosanoff and Nomejko 1955; Menzel 1955;
Hillman 1964; Li and Fleming 1967; Ahmed
1975). On the other hand, Buroker et al.
(1979) concluded that significant genetic
distinctions occur only between popula-
tions of C. virqinica from Nova Scotia and

18

140

120

60-'

40

20

0°

l?S^

PACIFIC OCEAN

40

Figure 6. The distribution of Crassostrea virginica is indicated by the shaded
line. Note the distribution of the other major North American species, Ostrea
Turida, shown by the solid line on the west coast (adapted from Ahmed 1975) .

19

west Florida. These researchers concluded
that the two populations were only 82%
genetically similar, approximately the
level of similarity between £. virginica
and £. rhizophorae. The latter two spe-
cies are genetically close enough to have
been successfully hybridized in the labor-
atory (Menzel 1968). Stauber (1950) pos-
tulated that C. virginica was discontin-
uously distributed on the east coast dur-
ing prehistoric times, and that speciation
was occurring before oyster culture activ-
ities by man removed the barriers to gene
transfer.

N. E. Buroker (University of Maryland
Marine Products Laboratory, Crisfield,
Maryland; pers. comm. ) indicates a single,
large panmictic (genetically homogeneous)
population exists between Cape Cod, Mary-
land, and Corpus Christi, Texas, with 96%
to 99% genetic similarity. Levinton (1973)
reported that six species of bivalve mol-
lusks (not including oysters) showed an
increase in genetic variability with an
increase in intertidal elevation, corre-
sponding to increasing environmental vari-
ability. This would be an interesting
parameter to study in intertidal reef oys-
ter populations.

Without further consideration of the
evolutionary origins of the oyster, we
will concentrate on the functional (eco-
logical) classification of C. virginica
between Cape Fear, North Carolina, and
Cape Canaveral, Florida. From this point
on, the generic term "oyster" will mean £.
virginica, and "oyster reef" will refer to
oyster reefs in the study area unless spe-
cified otherwise.

The general anatomy of the adult oys-
ter appears in Figures 7 and 8 (adapted
from Galtsoff 1964). Note the insert dia-
gram in Figure 7 showing the proper way to
describe oyster size.

2.2 OYSTER REPRODUCTION AND DEVELOPMENT

oyster is dioecious (with sepa-
0. but once a year some members

The
rate sexes]

of a given local population change their
gender from male to female (protandry) or
female to male (protogyny). This sexual
lability is possible partly because of the
simplicity of the oyster reproductive

system, which lacks ducts, glands, or sec-
ondary sexual structures (Yonge 1960).
Oysters develop functional gonads at a
young age (2 to 3 months) and small size
(less than 1 cm in height). Usually they
tend to develop as males during their
first season, with subsequent protandric
change (to females) in following seasons
(Menzel 1955). A small percentage of any
given population ( <1%) functions as true
hermaphrodites (Kennedy and Battle 1963),
and this pattern seems to hold for other
species in the genus Crassostrea (Asif
1979).

Some preliminary evidence indicates
that populations of oysters under certain
kinds of stress tend to develop a higher
proportion of males than females, but this
remains to be conclusively demonstrated
(Amemiya 1936; Loosanoff and Nomejko 1955;
Kennedy and Battle 1963; Bahr and Hillman
1964). It is interesting to speculate,
however, that the stress encountered in
the higher portions of the oysters' verti-
cal range in the intertidal zone (the
upper reef zone) could produce androgenous
(predominantly male) colonies that would
contribute little to the reproductive suc-
cess of the population.

After oyster gonads reach maturity in
a local population, a temperature (or sa-
linity) shock triggers the emission of
sperm from one or more males. The temper-
ature at which oyster populations in dif-
ferent regions begin to spawn has been
used in the past to distinguish physiolog-
ical races. Atlantic coast and gulf coast
oysters have thus been separated into
17° C, 20° C, and 25° C spawners (Yonge
1960). Reef oysters subject to very high
summer temperatures are probably members
of the last group.

The emission of sperm from male oys-
ters occurs via the exhalent chamber of
the mantle. A chemical constituent of the
sperm (a protein pheromone) stimulates the
females in the area to release eggs, and a
spawning chain reaction can sweep dramati-
cally over a dense population, turning the
water white. Females expel eggs from the
inhalent chamber rather than through the
exhalent chamber. This process involves a
preparatory contraction in portions of the
mantle margins to reduce the size of the
exhalent opening. Eggs then pass through

20

MOUTH

LABIAL PALPS
CEREBRAL GANGLION

LEFT MANTLE

PERICARDIUM

RIGHT MANTLE

GILLS

ADDUCTOR MUSCLE

SHELL
TENTACLES

FUSION OF TWO MANTLE
LOBES AND GILLS

X

_L

_L

CENTIMETERS

Figure 7. Anatomy of the ovster (Crassostrea virginica) and diagram showing the
correct method of measuring the height, length, and width of oyster shells (from
Galtsoff 1964).

21

CONNECTIVE TISSUE

INTESTINE

DIGESTIV
DIVERTICULA

GONAD

KIDNEY

EPIBRANCHIAL
CHAMBER

LATERAL
AFFERENTV

BRANC
EFFERENT VEIN

GILL ROD

LEFT MANTLE

GILLS

WATER TUBE
OF THE GILLS

GONAD

INTESTINE
BLOOD SINUS

STOMACH

DIGESTIVE
DIVERTICULA

KIDNEY

PROMYAL
CHAMBER

COMMON
AFFERENT VEIN

i<yj AFFERENT VEIN

BRANCHIAL
EFFERENT VEIN

GILL MUSCLES
RIGHT MANTLE

WATER TUBE
OF THE GILLS

GILLS

EDGE OF
LEFT MANTLE

EDGE OF
RIGHT MANTLE

MANTLE CAVITY

0 0.5

I 1 1

CENTIMETERS

Figure 8. Transverse section of the dorsal part of an adult Crassostrea virginica
(adapted from Galtsoff 1964).

22

the gill filaments (against the normal
feeding current) and accumulate near the
inhalent chamber. Rapid and repeated con-
tractions of the adductor muscle then
forcefully eject the eggs a considerable
distance. The latter mechanism is also
used to expel unwanted particulate mate-
rial (pseudofeces) from the mantle cavity.

Fertilization occurs in the water
column via chance encounters of eggs and
sperm, and larval development ensues.
Thus begins the free living phase of oys-
ter larvae. These larvae function as zoo-
plankters (meroplankton) in the water col-
umn, and probably are significant as a
food source for planktivores in local
areas.

After passing through blastula and
gastrula stages, the young oyster develops
into a trochophore larva characterized by
a band of locomotory cilia called the pro-
totroch. As development continues, the
larval oyster secretes a pair of shells,
and the prototroch becomes the larval
velum, a ring of locomotory and feeding
cilia characterizing the veliger larva.
The first shelled larval stage is also
termed the straight-hinge (veliger) stage.

The straight-hinge stage is succeeded
by the umbo (veliger) stage, in which the
larval "beak" on the left valve overhangs
the hinge line. During the latter part of
this stage, the larval oyster develops a
foot and a byssus gland with which it will
eventually attach itself to the substra-
tum. With the development of the foot the
larvae becomes known as a pedi veliger.
During the latter part of the pedi veliger
stage, the larval oyster develops a pair
of darkly pigmented eyes. The presence of
these eyes indicates that the free-swim-
ming oyster is ready to attach and meta-
morphose into the adult form. At that
time the larva is termed an eyed pedive-
liger.

Depending on water temperature and
food availability, the larval life stage
of C^. virginica will last approximately 7
to 10 days. However, some larvae will
remain planktonic for up to 2 months dur-
ing cooler periods or in the absence of
sufficient food. Early winter sets of
oyster larvae in the northern Gulf of Mex-
ico may be attributed to this phenomenon

(Edwin W. Cake, Gulf Coast Research Lab.,
Ocean Springs, Mississippi; pers. comm. ).

Feeding activities in larval oysters
are generally well understood due to
recent advances in commercial oyster cul-
ture. In the artificial conditions of an
oyster hatchery, mixed cultures of various
small "naked" flagellates (algae) produce
adequate nutrition for the growing oys-
ters. It is important to emphasize the
value of mixed cultures, as opposed to
monocultures, for oyster food sources.
There are apparently synergistic reactions
among various food items that are as yet
unknown but that are very important to
oyster growth (Epifanio 1979). This is
hardly suprising because the diet of
oyster larvae in the natural state is
obviously far from a pure culture and
probably includes bacteria and small de-
trital particles as well as algae and pro-
tozoa. The diet could also include dis-
solved organic matter.

After a variable planktonic period
(about 2 weeks) from initial fertiliza-
tion, the surviving oyster larvae prepare
for settlement and metamorphosis. At this
stage the "mature" larvae are signifi-
cantly larger than the younger straight-
hinge, early umbo, and late umbo stages;
and they are experimentally separable by a
160-y mesh sieve that retains the mature
stages but not the immature (Hidu and
Haskin 1971).

Several environmental factors influ-
ence the settlement of larval oysters,
including the physico-chemical and biolog-
ical factors discussed by Hidu and Haskins
(1971). They maintained that light, sa-
linity, temperature, and current velocity
all affect "prospective" spat (newly set-
tled oysters). Thorson (1964) proposed
that the settling response of marine
invertebrates is often cued by light. For
example, oyster larvae tend to be photo-
positive throughout their larval life span
but may become photonegative in response
to a temperature increase. Late settling
oyster larvae also tend to be more demer-
sally distributed than earlier larvae,
possibly because of their heavier shells.

Along the Atlantic coastal regions
south of Virginia, spatfall appears to be
denser in intertidal areas. Hidu and

23

Haskin (1971) related this phenomenon to a
water temperature increase during flood
tides over intertidal mudflats. The slack
water areas of eddy currents also seem to
favor heavier than average spatfall pat-
terns (Roughley 1933). Spatfall will be
discussed again in Chapter 4 when the dis-
tribution of reefs in an estuary is con-
sidered.

The biological cues to oyster larval
settling are related to the fact that oys-
ter larvae are gregarious and apparently
respond to a waterborne pheromone or me-
tabolite released by oysters that have al-
ready metamorphosed (Hidu and Haskin
1971). Larvae also seem to respond posi-
tively to a protein on the surface of oys-
ter shells. This gregarious tendency is
important to a reef-building (colonial)
organism such as the oyster, which re-
quires settlement in proximity for suc-
cessful fertilization (Crisp and Meadows
1962, 1963). See Chapter 3 for additional
details of gregarious behavior.

2.3 OYSTER FEEDING, DIGESTION,
AND ASSIMILATION

The feeding organs of oysters are (1)
the ciliated gills that provide the water
currents (with the assistance of the man-
tle) and sort particles; (2) the palps
surrounding the mouth that also play a
role in the particle-sorting process; (3)
the crystalline style, a semirigid clear
rod composed of digestive enzymes that
function in the mechanical breakdown of
food particles; (4) the gastric shield
against which the style rotates to grind
food particles; (5) the stomach, in which
food and digestive enzymes are mixed; and
(6) the digestive diverticula surrounding
the stomach, a group of blind-ending tu-
bules with ducts leading to the stomach.
The latter function in intracellular di-
gestion.

The feeding of all filter-feeding bi-
valves (including oysters) had been as-
sumed to be a continuous process in those
organisms that are always submerged. The
ciliary feeding currents and the produc-
tion and erosion (dissolution) of the re-
volving crystalline style have been
thought to occur continuously in undis-
turbed animals. This view was challenged

by Morton (1973, 1977), who presented per-
suasive evidence that even in many sub-
tidal bivalves, the feeding process is
cyclic and discontinuous, affected by
tidal and seasonal factors.

It is obvious that an intertidal oys-
ter cannot feed when exposed during ebb
tides, but an interesting aspect of Mor-
ton's hypothesis is that the feeding pro-
cess is necessarily cyclic in subtidal as
well as in intertidal bivalves. The impli-
cation of discontinuous ciliary suspension
feeding with a tidal rhythym is that tidal
and seasonal cycles were incorporated by
ancestral bivalves in the evolution of
their feeding process.

According to Morton (1977), the feed-
ing of intertidal oysters occurs in three
cyclic stages: (1) a feeding stage during
which the oyster pumps water with ciliary
currents produced by the gills; (2) an ex-
tracellular digestive stage, during which
the crystalline style acts on ingested
food that has been rolled into mucous
strings; and (3) an intracellular diges-
tive stage, during which small particles
of food are further digested, absorbed,
and assimilated within the digestive
diverticula of the stomach. The three
stages are illustrated in Figure 9. Note
that the production of pseudofeces (con-
solidated particulate matter that is
expelled without undergoing the digestive
process) occurs during the active feeding
cycle when rejected particles accumulate
in the inhalent chambers. Fecal produc-
tion results from the extracellular diges-
tive and intracellular digestive process-
es, but feces and pseudofeces cannot be
released except during inundation. Morton
concluded that the three feeding cycles
occur during two alternate phases: (1)
food is collected, filtered, selected, and
passed to the stomach; (2) food collection
ceases and the accumulated material is
digested.

The specific diet of intertidal oys-
ters, like that of most estuarine consum-
ers, is not clearly understood. The gills
of the adult oyster have been reported to
retain diatoms, dinoflagellates, and
graphite particles from 2\i to 3p but to
pass 70% to 90% of Escherichia coli and
80% of graphite particles from Ip to 2p .
On the other hand, Loosanoff and Engle

24

FEEDING

FECES AFTER

INTRA-CELLUlAR

DIGESTON

STYLE
DISSOLVES

EXTRA-CELLULAR

DIGESTIVE

CYCLE

BREAKDOWN OF
DIGESTIVE DIVERTICULA
FRAGMENTATION
SPHERULES

INTRA-CELLULAR

DIGESTIVE

CYCLE

ASSIMILATION

ABSORPTION
IN DIGESTIVE
DIVERTICULA

FECES AFTER

EXTRA-CELLULAR

DIGESTION

Figure 9. A schematic representation of the rhythmic nature of the feeding process
and extracellular and intracellular digestive mechanisms in oysters (adapted from
Morton 1973).

25

(1946) found ambiguous and variable re-
sults when examining the relation between
particle size and retention on the gill in
oysters. These results suggest that the
filtering efficiency of oysters is not
necessarily related to their pumping rate.
The role of mucous in actually trapping
food particles in oysters is unclear, as
is the importance of dissolved organic
material to the overall energy intake.

The assimilation of significant lev-
els of dissolved organic matter (DOM) in
oysters was documented by Collier et al.
(1953), although the methods were criti-
cized by Galtsoff (1964). Oysters probably
"leak" some organic carbon (Johannes et
al. 1969). Some workers feel that hetero-
trophic microorganisms (bacteria) repre-
sent the only significant consumers (and
packagers) of DOM (Sottile 1973).

Feeding activity in oysters is high-
est at low concentrations of food; there
is a negative correlation between pumping
rate and turbidity (Loosanoff 1962). The
effect of turbidity on the pumping rate is
illustrated in Figure 10 (Loosanoff and
Tommers 1948). Some ambiguity between
laboratory and field studies exists how-
ever; for example, oysters held above the
bottom, in the so-called maximum turbidity
zone, grew more rapidly than those on the
bottom in commercial beds in Buzzards Bay,
Massachusetts (Rhoads 1973). Reef oysters
may have a similar advantage in the study
area. The average suspended load of par-
ticulate organic matter (POM) in a typical
estuary in Georgia ranges between 4.6 and
15.8 mg/liter afdw (Odum and de la Cruz
1967). Hanson and Snyder (1979) reported
extraordinarily high levels of suspended
particulate organic carbon (POC) in the
study area (0.02 to 0.1 gC/liter), equiva-
lent to approximately 40 to 200 mg POM and
much higher than the 1967 estimate of Odum
and de la Cruz. High levels of suspended
organic matter could reflect strong tidal
currents.

Particulate organic matter is a mix-
ture of marsh plant detritus, phytoplank-
ton, benthic algae, bacteria, zooplankton
(incuding oyster larvae), and DOM adsorbed
onto clay particles. An intertidal oyster
diet is a mixture of these items, some of
which are not incorporated into oyster
tissue while others are more assimilable.

The presence of cellulolytic activity in
the crystalline style of the oyster has
been reported (Newell 1953), but the
amount and kind of cellulose that can be
used by the animal are unknown. Because
the diet of the oyster includes dinofla-
gellates and other algae with cellulose
tests (outer covering), the ability to
digest such structural polysaccharides
appears to be advantageous.

Results from laboratory experiments
on oyster feeding are sometimes ambiguous
or at least not directly applicable to
oysters in their natural setting. For
example, a study by Epifanio (1979) indi-
cated that the gross chemical composition
of experimental algal cultures fed to oys-
ters (protein, lipid, carbohydrates, and
ash) was less important to subsequent oys-
ter growth than was the specific type of
algae used. Oysters have even been shown
to grow on cornstarch-supplenented diets
(Ingle 1967).

A final note on the specific diet of
intertidal oysters: in the only analyses
of 6^^C (stable carbon isotope ratio test)
of oyster tissue from the Duplin River,
Georgia, Haines (1976) and Haines and
Montague (1979) found the stable carbon
isotopic ratio ranged from -21°/oo to
-24°/oo, typical of organic matter pro-
duced by phytoplankton. The interpreta-
tion indicates that oysters, even in small
tidal creeks surrounded by Spartina, feed
only on algae. We think this interpreta-
tion should be accepted cautiously due to
discrepancies found in different tissues
of shrimp. (Brian Frye, University of
Texas Marine Science Institute, Port
Aransas; pers. comm. )

The rate at which intertidal oysters
ingest particulate matter is the product
of four factors: (1) the average rate
(volume/time) at which they can clear the
water of POM of a favorable size range;
(2) the concentration of suspended food in
this size range; (3) the total time that a
given oyster (or reef) is inundated; and
(4) the percentage of inundation time that
oysters filter water. Any significant up-
take of DOM would add to this total rate.
An energy budget for individual oysters is
included in the Appendix and summarized in
Section 2.5; energy requirements of a unit
area of reef are discussed in Chapter 3.

26

z
o

(-
o

o

Z

o

90

80-

70

60

50-

40-

30-

0

•

.''^o- ■

SILT •• ■•

KAOLIN D D

CA CO, o- — -o

I I I —

1 2 3

CONCENTRATION g/liter

Figure 10. Effects of turbidity on pumping rate (adapted from Loosanoff and
Tommers 1948).

27

2.4 STRESSES ON OYSTER POPULATIONS:
NATURAL AND CULTURAL

Natural Stress

Much oyster literature concerns the
variety of microscopic organisms that
cause oyster mortalities. These pathogens
have caused massive oyster die-offs in
local areas and sometimes in broad re-
gions, e.g., the infamous outbreak of the
bacterium "MSX" (f^inchinia nelsoni ) in New
Jersey, Delaware, and Vircinia during the
late 1950's and early 1960's. "Disease
organisms" is an anthropomorphic and a
pejorative phrase typically applied to
organisms that appear to be harmful to
animals and plants valued by man, and it
often stands in the way of an objective
functional approach to ecosystems. Oys-
ters are ancient mollusks that undoubtedly
have been competitive with, preyed upon,
and parasitized by many species. Their
survival to the present attests to the
fact that they have maintained a comple-
mentary functional role within the estua-
rine ecosystem. As such, they have been
subject to various ecosystem feedback reg-
ulators, including so-called "disease
organisms" that maintain an oscillating
stability in oyster population density. In
the context of the present discussion,
protozoan, fungal, bacterial, and other
oyster parasites, comniensals, and preda-
tors, such as oyster drills and oyster
catchers, are considered oyster associ-
ates, or ecosystem regulators. These
function under natural conditions to con-
trol excessive populations and regulate
the distribution and density of oyster
reefs themselves. It appears, however,
that man-induced stresses on oysters miay
sometimes shift the balance in favor of
the oyster regulator by creating subtle
changes of temperature, oxygen, salinity,
or pollution levels (Galtsoff 1964).

We are unaware of any studies at-
tempting to distinguish between oyster
vulnerability to "disease" in subtidal vs.
intertidal habitats. Since oyster disease
is often density-dependent, extremely
dense intertidal reef populations may be
more vulnerable than sparse communities.
Reefs, however, persist in some areas for
long periods (see Chapter 4), and oysters
apparently have adapted better to the
stress of intertidal existence than have
the pathogens.

28

Oyster-associated organisms, includ-
ing common oyster commensals, are dis-
cussed in Section 3.2. Usually, the oc-
currence and density of commiensals are
less in intertidal reef oyster populations
than in subtidal oysters. Common commen-
sals include the boring sponge (Cliona ce-
lata), the polychaete mud worm (PoTydora
websteri ), and the pea crab (Pinnotheres
ostreum). None of these organisms actual-
ly kills the oyster, but they do produce
a stress. The boring sponge and the mud
worm induce additional shell deposition;
the pea crab lives within the oyster's
mantle cavity and steals food and mucous
from the gills, and perhaps even feeds on
developing gametes (Galtsoff 1964).

Other natural stresses include low
oxygen concentration, high temperature,
excessive turbidity (sedimentation), ei-
ther overabundance or shortage of appro-
priate food, crowding, and high wave ener-
gy or strong water currents. Oysters Are
remarkably tolerant of all these condi-
tions, however. For example, a subtidal
oyster population in the James River,
Virginia, was relatively resistant to a
severe freshet (flooding) associated with
the 1972 tropical storm Agnes (Larsen
1974). They close tightly and respire
anaerobical ly when exposed to the air or
during low oxygen conditions (Hochacka
and Mustafa 1972). Temperatures up to
40° C or more can be tolerated for short
periods (see Section 3.1). Reef growth
can accommodate slow, steady sedimentation
but not sudden pulses of sediment. Oysters
can withstand crowding, and as shown in
Chapter 3, population density is important
to their intertidal survival. Typically,
intertidal reef oysters are not robust and
fat, and do not contain high levels of
glycogen. The natural stresses of their
environment are reflected by the long nar-
row valves and watery tissue texture char-
acteristic of "coon" oysters.

Man-related stress

Man-induced perturbations on oysters
can conveniently be divided into eight
classes (Table 1) as follows: (1) physi-
cal disturbances, especially sedimentation
resulting from dredging and excessive boat
traffic; (2) salinity changes due to
freshwater diversion or local hydrologic
alteration; (3) eutrophication or over-
enrichment of water from organic matter,

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29

sewage, and/or fertilizer; (4) toxins.
Including pulp mill sulfites, heavy met-
als, chlorinated hydrocarbons, organophos-
phates, radionuclides, and petroleum
hydrocarbons; (5) physical impairment of
feeding structures by oil; (6) thermal
loading, primarily from power plants; (7)
overharvesting; and (8) wetland loss due
to development.

These perturbations can be lethal or
sublethal for oysters, but even when sub-
lethal, the oysters may be unfit for con-
sumption either by humans or by other
predators. Oysters, like most suspension
feeders, efficiently concentrate suspended
and dissolved constituents of the water
column to levels several orders of magni-
tude above background concentrations (bio-
accumulation). Human pathogens, pesti-
cides, and heavy metals are prime exam-
ples. Greig and Wenzloff (1978) reported
that oysters with high levels of heavy
metals in their tissues did not purge or
lose these metals rapidly when transferred
to clean water.

Quantifying sublethal effects on oys-
ters is complicated by the fact that oys-
ters live at the water sediment interface,
and most pollutant concentrations in sed-
iments are different from those in water.
While very low concentrations of some
toxins in oysters, like dioxin, may be
significant, the capability to detect
these pollutants has been achieved only
recently, so that much recent literature
on pesticide residues in oysters and other
organisms may be misleading (e.g., Buqq
et al. 1967).

The effect of crude oil extracts on
the carbon budget of Mytilus edulis, the
edible mussel, is illustrated in Figure
11. As shown, carbon ingested and assimi-
lated declines with increasing oil concen-
tration. Comparable effects could be
expected for the oyster.

The estuaries in the study area are
presently not as severely impacted by man-
induced (cultural) change as are some
other oyster-producing areas, such as sec-
tions of the Louisiana and Florida coasts,
Chesapeake Bay, and Long Island Sound. In
addition, intertidal reefs are in some
ways more resistant to man-induced pertur-
bations (e.g., salinity intrusion and

resultant susceptibility to predation)
because of the periodic exposure due to
tides. Conversely, intertidal reef exis-
tence is already stressful, and added
stress may inhibit reef formation.

Effects of marsh alteration in Texas
have decreased local oyster production
(Moore and Trent 1971). Changes in hy-
drology and pollution have probably con-
tributed to local declines in oyster reef
density in the Savannah, Georgia, area.
Historical change in intertidal oyster
reefs in the study area, caused by both
natural and cultural perturbations, is
discussed in Section 4.2.

Harvest of Intertidal Oysters

Because this paper's overall objec-
tive is to describe the ecological func-
tion and importance of the oyster reef as
a component of the coastal ecosystem in
the study area, we include here only a
brief discussion of several aspects of
exploitation of reef oysters by man. More
information on the present commercial har-
vest and potential for future exploitation
may be found in Gracy and Keith (1972),
Keith and Gracy (1972), and Gracy et al.
(1978). These references are for South
Carolina, where commercial harvest is con-
centrated in the study area.

(1) Oyster harvest by man has been
an important cultural activity since long
before recorded history (at least as early
as 2000 B.C., Keith and Gracy 1972). Nu-
merous oyster shell middens and shell
rings of apparent ceremonial significance
in the study area attest to the importance
of the oyster in the diet of early coastal
residents. Many oyster shells found in
these artifacts are large and thick,
which, when considered in light of the
presence of many whelk and oyster drill
shells, indicate that a significant por-
tion of the prehistorically harvested oys-
ters were of subtidal origin.

(2) Recent oyster harvest in the
study area, however, is primarily concen-
trated on intertidal oyster populations.
This harvest, both recreational and com-
mercial, involves the very labor-intensive
and time-consuming removal of clumps of
oysters from exposed mud flats, an effort

30

300-

200

% 100-

-100

A,

CARBON CONSUMED

CARBON ASSIMILATED

NET CARBON FLUX

CARBON RESPIRED

\

V

\

\
\

\

■v.:

\

01

10 50

%OIL EXTRACT

EM

Figure 11. Effects of crude oil extract on Mytilus edulis carbon budgets calcu-
lated for 100-mg mussels held at 3lo/oo salinity under summer conditions (15° C,
21!3Mg C/liter) (adapted from Gilfillan 1975).

31

conducted done from small, flat-bottomed
skiffs (bateaus).

(3) The majority of the (clumped)
oysters collected today are of a quality
that makes them less suitable for the raw
bar trade than for canned oysters. Thus
the oyster industry in the study area
traditionally has been an oyster steam-
canning industry.

(4) Of the intertidal oysters har-
vested, the most valuable, in terms of
their shape, size, and condition, are
found low in the intertidal zone rather
than in mature reefs, or oyster rocks, as
they are called locally.

(5) Oyster production or total har-
vest apparently peaked in the early 1900's
and has steadily declined for numerous
reasons as follows: over-harvesting and
generally poor management; pollution, re-
sulting in closing many local areas to
oystering; labor problems, i.e., a dwin-
dling number of people willing to work in
the labor-intensive oyster industry; and
changes in the hydrology of local area.

(6) Total oyster production from the
study area (principally South Carolina)
accounts for about 8% of total U. S. pro-
duction (Lee and Sanford 1963). Table 2
from Gracy et al. (1978) summarizes recent
oyster production from the study area and
includes both subtidal and intertidal oys-
ters. Presently it is unclear if the de-
cline in intertidal oyster harvest indi-
cates a decline in mature oyster reef den-
sity. For example, the closure of coastal
areas to oystering because of pollution by
human pathogens is in some respects bene-
ficial to natural oyster reef populations
that are thereby assured of nonexploita-
tion. On the other hand, hydrologic
changes accompanying marsh alteration and
increased coastal activities are likely to
be extremely damaging to the somewhat
fragile reefs. In Section 4.2 we discuss
the historical change in reef density in
the study area.

In summary, the true mature oyster
reef subunit of the coastal ecosystem in

the study area is not of commercial inter-
est because the reef oysters are of poor
market quality. The exception to this is
that high reef oysters can be removed and
replanted lower in the intertidal zone.
The increased efforts at oyster management
in the study area could benefit natural
reefs in that additional sources of oyster
larvae could be created. The commercial
exploitation of intertidal oysters ulti-
mately will depend on the study area's
economic climate. Increased mechanization
that would solve the labor problem (Hixson
1975) is constrained by continual rise in
energy costs.

2.5 ENERGY SUMMARY

A summary of estimates of energy flow
in oyster reefs in the study area appears
in Figure 12. These estimates were based
on the most reliable available information
(see the Appendix for details and ration-
ale). The numbers shown in Figure 12 are
the values for standing oyster biomass and
for oyster respiration rate. The respira-
tion estimate is particularly important as
an index of oyster function because it
represents the energy "tax" paid by reef
oysters to support their other activities.
The ratio between average biomass (kcal/
m2) and respiration (kcal/m^/yr) gives the
turnover time of the oyster portion of the
reef as 0.38 yr (or 2.6 times/yr). This
is the average time that any given organic
carbon molecule "survives" as a constitu-
ent of oyster tissue before becoming oxi-
dized to CO2 and recycled. Gamete produc-
tion represents another high energy expen-
diture, and the typical watery tissue of
"coon" oysters in reefs is symptomatic of
oysters that are continually spawned out

(or subjected to a po

itinual ly
or diet).

The extremely high ingestion and
egestion (biodeposition) estimates are ap-
proximate but indicate the qualitative im-
portance of reef oysters in the study area
for transferring suspended organic matter
to the reef surface. This process supports
the high bacterial metabolism noted in
Section 3.3, which in turn accelerates the
rate of carbon flux through the ecosystem.

32

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Close-up view of oyster shell debris characteristic of the high energy
beach shores at the mouth of large intertidal creeks. This shell pro-
vides a substrate for oyster spat settlement. Photo by Rhett Talbert,
University of South Carolina.

34

NET PRODUCTION 1000
(3.3% OF MAX.ASSIMILATION)

WORK

INGESTION
2.0-5.0 X iC

PREDATION 2000
(0.6% OF MAX.
ASSIMILATION)

BIODEPOSITION
1.8-4.9 X 106

GAMETE PRODUCTION
7500 - 13,000

RESPIRATION

13000

(43% OF MAX.ASSIMILATION)

Fioure 12. Summary of energy flow throuqh intertidal reef oysters,
expressed in kiloca lories per meter square per year.

Values ai-e

35

Intertidal reefs in coastal South Carolina. Note the relatively flat top of the
reefs in the background, a contnon feature indicative of the upper survival limit
of the oysters in the intertidal zone. Photo by Rhett Talbert, University of
South Carolina.

36

CHAPTER 3
OYSTER REEF DESCRIPTION AND SYNECOLOGY

The objective of this chapter is to
detail the intertidal oyster reef commun-
ity in the study area. The following sec-
tions will describe the reef, physically
and biologically, to set the stage for
Chapter 4 in which we discuss the rela-
tionship of the reef subsystem to the
entire estuarine ecosystem.

Much of the material in this chapter
was taken from Bahr (1974), the only
available study that treats the entire
reef community (in Georgia) quantitative-
ly. Extrapolations of the results from
Bahr (1974) to the entire study area
should be made cautiously, and with the
understanding that in South Carolina estu-
aries, oysters in reefs are less dense
and net growth is more significant than
is the case in Georgia (S. Stevens, Uni-
versity of Georgia, Sapelo Island; pers.
comm. ) .

3.1 GENERAL REEF DESCRIPTION

Intertidal oyster reefs range in size
from small scattered clumps to massive
solid mounds of living oysters and dead
shells. Reefs are limited to the middle
portion of the intertidal zone, where min-
imum inundation time determines the maxi-
mum elevation of reef growth. Predation
and siltation limit oyster populations in
the lower intertidal and subtidal zones to
scattered individuals.

The following passage by Dean (1892)
describes intertidal oyster reefs or
"ledges" in South Carolina at the turn of
the century.

Often at low tide the oyster ledges
appear to the eye curiously like a
low hedge of frosted herbage, gray-
ish-green in color. A nearer view
discloses branching clusters or
clumps of oysters, densely packed
together, whose crowded individuals
now become modified or distorted
according to their position on the

cluster. The individuals that cap
the cluster project upward like flat-
tipped fingers, slender, narrow, and
long, whose shape has given them
throughout the South the names "cat
tongues," "raccoon paws," or "rac-
coons." In many localities, as
throughout the region of Skull Creek,
the raccoon ledges, continuing for
ages to encroach upon the stream bed,
have formed vast oyster flats, acres,
sometimes miles, in extent.

During exposure to the atmosphere
(ebb tide), the surface of a reef dries
and turns gray, but upon wetting, a living
reef appears greenish-brown due to a thin
film of algae. In contrast, piles of dead
shells in the intertidal zone (wet or dry)
generally are less colorful than are liv-
ing reefs.

A section through a typical reef is
depicted in Figure 13. The uppermost por-
tion is level but slopes steeply at the
edges. The living portion of a reef is
thicker at the perimeter than in the cen-
ter, where mud trapped by biodeposition
and sedimentation smothers the oysters.
This sedimentation results from suspended
matter settling out as turbid water slows
down while passing over a reef.

Often the surface of a reef is uni-
formly covered with oysters closely wedged
together, so that it is difficult to re-
move an individual clump. Once a hole is
made in a reef, however, adjacent oysters,
lacking support, tend to fall toward the
cavity and are readily removed. Most ma-
ture oysters are long and narrow, and vir-
tually all are oriented with their growing
edges facing upwards (Figure 14). These
are the typical "coon oysters" described
in Galtsoff (1964). They seem to grow
toward the least disturbed water, like
branches on a tree seeking light, and away
from encroaching sediment beneath. A sim-
ilar growth pattern on a much smaller
scale was proposed for colonies of the
freshwater bryozoan, Lophopodella carteri.

37

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38

Figure 14. Several generations of oysters (C. virginica) growing vertically
on muddy bottom of Altamaha Sound, Georgia (adapted from Galtsoff 1964). This
growth pattern results in oyster clusters termed "coon" oysters as depicted in
photo. Photo by Wiley M. Kitchens, U.S. Fish and Wildlife Service.

39

by Bishop and Bahr (1973). Bahr (1974)
reported no evidence of orientation of
individual oysters with respect to cur-
rents in reefs in Doboy Sound (in contrast
to the studies by Lawrence 1971); but R.
Frey (University of Georgia Marine Insti-
tute, Sapelo Island; pers. comm. ) detected
such orientation among oysters in reefs
located in Blackbeard Creek, which is
characterized by strong bidirectional cur-
rents.

All reefs studied at Sapelo Island,
Georgia, were identical in height, 150 cm
above mean low water (MLW), except the
lower immature reefs, which presumably
were still growing. Peak height appears
to represent maximum equilibrium eleva-
tion, given present sea level and the
local tidal amplitude. Generally flooding
tides reach the lowest portion of the
reefs approximately 2 hours following
slack ebb, completely covering the upper-
most oysters approximately 2 hours before
peak flood. On an ebbing tide, the tops
of the reefs become visible about 2 hours
following peak flood, with the result that
the tops of the reefs are inundated only
4 hours per tide, or 8 hours per day. The
relationship between reef elevation and
tidal amplitude is unknown for other
areas.

Exposure to air during ebb tides
allows the visible portion of a reef to
dry. Only the upper layer (5-10 cm) of
oysters and dead shells actually dries
out, however. The underlying shell layer
remains moist and appears reddish-brown
when the dry shells are removed because a
thin layer of detritus covers each shell.
This lower layer of shells and living oys-
ters appears to lack the film of algae
characterizing the upper layer. A reef
can thus be considered as consisting of
three "horizons," one pale greenish-gray,
one reddish-brown, and one silver-black,
color characteristic of shells buried in
an anaerobic environment high in ferrous
sulfide (Wiedemann 1971). Fine scrape
marks appear on many shells from the green
and brown horizons, indicating that the
organic film is constantly grazed. Mud
crabs ( Panopeus herbstii and Eurypanopeus
depressus) graze these films on partially
inundated reefs (Bahr 1974).

Oysters in the upper (green) horizon
have sharper growing edges than those in

the brown layer, indicating faster growth.
Presumably this is a function of extreme
crowding and sediment encroachment on the
lower oysters. Many dead oysters are
found in the black and lower brown hori-
zons, with the valves still together, but
ful 1 of silt and clay.

Approximately 61% (by volume) of the
reef material collected from the upper
surface down to the black horizon consists
of living oysters, 21% consists of dead
shells, and the remaining 18% consists of
silt, clay, and nonoyster macrofauna.

Vertical Zonation

Although the three horizons described
for the oyster reef are somewhat arbitrar-
ily defined, there is a definite vertical
change in reef macrofaunal composition.
This is a result of interspecific toler-
ance to desiccation (drying) rather than a
feeding limitation resulting from reduced
inundation time. The pattern of zonation
in the study area (Figure 13) is typified
by the zonation pattern on dock pilings
from the lower Duplin River examined after
years of exposure to fouling organisms.
From these pilings one can extrapolate the
optimal elevations for oysters and other
epifauna of the reefs.

At Sapelo Island, Georgia, oysters on
pilings are virtually limited to an eleva-
tion (1.5m above MLW) corresponding to
the maximum elevation of reefs. One could
assume that this pattern of vertical zona-
tion would be compressed in areas of lower
tidal amplitude. Oyster growth is maximal
from about 60 to 70 cm above MLW, the ele-
vation corresponding to the level of the
sediment surface on which these reefs were
located. Dean (1892), observing growth
patterns on pilings, reported that oyster
growth in South Carolina was maximal in
the mid intertidal zone.

Populations of the barnacle Chthama-
lus fragilis dominate the upper 60 cm of
tidal range. Other barnacles (Balanus )
and two mussels (Ischadium and Guekensia)
representative of the reef community oc-
cupy the lower intertidal and upper sub-
tidal ranges on the pilings, which repre-
sent a zone extending beyond the lower
limits of the reef. In fact, optimum ele-
vation for these species appears to be be-
low the limits of the reef zone. Wiedemann

40

(1971) remarked on the paradoxical re-
striction of the barnacle, £. fragilis, to
the uppermost oysters in a reef or to
blades of marsh grass above the maximum
height of oyster reefs. Of the three spe-
cies of barnacles in the reef community,
C^. fragilis is restricted to the upper, or
green, horizon. Another related barna-
cle, C^. stel latus, has been described as
an obligate intertidal form for reasons of
competition rather than physiology (Con-
nell 1961; Barnes and Barnes 1969). The
restriction of Chthamalus to the mid to
upper intertidal zone was demonstrated by
Connell to result, not from intolerance to
constant inundation, but rather from com-
petitive exclusion by Balanus spp. In the
oyster reef community, where barnacle den-
sity is not as great as in Connell 's
study, oysters seem to assume the role of
"squeezing out" all but the uppermost
individuals of C. fragilis. Many well-
preserved individuals of the latter spe-
cies are found trapped and overgrown
between adjoining oysters. Chthamalus
fragilis represents the most obvious exam-
ple of vertical zonation in the reefs, but
other evidence of similar restrictions can
be observed; e.g., anemones occur almost
exclusively in the brown horizon.

Green and Hobson (1970) stated that a
difference in elevation of 6 cm in the
intertidal zone results in a significant
effect on rates of mortality; however,
they were describing an infaunal assem-
blage dominated by the little gem clam
(Gemma gemma). The oyster reef displays a
similar sensitivity at the upper limit of
its intertidal range. At slightly lower
elevations, however, these effects are
buffered by the physical complexity and
density of the reef, which trap and hold
moisture above the level of the surround-
ing sediment.

Temperature Effects on Oyster Reefs

Oysters adjacent to a hole in a reef
made by sampling often die after being
dislodged from their normal position in
the reef. Undisturbed oysters are normally
oriented vertically, (with the ventral
side upward) and those which collapse into
a sampling site are usually horizontally
oriented. The latter position results in
exposure of a greater proportion of sur-
face area to direct solar radiation, with

little chance for mutual shading. The tem-
perature of sediment within a reef varies
widely with depth; e.g., temperatures were
35°C at the surface and 28°C at 6 cm depth
during one measurement in October (Bahr
1974).

More critical than sediment tempera-
ture is the fact that the internal temper-
ature of an oyster is a function of the
orientation of the oyster with respect to
direct solar radiation. For example, the
internal temperature of a reef oyster in
Georgia varied (in the same October obser-
vation) from 34°C to over 38°C, according
to whether it was oriented vertically or
horizontally (Bahr 1974). In full shade
the temperature dropped to 31.5°C. This
implies that mutual shading of crowded
reef oysters is beneficial and important
to the maintenance of temperatures within
the tolerance limits of the oyster. In the
summer when the angle (azimuth) of the sun
is highest, significantly higher tempera-
tures result on incident surfaces; there-
fore, high mortalities could easily result
from the disruption of the angular orien-
tation of reef oysters which provides the
shading to protect the oysters. Copeland
and Hoese (1966) reported mass mortalities
of intertidal oysters in Texas during the
summer. Hodgkin (1959) concluded that an-
nual high mortalities of littoral fauna
and flora near Fremantle, Australia, re-
sulted from high temperature, which was a
major factor in the maintenance of charac-
teristic shore zonation. Thus, it appears
that oyster reefs grow to elevations above
that at which individual oysters could
survive the rigors of temperature stress
and minimal inundation time.

Lehman (1974) examined the effects of
thermal loading from the discharge water
of a local power plant on the oyster reef
community at Crystal River, Florida. He
concluded that an average annual increase
of 4° C in the water surrounding experi-
mental reefs (relative to unaffected
reefs) caused an increase in oyster bio-
mass, metabolic rate, and turnover rate,
but a decrease in the diversity of the
reef community.

Salinity Effects on Oyster Reefs

Although oysters are euryhaline and
can tolerate low salinities, reefs are

41

limited to areas with significant tidal
amplitudes ordinarily associated with rel-
atively high salinity coastal environ-
ments. The effect of long-term salinity
changes on oyster reefs has not been
reported (see Section 4.2). The reef life
style allows oysters to invade the preda-
tor-rich, high salinity zones of estua-
ries. Predators are excluded because of
the reef's daily exposure to the atmos-
phere resulting from the ebb and flood of
the tides.

Reef Surface Area

The surface area of oysters and dead
shells in a series of reef samples was
measured by Bahr (1974). He calculated
that at least 50 m^ of surface area is
available for habitation by epifauna for
every square meter of overall reef area.
The production of this large, highly ir-
regular surface area is an important
aspect of the functional role of the oys-
ter. In the marsh-estuarine ecosystem that
is relatively devoid of hard substrate,
the oyster provides this limited resource
for other oysters and for the associated
macrofauna that will be described in the
next section.

3.2 REEF-ASSOCIATED MACROFAUNA

A total of 42 species of macrofauna
(or groups of related species) represent-
ing seven phyla are associated with the
oyster reef community in Georgia (Table
3). This is only a fraction of the 303
species listed by Wells (1961) in his
monograph on the fauna of subtidal and
intertidal oyster beds, but slightly more
than the 37 species found by Dame (1979)
in South Carolina reef samples. Rarely
present and thus not shown in Table 3 are
unidentified species of boring sponges,
bryozoans, hydroids, and mites; all of
these, except mites, occur abundantly on
subtidal oysters but only incidentally in
the intertidal reef community. Probably a
maximum of 50 macrofaunal species, includ-
ing those not readily separable, occur in
the community samples on which these num-
bers are based (Bahr 1974). Twenty-one
species occurred in the majority of the
samples; 17 occurred in 93% or more sam-
ples; 8 species occurred in every sample.
Mean frequencies for each reef species

over the entire sampling period and rela-
tive frequency of each species are listed
in Table 4. The biomass and relative bio-
mass of each major species or group of
species are given in Table 5. No relation-
ship between the size of reefs and the
macrofaunal community was observed by Bahr
(1974) although a theory exists that indi-
cates a direct (positive) relationship
between reef size and species richness
(Simberloff 1974; Jackson 1977).

A comparison of the results of Dame's
reef survey with the reef macrofauna data
reported by Bahr (1974) indicates that
Dame found slightly fewer species or
groups of related species (Table 3). Dame
also found a lower density of macrofauna,
by an order of magnitude (about 3,300 in-
dividuals/m^ compared to about 38,000/m2
reported by Bahr). Some of these differ-
ences may result from differences in sam-
pling technique since Dame sieved his oys-
ter reef sediment samples through a 1.0-mm
screen, whereas Bahr used a 0.5-irjTi mesh
screen.

Lehman (1974) reported 31 species of
invertebrate organisms or groups of relat-
ed organisms from oyster reefs in Crystal
River, Florida. Of these, only nine spe-
cies were also found by Bahr (1974) to be
associated with Georgia reefs. Lehman re-
ported the total abundance of reef-associ-
ated organisms to be about 6,200/m2 and
oyster density to be about 3,800/m2 in his
control area. His estimate of biomass of
oyster reef associated organisms was 135g/
m^ dry wt.

Specific groups of organisms that
reside in oyster reefs in the study area
will be discussed below.

Oyster Commensals

The relationship between the oyster
pea crab (Pinnotheres) and the oyster
represents inquilinism, an association
slightly detrimental to the host species
(Nicol 1960). Beach (1969) reported that
Pinnotheres becomes increasingly rare in
oysters in the higher portions of the
intertidal zone. Dame (1970) found only
about 1% incidence of pea crabs among
intertidal oysters in South Carolina;
likewise, Bahr (1974) found only a 3%
incidence.

42

Table 3. Nacrofauna found in Georgia oyster reefs (adapted from Bahr 1974).

Taxa

Mollusca

Pelecypoda ^ ,

Crassostrea virqinica (Gmelin) ' '
Guekensia deniissa (Dil lwyn)^'°
Ischadium recurvum (Rafinesque)^'^'*-
Mya arenaria (Linnaeus )
Gemma gemma (Totten)^
Petricola pholadiformis (Lamarck)^

Gastropoda .

Odostomia impressa (Say) '
Arthropoda

Insecta .

Anurida maritima (Guerin)^' '^

Cirripedia

Balanus improvisus (Darwin) '
Balanus eburneus~rGou1d)^'"'^
Chthamalus fragilis (Dan-n'n)^

Decapoda a b c

Eurypanopeus depressus (Smith) ' '
Panopeus herbstii (Milne-Edwards)^'^'^
Pinnotheres ostreum (Say)^'°
Sesarma cinereum (Say ) ^
Clibanarius vittatus (Bosc)

Amphipoda , h

Melita nitida (Smith)"''^

Parhyale hawaiiensis

Gamma rus pa1ustris^>*^
Isopoda

Cassidinidea lunifrons (Richardson)

Edotea motosa (Stimpson)
Annelida

Polychaeta a b c

Neanthes succinea (Prey and Leuckart) ' '

Nereiphyllis fragilis (Webster)^''^

Streblospio benedicti (Webster)^'^

Heteromastus filiformis (Claparede)^''^

Polydora websteri <^^^^^

Tharyx setigera(Hartman)^

Spirorbis sp.

Sabel laria megaris^

Amphitrite ornata (Leidy)^'"

Marphysa sanguinea (Montagu)^'"

Lysidice ninetta

Syllidae (unidentified)

Dodecaceria sp.

Continued
43

Table 3. (Concluded)

Taxa

Annelida (continued)

Polychaeta (continued)

Lepidonotus sublevis( Verri 1 1 )
Polychaete (unidentified)
Polychaete (unidentified)
Polychaete (unidentified)

Nemertea ^

Nemertina (unidentified)

Coelenterata

Anthozoa (unidentified)

Platyhelminthes
Turbellaria

Polyclad (unidentified)

Sipuncul ida

Sipunculid (unidentified)

?Genus reported by Wells (1961).
Species reported by Dame (1979).
Species reported by Lehman (1974),

44

Table 4. Mean annual frequency distribution of reef macrofauna.

Mean freq. Variance Standard
Species (#/ni2) S deviation % of total

s-

X

Crassostrea virginica^ 14666.9 4811.3 717.2 38.65

Guekensia demissa 514.8 459.5 68.5 1.36

Ischadium recuryum 5028.0 4051.0 603.7 13.25

Mya arenarlja 852.8 1577.7 235.2 2.25

Gemma gemma

Petricola pholadiformis

Odostomia impressaa 1643.5 1792.5 264.3 4.33

Anurida maritimaa ^ 5453.7 3626.4 1300.5 14.37

fBalanus ?ip?o7Tsus^ 1063.9 1063.1 158.5 2.80

1 Balanus iburneus'^ , 16.9 58.8 8.7 0.04

Lchthamalus fragilis^ 166.3 387.4 57.7 0.44

Eurypanopeus depressus 1037.1 430.5 64.2 2.73

Panopeus herbItiT5 103.1 75.0 11.2 0.27

Pinnotheres ostreum 24.5 33.5 5.0 0.06
Sesarma cinereum
Clibanarius vittatus

Melita nitidis , 334.2 455.2 67.9 0.88

ParhyalFTa^iiensis^ 966.2 1278.4 190.6 2.55

Gammarus palustris"^ 5.2 - -

Cassidinidea lunifrons'^ 323.5 171.6 25.6 0.85

{
{

Edotea montosa

14666.9

4811.3

717.2

514.8

459.5

68.5

5028.0

4051.0

603.7

852.8

1577.7

235.2

1.3

-

-

0.4

-

-

1643.5

1792.5

264.3

5453.7

3626.4

1300.5

1063.9

1063.1

158.5

16.9

58.8

8.7

166.3

387.4

57.7

1037.1

430.5

64.2

103.1

75.0

11.2

24.5

33.5

5.0

0.1

-

-

0.4

-

-

334.2

455.2

67.9

966.2

1278.4

190.6

5.2

-

-

323.5

171.6

25.6

1.3

-

-

1739.1

1778.3

268.1

78.0

60.9

9.0

1362.4

1723.4

259.8

519.8

314.7

46.9

359.3

436.4

65.1

0.3

-

-

1.1

-

-

1.7

-

-

4.3

-

-

5.2

-

-

1.3

-

-

0.4

-

-

0.9

-

-

0.4

-

-

0.9

-

-

8.7

-

-

4.8

-

-

204.0

194.8

29.0

1442.5

1376.6

205.5

7.8

-

-

0.4

■"

^

4.58

Neanthes succinea

Nereiphyllis fragilis! 78.0 60.9 9.0 0.21

Streblo'spio benedicti^ , 1362.4 1723.4 259.8 3.59

Heteromastus filiformis^ 519.8 314.7 46.9 1.37

Polydora websterT^ 359.3 436.4 65.1 0.95

Tharyx setigera

Spirorbis sp.

Sabellaria megaris

Amphi trite ornata

Marphysa sanguinea

Lysidice ninetta

Syllidae (unidentified)

Dodecaceria sp.

Lepidonotus sublevis

Polychaete (unidentified)

Polychaete (unidentified)

Polychaete (unidentified)

Nemertina (unidentified)^ 204.0 194.8 29.0 0.54

Anthozoa (unidentified)^ 1442.5 1376.6 205.5 3.80

Polyclad (unidentified)

Sipunculid (unidentified)

Total: 37,947.4

^Twenty-two species found in 93% of all samples and considered dominant.
Brackets enclose groups of "similar" species that reduce major macrofauna

members of the reef community to 16.

45

Table 5. Ranked biomass of 16 major oyster reef species or
groups of species and proportion of total macrofaunal biomass.

~ Mean biomass

Species or group of species (g/m^ + 2 s-) % of total

Crassostrea virginica 969.6+93.4 87.534

Guekensia demissa 83.7+26.9 7.554

Ischadium recurvum 24.4+13.0 2.200

Eurypanopeus depressus 13.5 jH 2.3 1.220

Panopeus herbstii 7.3+ 4.4 0.656

Neanthes succinea 3.4 + 1.6 0.304

Anthozoa (unidentified) 1.5+ 0.5 0.131

3 Cirripedia species T-^l 0.6 0.130

3 Amphipoda species 1'2 ji 0.5 0.106

Nereiphyllis fragilis 0.8+ 0.5 0.069

Mya arenaria 0.3+ 0.5 0.024

Odostomia impressa 0.3+ 0.1 0.024

Nemertea (unidentified) 0.1 + 0.0 0.013

Anurida maritima 0.1 ± 0.1 0.013

3 Polychaeta species 0.1 + 0.1 0.013

Cassidinidea lunifrons 0.0 + 0.0 0.001

Total 1,107.7

46

Other inhabitants of shells of sub-
tidal oysters were virtually nonexistent
within reef oysters examined in the Geor-
gia study, e.g., worms (Polydora spp. )
were found free in the samples but not
inside oysters. Boring sponges (Cliona
spp.) were absent on intertidal oysters
but abundant on subtidal oysters and dead
shells. Infestation (with Cliona) results
in shell deterioration in subtidal oysters
due to shell erosion by Cliona. Infested
(with Cliona) oysters are particularly
vulnerable to predation, and the shells
are fragmented into pieces which tend to
be washed away rather than remaining in
situ as substrate for further coloniza-
tion. This is one of the principal reasons
that subtidal reefs are absent in the
study area. Guida (1976) discussed the
abundance of Cliona spp. in subtidal oys-
ters and oyster shells. No oyster drills
or starfish were ever seen on the reefs
examined. Parasitic gastropod, Odostomia
impressa, was abundant, (up to 5,460/rr,2).

Insects

An interesting organism occurring in
abundance on oyster reefs in the study
area is a collembolan insect, Anurida mar-
itima, a true marine insect (Miner 1951 ).
The trophic role of a similar intertidal
collembolan (Oudemansia esakii ) in Hong
Kong has been described as saprophagic on
recently dead macrofauna, including oys-
ters (Chan and Trott 1972). Anurida
appears to be a true oyster associate
since it is only observed on mud flats
near oysters. The greatest concentrations
are inside dead pairs of oyster shells,
which often house masses of live insects
along with large numbers of exuviae (shed
exoskeletons). Small and covered with a
nonwettable cuticle, Anurida is extremely
buoyant and would be washed away during
flood tides were it not for crevices in
oyster shells which allow masses of them
to cling together. As in the case of
Oudemansia, Anurida probably emerges to
the reef surface during ebb tide and
retreats before flood tide. Dame (1979)
reported a few Anurida ('^6/m2) present in
South Carolina reefs and Lehman (1974)
reported Anurida from Florida reefs.

Barnacles

has been noted in previous sections (see
Section 3.1). Dame (1979) did not report
C^. fragilis on South Carolina reefs, which
may indicate that these reefs were lower
in the intertidal zone. Since total bar-
nacle density on oyster reefs does not
approach the density observed on pilings
(Bahr 1974), it appears that unknown fac-
tors limit barnacle survival on intertidal
reefs. It has been reported that Balanus
eburneus reaches maximum density at a
elevation of 9 to 14 m below sea level
(Relini and Giordano 1969).

Mud Crabs

Two of the most characteristic mem-
bers of the reef community are the common
mud crabs Eurypanopeus depressus and Pano-
peus herbstii. observed by Bahr (1974) at
mean densities of l,037/m2 and lOS/m^,
respectively. They seem to remain quies-
cent in the brown horizon during exposure
of the reefs but begin active feeding with
tidal inundation. Feeding consists of us-
ing one or both chelae to scrape the film
of algae and detritus from shells in the
brown and green horizons. The "grazed"
appearance of shells and the fact that
neither algae nor detritus accumulates on
shells indicate the proficiency of graz-
ing. These two crabs are undoubtedly
omnivorous, and Bahr (1974) noted Panopeus
predation on small oysters on reefs and
Eurypanopeus predation on amphipods in the
laboratory. Dame (1979) reported much low-
er densities of mud crabs on South Caro-
lina reefs; he found the two species in
approximately equal densities.

Soft Shelled Clams

Common occurrence of small soft shell
clams in the reef samples was noted by
Bahr (1974) at densities ranging up to
6,460/m2. No adult clams have been ob-
served in reef samples. It appears that
clam spat (juveniles) settle on the reefs
and survive only temporarily. Mya arenaria
has not been reported to range success-
fully as far south as Georgia, although
adult specimens have been found at Sapelo
Island. Dame (1979) did not report find-
ing Mya arenaria in South Carolina reefs.

Mussels

A marked vertical zonation of Chtha- Kuenzler's (1961) study of the ribbed
malus fragilis, one of three barnacle spe- mussel Guekensia demissus (formerly called
cies identified from the reef community, Modiolus) demonstrates that this animal's

47

functional importance in the marsh system
resides more in terms of nutrient (phos-
phorus) cycling than in energy flow. He
estimated the mean density of Guekensia in
the entire marsh at 7.82 animals/m^,
whereas in oyster reefs in Georgia, this
mussel averaged over SOO/m^. Ischadium
recurvum was found to be 10 times more
numerous in reefs than was Guekensia (see
Table 4), and together these two species
contributed 9.5% of total macrofaunal bio-
mass (112.08 g/m2). Dame (1979) reported
about 7 Guekensia/m^ in South Carolina
reefs and about 71)0 Ischadium/m^, or two
orders of magnitude greater than Gueken-
sia.

Anemones

Anemones are sessile epibenthic sus-
pension feeders that have soft bodies and
are extremely vulnerable to dessication.
Thus, they are not normally considered
intertidal organisms. Their common occur-
rence in reef samples in Georgia (Bahr
1974) attests to the capacity of oyster
reefs to retain water above MLW and to
extend the vertical distribution of such
creatures. Dame (1979) did not report any
anthozoans in South Carolina reefs, but
this group could have been overlooked in
preserved samples.

Polychaetes

Polychaetes are generally one of the
dominant groups in benthic systems because
of their contribution to total biomass or
to numbers, or both; but they are usually
considered infauna, with some obvious
exceptions such as the serpulids, which
produce encrusting calcareous tubes. Smith
(1971) found that polychaetes constitute
the major portion of macrofauna in a sub-
littoral community near Sapelo Island. In
the oyster reef community, polychaetes
accounted for only 0A% of the total bio-
mass, most of which was contributed by one
species, Neanthes succinea, which averaged
1,739 animal s/m^, compared to 281 /m^ in
Long Island Sound (Sanders 1958).

The three most abundant small poly-
chaetes, Polydora websteri, Heteromastus
filiformis. and Streblospio benedicti,
together compri sed only about 0.01% of
total macrofaunal biomass. There is a
relative dearth of polychaetes in this

reef system compared with other communi-
ties. This is perhaps related to the pre-
dominantly epibenthic nature of the reef
community and to the absence of a substan-
tial layer of aerobic sediment. Dame
(1979) found significant numbers of Heter-
omastus in South Carolina reef samples,
but he did not find many of the other two
small polychaetes, probably because of the
large mesh size used to screen his benthic
samples.

Amphipoda

Amphipods are more numerous and di-
verse in sublittoral oyster beds than on
intertidal reefs since, in the latter sit-
uation, tidal pools are not available to
sustain them during ebb tides. Grackles
were observed feeding on oyster reefs,
probably preying on amphipods and mud
crabs (Bahr 1974). Dame (1979) found rel-
ativity few amphipods in South Carolina
oyster reef samples, and only one species,
Melita nitida, was reported.

Accidentals

Hydroids, bryozoans, flatworms, and
sponges, all commonly associated with sub-
tidal oysters (Guida 1976), were so rarely
encountered in Georgia oyster reefs as to
be considered "accidentals" in the reef
community.

3.3 REEF COMMUNITY ENERGETICS

The energy requirements, expenditures
and an overall energy budget for reef oys-
ters are discussed in the Appendix. The
additional energy requirements of nonoys-
ter members of the reef community are ad-
dressed in the following section. The data
used are primarily those reported by Bahr
(1974).

The best available estimate of total
energy requirements of the reef community
is the rate at which a unit area of reef
consumes oxygen (community respiration
rate). A sine curve fitted to oxygen con-
sumption of the total reef community in
Georgia for a 1-year period is depicted in
Figure 15. The variation in community oxy-
gen uptake ranged from approximately 6 to
50 g02/m2/day over a temperature range of
9° to 30° C.

48

o
O

E
E
o
o

Jan 12

Apr 13 May 18 Jun 22 Jul 22
Apr 20 May 26

Sampling dates

Aug 30 Sep 29 Oct 19 Nov 18

Oct 29 Nov 29

Figure 15. Seasonal oxygen consumption (QO2) of reef community. Data points
are average values for four samples with 95% confidence intervals (Bahr 1976),

49

The area beneath the curve in Figure
15 was integrated over a 1-year period to
yield a total of 8,168 gOa/m^/yr consumed
by the oyster reef community, equivalent
to 27,036 kcal/m2/yr, assuming a respira-
tory quotient of 0.85. This estimate of
the community metabolic energy demand by
the reef community is conservative in that
it is derived by multiplying hourly rates
by 12 hours, with the assumption that
little respiratory activity occurs during
reef exposure at ebb tide. However, Lehman
(1974) reported a significant metabolic
rate of exposed oyster reefs by using an
infrared gas analyzer to detect CO2 re-
leased from enclosed reef samples. This
measured rate was about 20% of the rate
measured by oxygen changes during inunda-
tion. Total community metabolism in the
Georgia reefs is partitioned among oys-
ters, other macrofauna, small organisms,
and chemical oxygen demand.

Macrofaunal Respiration

The contribution of each species of
macrofauna to total community oxygen con-
sumption at a given temperature is a func-
tion of its proportion to the total bio-
mass, its size-frequency distribution, and
the relationship between rate of respira-
tion and size of an individual. Small rare
species contribute little to total biomass
and cannot contribute significantly to
total Qxygen uptake (QO2); large rare spe-
cies, on the other hand, can often alter
total oxygen uptake (Smith 1971). Banse
et al. (1969) and Pamatmat (1968) con-
cluded that the most reliable method of
estimating relative importance of various
macrofaunal species in terms of total com-
munity respiration is to multiply mean ash
free dry weight (afdw) per species by the
density of that species in the community.
By this criterion, the oyster reef commu-
nity members were ranked in terms of
macrofaunal metabolic importance, as shown
in Table 6. The two species that comprised
95% of total biomass, Crassostrea virqin-
ica and Guekensia demissa. contributed
87.5% and 7.5% of total community biomass,
respectively.

The respiration of oysters accounts
for approximately 50% (48.1%), or about
13,000 kcal/mVyr of the total reef com-
munity respiration. Total oxygen require-
ments (hence energy requirements) of non-
oyster macrofauna was thus estimated to

account for only 10% of the total reef
requirements, about 800 g02/m^/yr or about
2,700 kcal/m^/yr. This latter figure is
similar to the total oxygen uptake rate of
the subtidal soft bottom community near
Sapelo Island (Smith 1971).

Nonoyster macrofauna were divided
into 14 species or groups of related spe-
cies, and estimates of the annual oxygen
consumption rates were derived experimen-
tally (Bahr 1974), as shown in Table 6.

Microbial and Meiofaunal Respiration

The metabolism of small consumer
organisms represents 22% of the total reef
community metabolism (Bahr 1974). This
estimate is approximate since it is based
on the difference between total community
oxygen consumption and the sum of esti-
mated macrofaunal and chemical oxidation
rates.

The large surface area of an oyster
reef (at least 50 times the area of a
plane surface) provides a large surface
for aerobic bacteria as well as for epi-
fauna (see Section 3.1), and thus this
estimated large energy requirement, 1,600
g02/m2/yr (5,400 kcal/mVyi"), is not too
improbable.

Chemical Oxidation

Bahr (1974) estimated that the pro-
portion of total reef community oxygen
uptake accounted for by the chemical oxi-
dation of reduced compounds (20%) was only
slightly lower than microbial metabolism.
This estimate reflects the continual
release of reduced compounds from the
anaerobic decomposition of reef-derived
organic matter.

Summary

The seasonal energy partitioning
estimates for the entire reef community
are depicted in Figure 16. To summarize,
the reef community converts about 3 x 10**
kcal/m2/yr to heat, which represents the
net "cost" to the ecosystem of supporting
the reef community. Systems theory would
indicate that this cost is repaid by the
reef community in the form of feedback
services. For example, the reefs contin-
ually release plant nutrients, ammonia
and phosphorus-containing compounds; they

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51

^ Oyster QO2

^ Macrofaunal QO2

I I Chemical QO2
HI Microbial QO2

Jan 12 Mario Apr 13 May 18 Jun 22 Jul 22

Apr 20 May 26

Sampling dates

Aug 30 Sep 29 Oct 19 Nov 18

Oct 29 Nov 29

Figure 16. Seasonal energy partitioning estimates for the entire reef community
(Bahr 1974). QOt = oxygen consumption rate.

52

significantly increase habitat diversity
and provide substrate for epifauna, de-
composers, and small nursery species (at
least during flood tides). The 3 x 10"^
kcal/m2/yr would require the total net
production of about 5 m^ of marsh estuary
for each square meter of reef if total
production were usable by the community.
If only phytoplankton production were
usable, the reef community would require
at least 50 m^ of marsh estuary for nutri-
tional support (see Section 1.3).

A final point should be made about
oyster reef energy requirements: the met-
abolic rate of this community ranks high
among the values measured for the macro-
fauna! metabolism of benthic communities,
exceeding even such systems as kelp beds.
Table 7 summarizes the results of some
representative benthic community metabolic
measurements. Of particular interest is
the 1974 study by Lehman, in which total
reef community metabolism from gulf coast
oyster reefs (Crystal River, Florida) was
measured at 16 to 21 g 02m^/day at 31.7°C.
Lehman's values for biomass were lower
than those measured from Georgia reefs
(119.5 g/m^ dry wt vs. 970 g afdw/m^), and
his experimental temperature was about the
same as the maximum experimental tempera-
ture used by Bahr (1974).

The increasing number of metabolic
studies in which partitioning has been at-
tempted have well established that macro-
fauna usually play a relatively minor role
in total benthic community energy flow.
Smith (1971), for example, determined that
the proportion of total respiration rate
attributable to macrofauna of a sublitto-
ral community was equal to only 12.1%.
Therefore, the oyster reef community is
unique among benthic subsystems in that
the oysters and other macrofauna conspicu-
ously dominate community metabolism as
well as community structure. Intertidal
oyster reefs may be thought of as hetero-
trophic "hot spots" in the marsh-estuarine
system.

3.4 REEF PREDATION

No quantitative information is avail-
able on the rate at which salt marsh con-
sumers prey on the inhabitants of the
intertidal reef community. From a quali-
tative standpoint, the predators include

53

three groups: (1) small reef residents
such as mud crabs; (2) strictly aquatic
forms that migrate onto the reefs to feed
during flood tides, e.g., the blue crab
(Cal linectes sapidus) and the sheepshead
minnow (Cyprinodon variegatus); and (3)
terrestrial animals that prey on exposed
reefs during ebb tides, e.g., raccoons and
wading birds. This "time sharing" arrange-
ment by both aquatic and terrestrial pred-
ators, representing a "coupling" between
the reef and adjacent ecosystems, would
appear to wreak havoc on the reefs; but
relatively little evidence of predation
was ever detected in the reefs examined by
Bahr (1974). Blue crabs were observed
feeding on small oysters on partially
exposed reefs; raccoon tracks were seen
around reefs; and the most commonly ob-
served reef predators were boat-tailed
grackles (Cassidix mexicanus), seen pick-
ing unidentified organisms (probably small
crustaceans, insects, and polychaetes)
from recently exposed reefs.

Drinnan (1957) estimated that the
European oystercatcher (Haematopus ostra-
lequs) preyed on between 28.5 and 51 cock-
les per hour during active feeding, each
cockle being between 23 and 30 mm in
length. He concluded that about 22% of
the total cockle population in his study
area in Nova Scotia were removed as a re-
sult of this predation.

Butler and Kirbyson (1979) reported
that the black oystercatcher {H. bachmani )
can eat up to nine large oysters per hour,
the oysters ranging from 80 to 160 mm.
These birds feed primarily on single oys-
ters, however, as opposed to American oys-
tercatchers (F[. palliatus) that feed on
clumped or reef oysters (Tomkins 1947).
The latter author observed predation on
Crassostrea by oystercatchers on reefs
near Savannah, Georgia, but no attempt at
quantification was made. It was assumed
from Tomkins' description of the feeding
behavior of f[. palliatus that only about 4
hr/day are available for feeding on inter-
tidal oysters (2/hr/tide). Observations
on the density of oystercatchers at Sapelo
Island indicated fewer than one bird per
reef, perhaps one per eight reefs, result-
ing in an estimated maximum of 25 oysters
eaten by oystercatchers per reef per day
(4 hr/ day x 1/8 bird/reef x 50 oysters/
hr/bird). If an average reef were approx-
imately 25 m^, a total loss of about

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54

0.1 g/mVday, or 40 g/mVyr (200 kcal/m"/
yr) could be estimated as sustained by
intertidal oyster reefs from predation by
birds. This estimate is obviously clear-
ly approximate.

3.5 COLONIAL ASPECTS OF THE REEF COMMUNITY

The gregarious tendency of oyster lar-
vae has obvious adaptive value in terms of
the reproductive success of subtidal oys-
ter populations. It is also of great
adaptive value for intertidal reef oys-
ters. Survival in the upper intertidal
zone in the study area may depend on a
crowded colonial life style.

The only single oysters (greater than
30 mm in height) or small clusters of oys-
ters normally observed in the intertidal
zone were either at the lower level of the
zone (not much higher than 60 cm above
MLW), or they were scattered among stalks
of cordgrass (Spartina alterniflora),
where they were shaded. The only way oys-
ter reefs attain their maximum steady-
state elevation, or mature stage, is via
the slow process of reef accretion based
on mutual support and self-shading.

On the other hand, oysters in the
study area in the low intertidal zone or

subtidal zone are characteristically heav-
ily fouled and colonized with boring
sponges, i.e., Cliona spp. These oys-
ters dre usually thick-shelled, with the
stunted shape characteristic of slow grow-
ing oysters, particularly in high-salinity
areas. It is obvious that relatively few
oysters survive in the subtidal zone in
these marsh-estuaries and that dead shells
are rapidly eroded away by Cliona spp.

Oyster spatfall may be so dense in
some low latitude areas that it consti-
tutes a "fouling" situation. This condi-
tion (dense spatfall) has not been ob-
served on an intertidal reef, however.
Neither the density of barnacles nor oys-
ter spat appears to be limited by space on
a reef. This is perhaps not attributable
to a lack of prospective spat but rather
to the predatory effects of adult members
of the reef community, especially filter
feeders like mussels, barnacles, and oys-
ters themselves. The vortices set up by
the feeding currents of reef community
filter feeders could make the reef surface
a somewhat dangerous place to settle. This
type of density-dependent feedback could
explain the relatively even distribution
of oysters in the mature reefs and the
symmetrical form of the reefs.

American oyster catchers "loafing" on an oyster reef in South Carolina. These birds,
rare over most of their range, are concentrated in coastal South Carolina and Georgia,
feeding primarily on reef oysters. They are year-round residents and represent one of
the major predators to the oysters. Photo by Wiley M. Kitchens, U.S. Fish and Wild-
life Service.

55

"Fringing" reefs typical of those lining the shores of tidal creeks of high
salinity estuaries in coastal South Carolina. Photo by Rhett Talbert, Univer-
sity of South Carolina

'^^•i:*S^^r

Oyster reefs interspersed in channels dissecting an intertidal mud flat,
by Rhett Talbert, University of South Carolina.

56

Photo

CHAPTER 4. OYSTER REEF DEVELOPMENT, DISTRIBUTION,
PHYSICAL EFFECTS, AND AREAL EXTENT

4.1 REEF DEVELOPMENT

From a physical standpoint, a reef is
a biologically constructed, wave-resistant
or potentially wave-resistant structure.
Worldwide, reefs range from mounds less
than 1 m in height and diameter to massive
structures 1,000 m across and 100 m thick
(Pettijohn 1975). In general, reef mor-
phology is a function of the constituent
organisms and organism byproducts of which
it is built, whether these organisms are
corals, encrusting or sediment-binding
algae, tube-building polychaetes, or oys-
ters.

The thesis presented here is that the
location of oyster reefs in the salt
marsh-estuarine ecosystem is not acciden-
tal; rather, it is the result of interact-
ing physical and biological processes
that, if fully understood, would explain
the natural distribution of reefs in a
given area. Marshall (1954) concluded from
a study of the distribution of oyster bars
in Alligator Harbor, Florida, that physio-
graphic conditions and predation were the
most important factors.

In terms of physical conditions, a
minimum stability is undoubtedly required;
that is, a water current or wave energy
regime above a certain threshold level
will prevent the development of an inter-
tidal oyster reef. At the same time, the
development of a reef presumably affects
the physical stability of an area by damp-
ening current velocity and wave energy. To
be viable, a reef also needs a minimum
current velocity for the input of food and
the export of waste products. The local
reef area could thus be self-limited by
its dampening influence on the current
regime.

The following general model of oyster
reef initiation, "ontogeny," and decline
has four stages: (1) initial colonization,
(2) clustering phase, (3) accretionary
phase, and (4) maturation and senescence.

Initial Colonization

Initial reef formation begins with
the settlement and growth of single oys-
ters and small scattered oyster clusters
within the lower intertidal zone. A suit-
able substrate must be present for the
settlement of oyster spat and initial oys-
ter growth in an area where water flow is
sufficient to prevent stagnation (Galtsoff
and Luce 1930). Suitable substrates may
consist of either sand, firm mud, or clay.
Shifting sand and extremely soft mud are
the only bottom types totally unsuitable
for oyster communities (Galtsoff 1964).
Oyster larvae will attach to any hard
object, such as fallen trees, driftwood,
bushes, branches, old shell material, or
discarded solid waste (bottles, cans,
plastic, etc.) exposed in the intertidal
zone. It is important that the areas be
subject to little sediment deposition.

Clustering Phase

With time, additional generations of
oyster larvae will settle in the area of
the new reef and attach themselves to
other live oysters and dead shell sur-
faces. This process results in the forma-
tion of distinct oyster clusters. A clus-
ter is a small colony of three to seven
generations of oysters, the majority of
which are dead (Grave 1905). The oldest
and lowest oysters in the cluster die from
overcrowding and suffocation, but their
shells remain to support the upward and
outward growth of the cluster. This sup-
port is aided by the relatively flat shape
and low specific gravity of oyster shells.

Accretionary Stage

Small oyster clusters increase in
size through the settlement of additional
spat and eventually coalesce, forming
larger, massed oyster clusters (Grinnell
1971) that comprise the true construc-
tional nucleus of the intertidal oyster
reef. If environmental conditions remain

57

stable, the newly formed reef accretes
laterally and vertically within the inter-
tidal zone. Dead shell material scattered
around the reef aids in building up the
channel floor or reef platform, paving the
substrate for the reef to spread laterally
(Wiedemann 1972). Lateral reef accretion
generally occurs in a direction perpendic-
ular to tidal currents so that the effec-
tiveness of currents in transporting
nutrients and removing fecal material is
exploited (Grave 1905; Grinnell 1971).

On a still smaller scale, individual
oysters on the reef surface tend to orient
themselves so that their planes of commis-
sure (i.e., opening between the valves)
are alined roughly parallel to the current
direction (Lawrence 1971). Lawrence (1971)
found that either the anterior or poste-
rior shell margin may face the oncoming
current direction, a fact suggesting that
this alinement is necessary for the hydro-
dynamic stability of the individual oys-
ters. The macro-orientation of a reef with
respect to the local current regime and
the micro-orientation of its constituent
oysters are only demonstrable where the
currents are uni- or bi-directional. For
example, most of the reefs examined by
Bahr (1974) were located at the southern
edge of Sapelo Island in Doboy Sound, an
area with multidirectional currents, and
no definite macro- or micro-orientation
was observed.

Vertical accretion continues as long
as the upper (living) layer of the oyster
reef remains within the portion of the in-
tertidal zone in which oysters are viable.
Bahr (1976) found the maximal reef height
for oysters to be a constant feature of
the intertidal oyster reefs in Doboy
Sound. No reefs in this area exceeded
72 cm above the surrounding mud surface or
1.5m above mean low water.

At this stage of development, the
reef consists of an approximately 1-m
thick accumulation of live oysters, dead
shell, and mixed shell and mud (Figure
13). The uppermost portion of the reef is
level, sloping off steeply at the edges.
The living portion of the reef is thicker
at the edge than in the center because of
mud trapped by the reef. The central core
of the reef is corposed of mixed dead
shell and mud. If, for example, the reef

is formed on a soft mud substrate, its
weight will cause the entire structure to
slowly subside or sink. Vertical upbuild-
ing in a viable reef keeps pace with grad-
ual subsidence, and the upper reef surface
remains at a steady state with respect to
mean water level. The reefs examined by
Bahr (1974) were typical of this stage of
development.

Senescent Stage

A senescent stage of intertidal oys-
ter reef development is reached when the
upper surface of the reef can no longer
accrete vertically and the majority of
live oysters populate only the flanks of
the reef. The mature reef will have a bar-
ren central zone, or ridge in the case of
long linear reefs, comprising dead shell
and various sized fragments of shell. The
barren central region has been referred to
as a "hogback" (Gunter 1979) or flatland
surface (Grinnell 1971). Gunter (1979)
suggests that for gulf coast reefs the
constant motion or saltation of fine shell
"grit" in the central zone prevents the
survival of new oyster spat, so that this
area remains void of organisms. This
"grit theory" would not hold, however, for
the smaller, relatively sheltered reefs in
the environment of the salt marsh estuary.

An extension to the senescent stage
of reef development was proposed by Grave
(1905). He suggested that with time, the
barren central "flatland" surface would be
built up with thicker accumulations of
sand, mud, and shell debris, and would be
colonized by Spartina. The reef would then
become an oyster marsh island, with a
length and width greater than that of the
original oyster reef, and surrounded by a
thin band of intertidal oysters. Little
Egg Island in the mouth of the Altamaha
River in Georgia may be an example of such
an oyster-formed island.

4.2 DISTRIBUTION OF OYSTER REEFS IN THE
MARSH-ESTUARINE ECOSYSTEM

This section includes some specula-
tive material that remains to be confirmed
by scientific study. There is, however,
ongoing research at Sapelo Island, Geor-
gia, that should help explain the observed
distribution of reefs in the ecosystem

58

(S. Stevens, University of Georgia Marine
Institue, Sapelo Island, Georgia; pers.
comm. ) .

Present Distribution

Current speed and bottom roughness
have been theorized as controlling the
distribution of estuarine suspension-feed-
ing macrobenthos (Wildish and Kristmanson
1979). The distribution of intertidal oys-
ter reefs in the study area is described
in terms of the three hydrographic zones
of the estuary (see Section 1.2). The
zones are (1) the lower sound and inlet
areas between barrier islands; (2) the
middle region of the estuary, including
the major rivers feeding the sounds; and
(3) smaller tidal creeks draining the
marshes (Figure 2).

The typically high energy regime and
sedimentary instability of the lower sound
region render this zone the least favor-
able for reef development. Where reefs
are found in the lower sound areas, they
presumably indicate local pockets of shel-
ter from storm surges.

From the lower to middle estuarine
zone, wave energy is probably the control-
ling factor. The middle zone is charac-
terized by an optimum current regime for
reefs; the regime of the lower zone is too
turbulent, and the upper zone is too slug-
gish. Oyster reefs, sometimes exceeding a
kilometer in length, in the middle estua-
rine zone are predominantly (but not ex-
clusively) oriented along the banks of
rivers. Circular reefs and oyster reef
islands also occur infrequently in this
zone. Many reefs in the middle estuarine
zone are near the entrances to small tidal
creeks that feed the larger rivers. This
orientation is not accidental and may
indicate the importance of slight differ-
ences in current regimes, which are en-
hanced at the confluence of water bodies.

The complex network of tidal creeks
and small rivers that drain the marshes is
also an area of significant oyster reef
development. The distribution of inter-
tidal oyster reefs within this zone is
perhaps the most consistent and predict-
able of the three estuarine subdivisions.
The pattern of oyster reef development and
tidal creek meander systems are strongly

correlated. Oyster reefs are likely to
occur in three zones within a tidal creek
system (Figure 17): (1) on the concave
outer banks of meander loops, (2) in areas
immediately adjacent to smaller tidal
tributaries, and (3) at points of tidal
stream confluence.

The oyster reef tendency to develop
on the concave outer banks of tidal creeks
is predictable from the hydrography of
stream meanders. The outer or cut-bank of
the meander loop is the zone of highest
current velocity within the channel. The
sediment substrate, therefore, tends to
consist of firm, consolidated mud, swept
clean of soft mud and slime unsuitable as
a spat settlement surface. Once the reef
colony is established, these higher veloc-
ity currents provide nutrients and remove
fecal matter. Keck et al. (1973) discussed
this same relationship between meander
morphology and oyster distribution in the
Murderkill River, Delaware. Reefs in that
region tend to form in areas adjacent to
smaller tidal tributaries where important
marsh-derived nutrients are. Oyster reefs
at points of tidal stream confluence are
also influenced by hydrographic factors.
During flood tide, the confluence of flow
between the two tidal creeks results in a
zone of circular back-eddy formation lo-
cated at the point bar (Figure 17). The
turbulence associated with this process
provides nutrients to the reef. During
flood tide, the point bar is an area of
relatively higher current velocity and
little deposition.

Historical Changes in Reef Distribution

Four surveys of intertidal oyster
reefs along the Georgia coast demonstrate
changes in oyster distribution from 1889
to 1977. These are Drake (1891), Galtsoff
and Luce (1930), Linton (1968), and Harris
(1980). The survey results reveal two
aspects of the change in oyster reef dis-
tribution over time: a change in total
reef area, and local changes (increases or
decreases) in specific areas.

Galtsoff and Luce (1930) reported few
significant changes occurring in the dis-
tribution and extent of natural oyster
beds between the years 1889 (Drake 1891)
and 1925. They reported, however, a de-
cline in the health of many intertidal

59

Figure 17. Typical distribution of oyster reefs in small tidal creeks.
Zones are (1) concave outer banks of meander loops, (2) areas adjacent
to tidal tributaries, and (3) tidal stream confluence.

60

oyster communities, noting in a number of
cases, nothing but silt-covered, dead oys-
ter shells remained of once-productive
oyster reefs. This historical decline in
the welfare of the intertidal oyster com-
munity is further supported by the most
recent survey of Harris (1980), Total
acreage of the intertidal oysters has
decreased dramatically from approximately
688 ha (1,700 acres) in 1889 to less than
121 ha (300 acres) in 1977 (Harris 1980).
Large areas of dead oyster shell were also
reported in the 1977 survey. Harris re-
lated the steady decline of the Georgia
commercial oystering industry to the de-
crease of total oyster acreage. In addi-
tion, there is reason to believe that the
acreage figures reported by Harris (1980)
are somewhat exaggerated, perhaps because
they were partly based on aerial imagery
that did not permit easy distinction be-
tween living reefs and dead shells. For
example, Harris reported a total reef area
of 9,632 m^ in the Duplin River; Bahr
(1974) reported 6,040 m^ of living oyster
reefs in the same river based on a ground-
level survey.

Intertidal oyster populations in
South Carolina have apparently also de-
clined during the same period. We are un-
able at present to attribute this decline
to any specific factor. It may be the
result of a slow shifting of ecological
conditions that reflect a natural succes-
sional pattern in the marsh-estuarine eco-
system (e.g., sea level change). Puffer
and Emerson (1953) cited natural cyclic
changes in environmental conditions — pri-
marily temperature and salinity--as the
cause of oyster reef death and subsequent
repopulation in Aransas Bay, Texas. Alter-
natively, this decline may be the result
of a man-induced perturbation of the
marsh-estuarine ecosystem, such as dredg-
ing, waterway construction, pollution, or
overharvesting.

It is easy to explain a decline in
oyster reefs near population and indus-
trial centers such as Savannah, Georgia,
but it is much more difficult to account
for a decline of reef area in the more
pristine part of the Georgia coast near
Sapelo Island.

The salinity of the Duplin River at
Sapelo Island, Georgia, appears to have

increased recently (B. J. Kjerfve, Univer-
sity of South Carolina, Columbia; pers.
comm. ). This salinity increase could be
caused by a reduction in ground water
inputs due to consumptive losses resulting
from pumping for agricultural irrigation.
This change could partly explain the grad-
ual decline in viable oyster reef area in
the Duplin River and in other parts of the
study area, although, it is not clear how
a salinity increase up to 25 /oo or 30 /oo
would affect the reef community.

With respect to local changes in reef
distribution, it is possible to find exam-
ples of reef area increases in some spe-
cific portions of the Georgia coast. For
example, in Altamaha Sound, Georgia, oys-
ter reefs have developed in areas farther
inland in the lower sound than they oc-
curred in 1889 (Figure 21). Associated
with this shift in reef distribution is
the accretion of marsh islands in south-
ern Altamaha Sound. The accretion of
marsh and marsh islands may relate to the
sediment-trapping capacity of intertidal
oyster reefs (Grave 1905; Wiedemann 1972;
Stephens et al. 1976). The growth of
intertidal oyster reefs farther inland of
the lower sound may relate to shifting
salinity conditions in Altamaha Sound.

In summary, reef distribution along
the Georgia coast surprisingly has changed
little over the last 90 years. Oyster
reefs occur (in general) today in approx-
imately the same locations where they
occurred in 1889 (see Figure 21). The
living oyster reef area, however, signifi-
cantly has declined in the same period.

4.3 THE PHYSICAL EFFECTS OF OYSTER REEFS
ON THE MARSH-ESTUARINE ECOSYSTEM

Hypothetical ly, reefs affect the
physiography and hydrologic regime of salt
marsh estuaries three ways: by modifying
current velocities, both positively and
negatively; by passively changing sedimen-
tation patterns; and by actively augment-
ing sedimentation through biodeposition.

Interpretation of reef effects on the
ecosystem over time from analyses of sur-
vey data of the last century is difficult
because, although 90 years is a long bio-
logical time, it is short geologically.

61

For example, the average sediment deposi-
tion rate in the study area is less than 4
mm/yr (Letsch and Frey 1980). This means
that from the years since the first reef
survey in 1889, theoretically only about
one-third of a meter of sediment has
accumulated.

Oyster reefs undoubtedly dampen tidal
current velocities over the entire ecosys-
tem because of friction, but the magnitude
of the drag coefficient of a unit area of
reef is unknown, as is the overall effect.
Reefs also augment current velocity in lo-
cal areas by constricting tidal streams,
but no quantitative data are available to
detail the specific effects.

Grave (1905) noted that oyster reefs
are wave- and current-resistant structures
that exert a physical influence over the
marsh system. He observed that small reefs
originating at points along a tidal stream
accrete laterally across the stream (into
the current), and by displacing and con-
stricting the current cause erosion of the
opposite marsh bank. This process may re-
sult in the formation of marsh islands.

Passive sedimentation due to the
presence of reefs is qualitatively obvious
but has not been quantified. The magni-
tude of this effect would be related to
the overall reduction in tidal current
velocities and turbidity levels. Active
sedimentation through biodeposition can be
estimated (see Appendix). The biological
process of aggradation increases the size
of suspended particles and increases their
effective settling rates. The dominant
oyster reef zone's coinciding with the
maximum turbidity zone in estuaries in
the study area indicates that this effect
may be significant. Lund (1957a) reported
that oysters biodeposited or "self-silted"
eight times the volume of sediment in test
containers than would have deposited in
the same time due to gravity alone. He
calculated that a uniform single layer of
oysters in a natural setting with rela-
tively low turbidity water could biode-
posit sediment at a rate of about 280
tons/acre/yr (6 x lO** g/m^/ yr).

4.4 AREAL EXTENT OF OYSTER REEFS IN THE
COASTAL ECOSYSTEM

The most obvious criterion by which
to assess the importance of oyster reefs

on the marsh-estuarine ecosystem is the
relative proportion of reef surface area
to the total surface area of the system.
Planimetry on maps of the Georgia coastal
zone (Galtsoff and Luce 1930) indicated
that the total intertidal and subtidal
zones of the entire area occupied approxi-
mately 1.8 X lO^m^. Of this area, approxi-
mately 75% was marsh and tidal creeks, and
25% was open water (wider than about 350
m). The linear extent of the oyster reefs
measured about 403,000 m. If the average
reef were estimated as 2 m in width, the
total reef area in 1925 would have com-
prised about 8 X 10^ m, or 0.04% of the
marsh-estuarine area. If the mean reef
width were 3 m, reef area would increase
to 1.2 X 106 m2^ or 0.06%, Harris (1980)
estimated that the total viable reef area
in the Georgia coastal zone in 1977 was
equal to 102 ha, or about 0.05% of the
marsh-estuarine area. This presumably rep-
resents a decline from 1889, when Drake
(1890) estimated that 6.8 x 10& square
meters of reefs existed, or 0.3% of the
total marsh estuarine zone was occupied by
oyster reefs. In a detailed survey of the
Duplin River drainage basin, Bahr (1974)
estimated that about 0.06% of the marsh
estuarine zone was occupied by viable
reefs.

The absence of quantitative informa-
tion about the areal extent of intertidal
oyster reefs in South Carolina and north-
eastern Florida does not allow a compari-
son with Georgia. Apparently oyster reefs
comprise a larger percentage of the marsh
estuary in the South Carolina area than in
Georgia, but the relative difference is
unknown. A detailed analysis of the rela-
tionship between reef area and tidal
amplitude in the study area would be
interesting. A small area of the Savannah
River basin in South Carolina surveyed by
McKenzie and Badger (1969) indicated an
extremely high oyster reef density (9%),
Lunz (1943) reported an extremely high
density of reefs along a 1-mi wide and
40-mi long strip surrounding the intra-
coastal waterway in South Carolina from
Charleston to the Santee River, He report-
ed that 33,6% of the total creek banks was
lined with reefs, Lunz (1943) also report-
ed that these reefs were populated by
about 136 oysters/yd^, (or about 114/m )
of 2-inch (50-mm) or larger sized oysters.
This represents a biomass of approximately
50 g/m^ afdw, much lower than that for the

62

more mature reefs described in Georgia.
Lehman (1974) reported that oyster reefs
in the Crystal River estuarine ecosystem
in West Florida occupied about 3% of the
total surface area.

To put these various estimates in
perspective, it must be remembered that
different survey techniques were used, and
that some subjectivity is involved in dis-
tinguishing viable reefs from areas of
dead shell. Whether or not a major de-
cline in oyster reefs has occurred since

1899, the present proportion of reef area
to marsh-estuarine area throughout the
study area appears to be between 0.04% and
0.06%, with some local variation. The reef
community's occupying such a small propor-
tion of the total marsh-estuarine area may
reflect both the very specific physico-
chemical requirements of the reef commun-
ity and the limited productive capacity of
the total system in supporting the high,
heterotrophic demands of the oyster com-
munity.

63

An example of Spartina marsh invading the top levels of an oyster reef. Photo by
Rhett Talbert, University of South Carolina.

64

CHAPTER 5. CONCEPTUAL MODELS OF THE INTERTIDAL
OYSTER REEF COMMUNITY

5.1 OBJECTIVES AND LEVELS OF RESOLUTION

This chapter summarizes some conclu-
sions, primarily qualitative, about the
significance of oyster reefs to the coast-
al ecosystem in the study area. The sum-
mary is in the form of a set of three con-
ceptual models that are explicit diagram-
matic illustrations of the interactions
among oyster reefs and other salt marsh
ecosystem components. Conceptual models
can provide succinct, qualitative expres-
sions of the feedback pathways, forcing
functions, and major interconnections
characterizing a particular ecosystem.
Conceptual models are usually over-simpli-
fications of the real world, but their
formulation may indicate deficiencies of
information that can become future re-
search goals. Conceptual models take a
variety of forms, from simple box and ar-
row diagrams to detailed and complex "spa-
ghetti" diagrams that are difficult to
interpret. Figure 18 (from Odum 1971)
illustrates one conceptual model of an
oyster reef that compares it in functional
terms to a city.

Oyster reef organization and function
must be considered at different levels of
space and time, and our conceptual models
are presented at three (hierarchical) lev-
els of resolution: a regional level, a
drainage unit level, and a reef level
(Figure 19). The regional level model
treats the oyster reef system over the
entire study area or a large portion of
the study area. At the regional level,
detailed reef community information is
relatively unimportant compared with that
of long-term geological processes affect-
ing regional ecology. The relative propor-
tions of salt marsh, open water, and total
reef area and patterns of their spatial
distribution are particularly significant
at the regional level since these factors
are regulated by long-term geological pro-
cesses.

The second level of resolution is on
a smaller and more detailed scale — that of

a single marsh-estuarine drainage unit.
For example. Figure 20 shows the oyster
reef distribution in the Half Moon River
estuary on Wilmington Island, Georgia.
This tidal river and its surrounding salt
marsh watershed exemplify a "typical" lo-
cal drainage unit in which oyster reefs
are distributed in a nonrandom pattern.
At this intermediate scale of resolution,
the reef community is more visible than at
the regional level and presumably exerts a
more profound short-term influence on the
local ecosystem. Another example of the
resolution achievable at this level may be
seen in Figure 21. The information content
at this scale is such that only broad spa-
tial patterns of reef distribution within
the marsh-estuarine ecosystem are discern-
able. The perspective, then, is an "over-
view." At scales smaller than this (great-
er resolution), the oyster reef system is
obscured.

The third conceptual level of resolu-
tion is of a discrete reef and its immedi-
ate surroundings. At this level, a reef
can be considered analogous to an individ-
ual in a "population" of reefs, each mem-
ber being influenced by local forcing
functions--hydrologic forces, short-term
episodic events, and biological phenomena,
such as spawning events and predation.
An individual reef is subject to local
phenomena, and its influence is primarily
restricted to its immediate surroundings.
The purpose of the third level conceptual
model is to summarize the specific phenom-
ena regulating the welfare of a given
reef. The cumulative effects of the "pop-
ulation" of reefs in a drainage basin are
addressed at the drainage unit level.

Some important differences among the
above three conceptual levels of organi-
zation and function of oyster reefs in the
study area are summarized in Table 8. The
three different scales of resolution are
discussed in Sections 5.2, 5.3, and 5.4.

Symbols used in the models were de-
veloped by H.T. Odum (1971) as a shorthand

65

Figure 18. Comparison of two systems of concentrated consumers whose survival
depends on strong flows that bring in fuels and oxygen and outflow wastes: (a)
reef of oysters and other marine animals characteristic of many estuaries; (b)
industrialized city (adapted from Odum 1971).

66

DUPLIN RIVER

DRAINAGE BASIN LEVEL

INDIVIDUAL REEF LEVEL

Figure 19. Three hierarchical levels of oyster reef organization.

57

Figure 20. Reef distribution in a single drainage basin, the Half Moon River
Estuary, Wilmington Island, Georgia. Reefs are indicated by bold, black lines.

68

Figure 21. Recent and historical reef distribution in the Duplin River Estuary,
Sapelo Island, Georgia (adapted from Bahr 1974 and Drake 1891).

69

Table 8. Time scales relating ecosystem processes and components at
the three conceptual levels of oyster reef organization and function.

Regional level

Drainage unit level

Reef level

Factors

Approximate time scale

1x10^ to 1x10^

yr

1 to 100 + yr

<1 to 25 yr

System
components

Intertidal area
Marsh area
Reef area
Mudflat area
Water surface area

Wetland area
Water area

Phytoplankton biomass
Reef area
Reef biomass
Suspended load

High (mature) reef area
Low (mature) reef area
Suspended load (POC and
inorganic carbon)
Reef biomass
Predator component
Oyster larvae
Nutrient pool

Forcing Sea level rise

functions Latitude-tidal

pattern

Lati tude-temperature

regime

Riverine sediment

input

Marine input-salts

Marine inputs-storm

energy

Solar

Tidal

currents

Sediment,

riverine

insolation

and wind-driven

marine or

Local tidal regime
(amplitude and period)
Currents (tidal and wind)
Temperature effects
Sediment input
POC input

Important
system
processes
related to
reefs

Areal trade offs
among wetlands,
waterbodies, and
reefs

Physiographic changes
in basin caused by
reefs

Reef growth (vertical)

Reef growth (lateral )

Water clearance and

biodeposition

Mineralization and nutrient

release

Hydrologic damping by reefs

70

for expressing the functional connections
in many different kinds of systems to com-
pare these systems in thermodynamic
(energy flow) terms. Odum calls the short-
hand "energese," and it is becoming more
popular, as evidenced by its increasing
use in published reports. This shorthand
"language" is flexible and information-
rich, and it can be used in both qualita-
tive conceptual models and in quantitative
"working" models. The symbols are defined
in Figure 22, taken from Odum (1971).

5.2 REGIONAL LEVEL CONCEPTUAL MODEL

The regional level model of oyster
reef function in the study area is broad
in its coverage and necessarily quite
simple. At this level of resolution, oys-
ter reefs were probably not a major factor
in the geomorphological development of the
area, although their wide surface distri-
bution and largely unknown subsurface
(fossil) distribution indicate that they
indeed may have played a geological role.
No one has as yet quantified the physical
importance of oyster reefs to long-term
coastal processes.

In Figure 22 we illustrate the theo-
retical role of oyster reefs at this broad
regional scale. As indicated in Table 8,
the time-scale of change at the regional
level is in the geological range, outside
the realm of control of environmental
managers (although not immune to cultur-
ally induced alteration).

The major process symbolized in the
regional scale conceptual model is the
dynamic tradeoff in area between inter-
tidal and subtidal zones. Oyster reefs
primarily are distributed at the interface
between these two zones, and thus the reef
"fringe" partially reflects the outline of
the marsh-water interface throughout the
study area. Changes in the position of
this outline are a function of such long-
term processes as subsidence, sea level
rise, and sedimentation regimes. For all
practical purposes, reef distribution at
the regional level can be considered spa-
tially homogeneous.

Interactions between the intertidal
and subtidal zones are described in the

order of the work gates (1-4) shown in
Figure 22.

(1) A gradual and persistent rise in
sea level (about 4 mm/yr) has
occurred since the relative sta-
bilization of mean water level
(MWL) following the last ice
age. This has resulted in a con-
stant encroachment upon the in-
tertidal zone by open water. In
the absence of other processes,
the intertidal zone would even-
tually become open water.

(2) The loss of intertidal area is
accelerated by erosion from
strong tidal currents and storm
surges.

(3) Losses of intertidal habitat are
offset in most undisturbed por-
tions of the study area by in-
puts of sediment from rivers
and/or from the marine system.
This sedimentation process is
augmented by increases in the
volume of estuarine basins as a
function of sea level rise. Mean
water current velocities decline
as volume increases, and sedi-
mentation is enhanced.

(4) Latitude determines tidal ampli-
tude in the study area, which,
in conjunction with sediment
sources, regulates the deposi-
tional patterns.

5.3 DRAINAGE UNIT LEVEL CONCEPTUAL MODEL

The components and interrelationships
of a marsh estuary drainage unit including
and affected by oyster reefs are shown in
Figure 23. A major assumption at this lev-
el of resolution is that there is an opti-
mum ratio of wetlands and open water
which, in conjunction with tides, support
the oyster reef area in a given drainage
basin. One implication of this assumption
is that relative reef area in a given
drainage unit is limited by ecosystem lev-
el processes, (e.g., the relationship be-
tween the velocity of tidal currents, the
cross-sectional area of tidal creeks, and
the distribution of reefs). This thesis is

71

WETLAND AREA
MUDFLAT AREA
OYSTER REEF AREA 1

TOTAL
INTERTIDAL
AREA

Driving force or onergv source - indicates 8 lource of energy outtide the tyitem under consideration. Example: Staady
flowing source - rive rjvari able source - sunlight.

^ X X^ ^ Energy or material storage tank — indicates passive storage of energy or matter within the system. Example: energy itorad
^\^^ / in a water tank: water contained with an estuarine basin.

Interaction or work gate - indicates the interaction of two or more types of energy required for a process. Example: fer-
tilizer requirements for plant growth.

Production unit or green plants — indicates the processes, interactions, storage, etc., involved in producing high-quality
energy from dilute sources like sunlight. Example: biomass of green plants.

^

>l/ HMt sink — energy lottet to heat according to the Mcond law of tharmodynamics.

Figure 22. Regional level conceptual model and explanation of symbols,

72

Figure 23. Drainage unit level conceptual model.

73

supported by the relatively static distri-
bution of reefs within the Duplin River
basin over time, shown in Figure 21.

Specific interactions shown in Figure
23 are described below:

(1) The local tidal regime is the
primary forcing function for
oyster reef distribution (and
relative area) in a given salt
marsh drainage unit. The tidal
effect is shown interacting si-
multaneously with water area and
wetland area. These respective
components (water and wetlands)
have a 1 to 2 ratio in the Geor-
gia marsh-estuarine ecosystem
(Pomeroy and Wiegert 1980). The
pattern of distribution of oys-
ter reefs in the Duplin River,
as shown in Figure 21, is prob-
ably not a chance distribution.
For example, oyster reefs are
absent from the upper one-fourth
of the basin, probably because
of ecosystem level processes
(e.g., a function of reduced
current velocities in the upper
reaches of the river).

(2) Oyster reef area in a given lo-
cale can affect local turbidity
levels by filtration and bi ode-
position. By stabilizing and
elevating sediment, wetland de-
velopment can be enhanced. Marsh
grass and oyster reefs have a
reciprocal functional relation-
ship in that reefs develop al-
most exclusively at the inter-
face between wetland and water.
There they subsequently grow and
trap sediment, eventually becom-
ing colonized by Spartina. The
marsh invades formerly subtidal
areas in this leapfrog fashion.
For example, subsurface (fossil)
oyster reefs occur in a pattern
of increasing depth extending
from an existing reef into the
marsh. (S. Stevens, University
of Georgia Marine Institute,
Sapelo Island; pers. comm. ).

(3) Suspended materials in water
column inhibit the primary pro-
duction by phytoplankton as a

result of shading. Therefore,
oyster reefs theoretically aug-
ment phytoplankton productivity
by actively filtering these
materials and thereby reducing
turbidity.

(4) Oyster reefs in local areas also
contribute to primary production
(especially of phytoplankton and
benthic algae) by rapidly miner-
alizing ingested organic matter
into usable plant nutrients.
Kuenzler (1961) showed that the
regeneration of phosphorus by
mussels in the salt marsh was
more important than their role
in energy transformation. Kit-
chell et al. (1979) discussed
the roles of consumers in nutri-
ent cycling. Oyster reefs by
Interactions (3) and (4) can
increase food availability, pro-
viding feedback in keeping with
ecosystem theory, (e.g., Odum
1971).

(5) Tidal currents maintain extreme-
ly high suspended sediment loads
in some study area estuaries,
like the Duplin River (Hanson
and Snyder 1979). The conse-
quences of this siltation relate
to Interactions (2) and (3).

5.4 REEF LEVEL CONCEPTUAL MODEL

The third conceptual model is shown
in Figure 24, where reef development is
expressed as growth in three dimensions:
(1) upward toward the high intertidal
zone, (2) downward toward the subtidal
zone, and (3) lateral accretion.

The interactions involved in such
changes are described below:

(1) Ingestion by oysters and other
suspension-feeding members of
the reef community is affected
negatively by increased water
turbidity (Section 2.3).

(2) Turbidity of estuaries in the
study area is usually high and
closely related to the high
tidal current regime. Thus,

74

<u
-a
o

■i->

Q.
<U

u

c
o
o

N
■r-

(O

en
s-
o

CM

0)

S-
=3

75

currents indirectly can reduce
oyster feeding.

(3) Currents have been shown, how-
ever, to positively affect oys-
ter ingestion (Walne 1972). Thus,
an optimum low-current level
probably exists to stimulate
oyster feeding with a minimum of
sediment erosion.

(4) Eroded sediments in the water
column can settle out on a reef
and bury the lower level oys-
ters, causing a decline in reef
viability. Sediment input by
currents, coupled with a high
rate of biodeposition, can suf-
focate all but the uppermost
oysters in a reef.

(5) Oyster reef growth in a positive
vertical direction is limited
absolutely by the local tidal
amplitude. The highest portions
of the reefs examined at Sapelo
Island were limited to 1.5m
above MLW, corresponding to a
daily inundation tim.e of only
8 hours, or conversely, to an
exposure time of 16 hours,

(6) Lateral extension of oyster
reefs apparently occurs at a
rate limited by suitable sub-

strate at the proper elevation
in the intertidal zone, by water
currents, and by available food.

(7) In addition to a minimum inunda-
tion time, vertical reef growth
is also subject to temperature
stress in the study area (ex-
tremely cold spells and hot
spells during reef exposure).

(8) Reef crowding appears to buffer
temperature stress and to allow
vertical reef accretion beyond
the maximum level at which indi-
vidual oysters survive.

(9) Downward extension of oyster
reefs toward the subtidal zone
appears limited by increased
predation, fouling, and shell
erosion by boring sponges.

(10) Predation by filter feeding
organisms, nektonic, and epiben-
thic, reduces the available pool
of oyster larvae and perhaps
prevents overcrowding.

(11) The gregarious behavior of oys-
ter larvae ensures a new crop of
spat to replenish mortality
losses and maintain the viabil-
ity of existing reefs.

76

ir.\

'*>.

n

•ij

4i> ^

<\

rj

'^:

*:j^'

m

i^A

3i^

V

h

^

w

t i^^k

Wsk

w%r*. l«-^

Immature reef at the mouth of an intertidal creek. Note the
mature reefs in the background. Photo by Rhett Talbert, Uni-
versity of South Carolina.

77

The seeding of intertidal oyster beds with oyster shell to induce increased
oyster spat settlement in areas that are being commercially harvested. Photo
by South Carolina Wildlife and Marine Resources Department.

78

CHAPTER 6. SUMMARY AND MANAGEMENT IMPLICATIONS AND GUIDELINES

6.1 SUMMARY AND OYSTER REEF SIGNIFICANCE

The American oyster (Crassostrea vir-
qlnica) is not only an extremely valuable
commodity to man but is also a cosmopol-
itan, physiologically plastic, and ecolog-
ically interesting estuarine organism.
Its natural range spans the Atlantic coast
and much of the gulf coast, and its ge-
neric "brothers" exist in coastal systems
worldwide.

One intriguing aspect of oyster be-
havior is its propensity, under certain
conditions, to form massive, discrete,
intertidal colonies, or reefs. The larg-
est individual oyster reefs formed by the
American oyster occur in open bays along
the northern gulf coast. Some reefs are
many kilometers in length; they consist
mainly of dead shells, and their geometry
is partially the result of reworking by
storm surges.

In the South Atlantic Bight, tidal
amplitude ranges from 1 m to over 3 m (3
to 10 ft), and oyster reefs occur in close
association with extensive salt marshes
characteristic of the area. Oyster reefs
within this region achieve a greater ele-
vation above mean sea level and a greater
oyster density (in terms of numbers and
biomass) than in any other coastal region.
The structure and ecological function of
these reefs are the subjects of the pre-
vious five chapters.

Whereas most oyster research has been
carried out at the individual or popula-
tion level of detail, this paper has em-
phasized the behavior of the oyster at the
ecosystem level. The reef community de-
scribed throughout this community profile
exhibits characteristics and has ecosystem
importance that could not be predicted
from even "perfect" knowledge of the bio-
logy of individual oysters. Thus, just as
a termite colony is more than a collection
of termites, so an oyster reef shows emer-
gent properties, including its capability
of extending the intertidal range of the
reef assemblage upward beyond the eleva-
tion at which individual oysters normally

could survive. Oyster reefs possess the
following characteristic properties: (1)
individual oysters in a reef must grow
with a strong vertical orientation to sur-
vive; (2) individual reefs strictly are
limited to the intertidal zone, and the
geometry of a given reef is strongly
determined by mean water level, sediment
stability, and current regime; and (3)
patterns of reef distribution are discern-
able within drainage basins, such that
reef density is usually maximal at inter-
mediate channel widths and current veloc-
ities. In other words, if all living oys-
ters in a drainage basin were redistrib-
uted either randomly or homogeneously
throughout the ecosystem, a large portion
of the function (and value) of the oyster
community would be lost.

One primary ecosystem value of the
oyster reef community relates to its phys-
ical, rather than its biological, proper-
ties. Mature reefs are stabilizing influ-
ences on erosional processes and may mod-
ify long-term changes in tidal stream flow
and overall marsh physiography, although
these effects have not been quantified
yet.

The extent of the physical influence
of reefs on the marsh system is a function
of the average relative proportion of reef
area to total intertidal area in a given
drainage basin. The available estimates
of this relationship vary, but about 0.05%
of reef area to total intertidal area
(marsh and water) may be a reasonable
estimate.

Another aspect of the ecosystem value
of oyster reefs relates, in natural estua-
rine areas, to reefs' being stable islands
of hard substrate in an otherwise unstable
soft muddy environment. These islands are
essential habitat for some organisms,
especially the sessile suspension-feeding
epifauna usually limited by the available
surface area. Reefs also provide a highly
irregular surface with crevices that serve
as havens for motile invertebrates; and
some small fish use reefs for shelter
during flood tides. Oyster reefs are

79

Photo indicates the "soupy" nature of the sediments that oft times support oyster
reefs. The reefs represent a hard substrate "island" habitat in an otherwise soft-
bottomed environment. Photo by Leonard Bahr, Louisiana State University.

80

densely populated with mussels, mud crabs,
polychaetes, barnacles, and other macro-
fauna, and countless smaller metazoa, pro-
tozoa and bacteria.

The members of the oyster reef com-
munity are limited primarily to suspension
and deposit feeding macrofaunal consumers.
The trophic role of this macrofaunal com-
munity as a whole assimilates carbon de-
rived from phytoplankton and detrital
sources and makes it available to higher
consumers, i.e, terrestrial and aquatic
animals. Of the former, raccoons and
birds like oyster catchers and grackles
are predators on oyster reefs. Aquatic
consumers that prey on healthy living oys-
ters include the blue crab (Callinectes
sapidus) and the black drum (Poqonias
cromis). Many other aquatic carnivores
undoubtedly visit oyster reefs during
flood tides and prey on the host of small
invertebrates residing there.

More important than the food web
roles of oyster reef inhabitants in the
salt marsh estuarine system is their role
in mineralizing organic carbon and releas-
ing nitrogen and phosphorus in forms
usable by the primary producers. The
significance of the energetic roles of the
reef community is exemplified by the meta-
bolic rates of the entire community being
among the highest measured for any benthic
community (27,000 kcal/m2/yr). This rate
is partly due to the great surface area in
a reef, supporting a large population of
aerobic bacteria, and to the high biomass
of the resident macrofauna (up to 1,100 g
afdw/m2).

Each summer the reef community con-
tributes a stream of high quality protein
to the water column in the form of gametes
and larvae of oysters and other resident
macrofauna. These meroplankton (or larvae)
are food for nektonic filter feeders, food
for other benthic organisms, and recruits
for the next generation of reef oysters
and associates. Because reefs continually
subside into the mud, new generations of
oysters at the top are necessary to main-
tain the steady state elevation of the
upper reef surface.

Oyster growth in mature reefs appears
extremely slow, and some of the larger
resident oysters probably are 5 to 10 or

more years of age. They are typically long
and narrow and usually display a watery
condition with little glycogen reserves, a
sign of stress or being spawned out.

Because oysters in reefs apparently
live close to their stress tolerance
threshold, further perturbation by man can
easily destroy the entire reef community.
Reefs are particularly susceptible to
artificial hydrologic changes, such as
those that follow the impoundment or
diversion of waterbodies as large as
coastal rivers or as small as individual
tidal streams. Reefs primarily are found
at the interface between wetland and open
water, and the destruction of wetlands for
any reason results in a decrease in this
interface zone. Oysters and other benthic
macrofauna are, of course, also connected
to and depend upon wetland macrophytes via
trophic pathways still not well under-
stood.

Reef oysters are susceptible to the
increasing array of man-made chemicals and
heavy metals becoming more prevalent in
coastal waters. They are also vulnerable
to the eutrophic effects of fertilizer-
and sewage-loading in coastal waters
through the potential alteration of the
composition of the natural phytoplankton
community in a manner that may be less
desirable or even toxic to oysters.

Reef oysters have evolved to tolerate
high levels of turbidity, but increased
sedimentation on top of natural levels can
smother them. Dredging related to shell
or phosphate mining, navigation or pipe-
line canals, or other construction activi-
ties in the coastal zone can drastically
increase the natural sediment load in
local areas. In addition, the artificial
mixing of reduced bottom sediments with
water above the bottom can deplete the
water column of its dissolved oxygen.

Direct physical alteration of mature
oyster reefs, e.g., by harvesting, can
destroy an entire reef, even if the reef
is only moderately disturbed. Harvest of
intertidal oysters is productive only on
immature oyster reefs low in the inter-
tidal zone, where oysters are not as
crowded as in mature reefs and where
growth is more rapid. Thus, mature reefs
are most valuable to the ecosystem and to

81

society if
rather than
food value.

they are
harvested

left undisturbed,
for their limited

6.2 MANAGEMENT IMPLICATIONS AND GUIDELINES

Clearly, the oyster reef component of
the coastal ecosystem in the Southeastern
United States depends on a healthy marsh-
estuarine environment. Thus, the most
logical recommendation for reef management
is to mitigate increasing man-induced
alterations on the marsh system to the
extent possible. Changes in water flow,
both surface and subsurface, appear to
cause the most far reaching and cumulative
damage to the entire system, and thus
indirectly to the reef subsystem. See
Table 1 for a summary of cultural stress
on oysters.

The maintenance of high water quality
is, of course, important to the continued
viability of oyster reefs; and the intro-
duction of urban, industrial, and agricul-
tural pollutants from both point and non-
point sources is to be avoided. Subtidal
oysters normally can tolerate a fair
amount of insult in terms of poor water
quality before succumbing to many of the
common pollutants. Such oysters usually
become dangerous to eat before they die
from chemical pollution. Reef oysters, on
the other hand, are already stressed and
may not be as hardy. At present, the oys-
ter reef zone of the South Atlantic Bight
appears relatively free of toxic chemicals
and excess nutrients, except in the immed-
iate vicinity of major population centers
such as Savannah, Georgia, and Charleston,
South Carolina.

Long-term effects of increasing
freshwater pumping may pose a problem more
serious than pollution for the marsh oys-
ter reef system. Therefore, future urban,
industrial, and agricultural requirements
for freshwater need to be examined and
their long-term effects on salinity dis-
tribution predicted, in order to under-
stand the implications of development for
the entire coastal ecosystem.

There have been several proposals and
attempts to increase oyster reef area
locally by spreading cultch along the
fringe between marsh and water to induce
oyster settlement. These efforts have
been largely unsuccessful, implying that
our thesis is valid; that is, the distri-
bution of reefs relates to a specific set
of conditions, especially with respect to
water flow, and the proportion of a marsh
drainage unit occupied by oyster reefs is
not indefinitely expandable. The guide-
line derived from these observations is
that artificial oyster reef development
should be seriously attempted only at
former reef sites.

In conclusion, the intertidal oyster
reef subunit of the marsh estuarine eco-
system is an important component of the
coastal zone in the Southeastern United
States, and this subunit has declined in
total area during the last 90 years. We
can only guess at the consequences of the
continued loss of reef area, but these
effects could be both obvious and subtle,
and could definitely result in an ecosys-
tem less healthy, rich, and productive,
and certainly less interesting from an
aesthetic point of view.

82

REFERENCES

Abbott, R. T. 1974. American seashells:
the marine mollusca of the Atlantic
and Pacific coasts of America. Van
Nostrand-Reinhold Co., New York.
2nd ed.

Ahmed, H. 1975. Speciation in living oys-
ters. Adv. Mar. Biol. 13:357-397.

Amemiya, I. 1936. Effect of gill exci-
sion on the sexual differentiation of
the oyster, Ostrea gigas Thunberg
(Japanese) (English abstract). Nippar
Gak, Kyok. H. 10(4) :1023-1026. Abst.
Jpn. J. Zool. 6:84 on Rec. Oceanog.
Works Japan 8(2):237.

Asif M. 1979. Hermaphroditism and sex
reversal in the four common oviparous
species of oyster from coast of Ka-
rashi. Hydrobiologia 66(1 ):49.

Bahr, L. M., Jr. 1974. Aspects of the
structure and function of the inter-
tidal oyster reef community in Geor-
gia. Ph.D. Dissertation. Univer-
sity of Georgia, Athens.

Bahr, L. M., Jr. 1976, Energetic aspects
of the intertidal oyster reef com-
munity at Sapelo Island, Georgia
(U.S.A.). Ecology 57(1 ): 121-131 .

Bahr, L. M., and R. E. Hillman 1967. Ef-
fects of repeated shell damage on
gametogenesis in the American oyster,
Crassostrea virginica (Gmelin). Proc.
Natl. Shellfish. Assoc. 57:59-62.

Banse, K. , F. H. Nichols, and 0, R. May.
1969. Oxygen consumption by the sea-
bed III. On the role of the macro-
fauna at three stations. Vie Milieu,
Supp. 22A:l:31-52.

Barnes, H., and M. Barnes. 1969. Seasonal
changes in the acutely determined
oxygen consumption and effect of
temperature for three common cirri-
pedes, Balanus balanoides (L.), B^.
balanus (L.), and Chthamalus stella-
J.

Beach, N. W. 1969. The oyster crab Pin-
notheres ostreum Say, in the vicinity
of Beaufort, North Carolina. Crusta-
ceana 17(2): 187-199.

Bernard, F. R. 1974. Annual biodeposi-
tion and gross energy budget of
mature Pacific oysters Crassostrea
gigas. J. Fish. Res. Board. Can..
3UJJ-- 185-190.

Bishop, J. W., and L. M. Bahr. 1973. Ef-
fects of colony size on feeding by
Lophopodella carteri (Hyatt). Pages
433-437 j_n Boardman, Cheatham, and
Oliver, eds. Animal colonies. Dowden,
Hutchinson and Ross, Inc. Strouds-
burg, Pa.

Bowden, K. F. 1967. Circulation and diffu-
sion. Pages 15-36 j_n G. H. Lauff, ed.
Estuaries. Am. Assoc. Adv. Sci.Publ. 83.

Bugg, J. C, Jr., J. E. Higgins, and E. A.
Robertson, Jr. 1967. Chlorinated
pesticide levels in the eastern oys-
ter (Crassostrea virginica) from se-
lected areas of the South Atlantic
and Gulf of Mexico. Pestic. Monit.
J. 1 (3):9-12.

Buroker, N,

W. K. Hershberger, and

K. K. Chew. 1979. Population gene-
tics of the family ostreidae 2. In-
traspecific studies of the genus
Crassostrea and Saccostrea. Mar.
Biol. 54(2):171.

Butler, R. W. , and J. W. Kirbyson. 1979.

Oyster predation by the black oyster

catcher in British Columbia. Condor
81(4):433.

Chan, T. D., and L. B. Trott
collembolan, Oudemansia
intertidal marine

1972. The

esakii, an

insect in Hong

tus
T176.

TPoli),
•50.

Mar. Biol. Ecol,

Kong, with emphasis on the floatation
method of collection. Hydrobiologia
40(3):335-343.

Cleary, W. J., P. E. Hosier, and G. R.
Wells. 1979. Genesis and signi-
ficance of marsh islands within

84

southeastern marsh island lagoons.
J. Sediment. Petrol. 49:703-710.

Collier, A., S. M. Ray, A. W. Magnitsky,
and J. 0. Bell. 1953. Effect of
dissolved organic substances on oys-
ters. U. S. Fish Wildl. Serv. Fish.
Bull. 54:167-185.

Connell, J. H. 1961. The influence of
interspecific competition and other
factors on the distribution of the
barnacle Chthamalus stel latus. Ecol-
ogy 42(4):710-723.

Copeland, B. J., and H. D. Hoese. 1966.
Growth and mortality of the American
oyster, Crassostrea virqinica, in
high sal inity shallow bays in central
Texas. Publ. Inst. Mar. Sci. Univ.
Tex. 11: 149-158.

Dame, R. F. 1972a. Comparison of various
allometric relationships in inter-
tidal and subtidal American oysters.
Fish. Bull. 70(4)1121-1126.

Dame, R. F. 1972b. The ecological ener-
gies of growth, respiration, and
assimilation in the American oyster,
Crassostrea virqinica. Mar. Biol.
17:243-250.

Dame, R. F. 1976. Energy flow in an
intertidal oyster population. Estua-
rine and Coastal Marine Science.
4243:283.

Dame, R. F. 1979. The abundance, diver-
sity and biomass of m.acrobenthos on
North Inlet, South Carolina, inter-
tidal oyster reefs. Proc. Natl.
Shellfish. Assoc. 69: 6-10.

Costanza, R. 1980. Embodied energy and
economic valuation. Science 210:
1219-1224.

Coull B. C, and S. S. Bell. 1979. Per-
spectives of marine meiofaunal ecol-
ogy. Pages 548 2£ R. J. Livingston,
ed. Ecological processes in coastal
and marine systems. Marine Science
Series, Vol. 10. Plenum Press, New
York.

Cowardin, L. M., V. Carter, F. C. Golet,
and E. T. LaRoe. 1979. Classifica-
tion of wetlands and deepwater habi-
tats of the United States. U.S. Fish
and Wildlife Service, Biological Ser-
vices Program, Washington, D.C. FWS/
OBS-79/31. 103 pp.

Crisp. D. J., and P. S. Meadows. 1962.
The chemical basis of gregariousness
in Cirripedia. Proc. R. Soc. Biol.
156: 500-520.

Crisp, D. J., and P. S. Meadows. 1963.
Adsorbed layer: the stimulus to set-
tlement in barnacles. Proc. R. Soc.
Biol. 158:364-387.

Dame, R. F. 1970. The ecological energies
of growth, respiration, and assimila-
tion in the intertidal American oys-
ter, Crassostrea virqinica (Gmelin).
Ph.D. Dissertation. University of
South of Carolina, Columbia.

Darnell, R. M. 1961. Trophic spectrum of
an estuarine community based on stud-
ies of Lake Pontchartrain, Louisiana.
Ecology 42(3):553-568.

Davies, J. L. 1964. A morphological
approach to world shorelines. Z.
Geomorphol. 8:127-142.

Day, J. H. 1951. The ecology of South
African estuaries. R. Soc. So. Afr.,
Trans. 33(1):53-91.

Dean, B. 1892. The physical and biologi-
cal characteristics of natural oyster
grounds of South Carolina. Bull,
U.S. Fish. Comm. 10:335-362.

Dorjes, J., and J. D. Howard. 1975. Estu-
aries of the Georgia coast, U.S.A.:
sedimentology and biology. IV, Flu-
vial-marine transition indicators in
an estuarine environm.ent, Ogeechee
River-Ossabaw Sound, Senckenb.
Marit. 7:137-179.

Drake, G. C. 1891. On the sounds and
estuaries of Georgia with reference
to oyster culture. U.S, Coast and
Geodetic Survey Bull. 19:179-209.

Drinnan, R. E. 1957. The winter feeding
of the oyster catcher (Haematopus
ostraleous) on the edible cockle
(Cardium "edule). J. Anim. Ecol. 26:
441-469.

85

Dunnington, E. A., Jr. 1968. Survival
time of oysters after burial at var-
ious temperatures. Proc. Natl. Shell-
fish. Assoc. 58:101-104.

Epifanio, C. E. 1979. Growth in bivalve
molluscs: nutritional effects of two
or more species of algae in diets fed
to the American oyster Crassostrea
virqinica (Gmelin) and the hard clam
Mercenaria mercenaria (L.). Aquacul-
ture 18(1):1.

Fenchel, T. M., and R. J.
The sulfide system:
community underneath
layer of marine sand
Biol. 7(3):255-268.

Riedl. 1970.

a new biotic

the oxidized

bottoms. Mar.

Finley, R. T. 1975. Hydrodynamics and
tidal deltas of North Inlet, South
Carolina. Pages 277-291 in L. E.
Cronin, ed. Estuarine research. Vol.
2. Academic Press, New York.

Frankenberg, D., and C. Westerfield. 1968.
Oxygen demand and oxygen depletion
capacity of sediments from Wassaw
Sound, Georgia. Bull. Ga. Acad. Sci.
26(4):160-172.

Galtsoff, P. S. 1964
ter Crassostrea
U

,S. Fish
64:1-480.

The American oys-
virginica (Gmelin),

Wildl. Serv. Fish. Bull,

Galtsoff, P. S., and R. H. Luce. 1930.
Oyster investigations in Georgia.
Doc. 1077, App. V, Rep. U.S. Comm.
Fish. 1930: 61-100.

Ghiretti, F. 1966. Respiration. Pages
175-208 in K. M. Wilbur and C. M.
Yonge, eds. Physiology of mollusca.
Vol. 2. Academic Press, New York.

Gilfillan, E. S. 1975. Decrease of net
carbon flux in two species of mussels
caused by extracts of crude oil. Mar.
Biol. 29:53-57.

Gosselink, G., C. L. Cordes, and J. W.
Parsons. 1979. An ecological charac-
terization study of the Chenier Plain
Coastal Ecosystem of Lousiana and
Texas. 3 vols. U. S. Fish and Wild-
life Service, Office of Biological
Services, Washington, D.C. FWS/OBS-
79/9 through 78/11.

Gracy, R. C, and W. J. Keith. 1972. Sur-
vey of the South Carolina oyster
fishery. S.C. Wildl. and Mar. Re-
sources Dept. Tech. Rep. 3. 28 pp.

Gracy, R. C, W. T. Keith, and R. T.
Rhodes. 1978. Management and devel-
opment of the shellfish industry in
South Carolina. S. C. Mar. Resource
Center. Tech. Rep. 28.

Grave, C. 1905. Investigations for the
promotion of the oyster industry of
North Carolina. Pages 247-329 in
Report of the U.S. Fish Commission
for 1903.

Green, R. H., and K. D. Hobson. 1970.
Spatial and temporal structure in a
temperate intertidal community, with
special emphasis on Gemma gemma
(Pelecypoda: Mollusca). Ecology 5(6):
999-1011.

Greig, R. A., and D. Wenzloff. 1978.
Metal accumulation and depuration by
the American oyster Crassostrea
virginica. Bull. Environ. Contam.
Toxicol. 20: 499-504.

Grinnell, R. S., Jr. 1971. Structure and
development of oyster reefs on the
Suwannee River Delta, Florida. Ph.D.
Dissertation. State University of
New York, Binghamton. 186 pp.

Guida, Vincent G. 1976. Sponge predation
in the oyster reef community as dem-
onstrated with Cliona celata Grant.
J. Exp. Mar. Biol. Ecol. 25:109-122.

Guilcher, A. 1967. Origin of sediments
in estuaries. Pages 149-157 in 6. H.
Lauff, ed. Estuaries. Am. Assoc.
Adv. Sci. Publ. 83.

Gunter, G. 1951. The West Indian tree on
the Louisiana coast, and notes on
growth of the gulf coast oysters.
Science 113:16-517.

Gunter, G. 1967. Origin of sediments in
estuaries. Pages 149-157 in G. H.
Lauff, ed. Estuaries. Am. Assoc.
Adv. Sci. Publ. 83.

Gunter, G. 1979. The grit principle and
the morphology of oyster reefs. Proc.
Natl. Shellfish. Assoc. 69:1-5.

86

Haines, E. B. 1976. Stable carbon isotope
ratios in the biota, soils, and tidal
water of a Georgia salt marsh. Estu-
arine Coastal Mar. Sci. 4: 609-619.

Haines, E. B. 1977. The origins of de-
tritus in Georgia salt marsh estu-
aries. Oikos 29:254-260.

Haines E. B., and C. L. Montague. 1979.
Food sources of estuarine inverte-
brates analyzed using 13c 12c ratios.
Ecology 60: 48-56.

Hammen, C. S. 1969. Metabolism of the
oyster Crassostrea virqinica. Am.
Zool. 9:309-318.

Hanson, R. B., and J. Snyder. 1979. Mi-
croheterotrophic activity in a salt
marsh estuary, Sapelo Island. Ecol-
ogy 60(1): 99-107.

Harris, C. D. 1980. Survey of the inter-
tidal and subtidal oyster resources
of the Georgia coast. Publ. Ga. Dept.
Nat. Resources, Coastal Resources
Division, Brunswick. 44 pp.

Haven, D. S., and R. Morales-Alamo. 1967.
Aspects of biodeposition by oysters
and other invertebrate filter feed-
ers. Limnol. Oceanogr. 11:487-498.

Haven, D. S., and R. Morales-Alamo. 1970.
Filtration of particles from suspen-
sion by Amerian oyster Crassostrea
virqinica. Biol. Bull. 139(2): 248-
264.

Hayden, B. P., and R. Dolan. 1979. Bar-
rier islands, lagoons, and marshes.
J. Sediment. Petrol. 49:1061-1972.

Hayes, M. 0. 1975. Morphology of sand
accumulation in estuaries: an intro-
duction to the symposium. Pages 2-22
in L. E. Cronin, ed. Estuarine re-
search. Vol. 2. Academic Press, New
York.

Heck, K. L. 1976. Community structure
and the effects of pollution in sea-
grass meadows and adjacent habitats.
Mar. Biol. 35:345-357.

environmental
havior. Proc.
61:35-50.

factors and larval be-
Natl. Shellfish. Assoc.

Hillman, R. E. 1964. Chromatographic
studies of allopatric populations of
the eastern oyster Crassostrea vir-
qinica. Chesapeake Sci. 6(2):115-116.

Hixson, S. L. 1975. The South Carolina
oyster industry: an economic analy-
sis of institutional arrangements.
Masters Thesis. Clemson University,
Clemson, S.C.

Hochachka, P. W. ,
Invertebrate
sis. Science

and T. Mustafa. 1972.
facultative anaerobio-
178:1056-1060.

Hodgkin, E. P. 1959. Catastrophic de-
struction of the littoral fauna and
flora near Freemantle. West. Aust.
Nat. 7:6-11.

Howard, J. D. 1975. Estuaries of the
Georgia coast, U.S.A. Sedimentology
and biology. IX. Conclusions. Senc-
kenb. Marit. 7:297-305.

Howard, J. D., C. A. Elders, and T. F.
Heinbokel. 1975. Estuaries of the
Georgia coast U.S.A. Sedimentology
and biology. V. Animal-sediment re-
lationships in estuarine point bar
deposits Ogeechee River - Osssabaw
Sound, Georgia. Senckenb. Marit. 1:
181-203.

Howarth, R. W., and J
Sulfate reduction
salt marsh. Limnol ,
1013.

. M. Teal. 1979.

in a New England

Oceanogr. 24:999-

Hidu, H.

and H. Haskin. 1971. Setting

of the American oyster related to

Hubbard, D. K., G. F. Oertel , and D.
Nummendal. 1979. The role of waves
and tidal currents in the development
of tidal inlet sedimentary structures
and sand-body geometry: examples
from North Carolina, South Carolina
and Georgia. J. Sediment. Petrol. 49:
1073-1092.

Ingle, R. M. 1967. Artificial food for
oysters. Sea Frontiers 13(5):296-303.

Jackson, J. B. C. 1977. Habitat area,
colonization, and development of epi-
benthic community structure. Pages

87

349-358 In B. F. Keegan, T. 0.
Ceidgl, and P. J. S. Boaden, eds.
Biology of benthic organisms. Perga-
mon Press, New York.

Johannes, R. E., S. J, Coward, and K. L.
Webb. 1969. Are dissolved amino
acids an energy source for marine
invertebrates? Comp. Biochem. Phys-
iol. 29:283-288.

Kanwisher, J. W. 1962. Gas exchange of
shallow marine sediments. Univ. R.
I., Narragansett Mar. Lab. Occ. Pub.
1:13-19.

Keck, R., D. Maurer, and L. Watling. 1973.
Tidal stream development and its
effect on the distribution of the
American oyster. Hydrobiologia
42(4):369-379.

Keith, W. J., and R. C. Gracy. 1972.
History of the South Carolina oyster.
S.C. Wild!, and Mar. Resource Dept.
Educational Rep. 1.

Kennedy, A. V., and Battle, H. I. 1963.
Cyclic changes in the gonad of the
oyster. Crassostrea virginica (Gme-
lin) Can. J. Zool. 42(20) :305-321.

Kennedy, V. S. , and J. S. Mihursky. 1972.
Effects of temperature on the respi-
ratory metabolism of three Chesapeake
Bay bivalves. Chesapeake Sci. 13(1):
1-22.

community to a natural and severe
reduction in salinity. Proceedings
First International Congress of Ecol-
ogy: functioning and management of
ecosystems. The Hague, Netherlands,
8-14 Sept 1974. 414 p.

Lawrence, D. R. 1971. Shell orientation
in recent and fossil oyster communi-
ties from the Carol inas. J. Pale-
ontol. 45(2):347-349.

Lee, C. F., and F. B. Sanford. 1963. Oys-
ter industry of Chesapeake Bay, South
Atlantic, and Gulf of Mexico. Comm.
Fish. Rev. 25(3):8-17.

Lehman, M. E. 1974. Oyster reefs at
Crystal River, Florida and their
adaptation to thermal plumes. Ph.D.
Dissertation. University of Florida,
Gainesville. 197 pp.

Letsch, S. W., and R. W. Frey. 1980. De-
position and erosion in a holocene
salt marsh, Sapelo Island, Georgia,
J. Sediment. Petrol. 50(2) :529-542.

Levinton, J. 1972. Stability and trophic
structure in deposit-feeding and sus-
pension-feeding communities. Am.
Nat. 106(950):472-486.

Levinton, J. 1973. Genetic variation in
a gradient of environmental variabil-
ity: marine bivalva (Mollusca). Sci-
ence 180:75-76.

Ketchum, B. H. 1951. The exchanges of
fresh and salt water in tidal estu-
aries. J. Mar. Res. 10(l):18-38.

Kitchen, J. F., R. V. O'Neill, D. Webb,
G. W. Gallepp, S. M. Bartell, J. F.
Koonce, and B. E. Ausmus. 1979.
Consumer regulation of nutrient cycl-
ing. Bioscience. 291 (l):28-34.

Krauter, J. N.
salt marsh
35:215-223.

1976. Biodepositon by
invertebrates. Mar. Biol.

Kuenzler, E. J. 1961. Phosphorus budget
of a mussel population. Limnol.
Oceanogr, 6:400-415.

Larsen, P. F. 1974. Structural and func-
tional responses of an oyster reef

Li, M. F., and C. Fleming. 1967. Hemaglu-
tinin from oyster hemolymph (Crasso-
strea virginica). Can. J. Zool. 45:
1225-1234.

Lindemann, R. L. 1942. The trophic dyna-
mic aspect of ecology. Ecology 23(4):
399-418.

Linton, T. L. 1968. Inventory of the in-
tertidal oyster resources in Georgia.
Pages 69-73 jn^ T. Linton, ed. Fea-
sibility study of the methods for im-
proving oyster production in Georgia.
Completion rep. 2-10-R. Marine Fish-
eries Division, Ga. Game and Fish,
Comm. and Univ. of Ga. 158 pp.

Loosanoff, V. L. 1962. Effects of tur-
bidity on some larval and adult

88

bivalves. Proc.
Inst. 14:80-95.

Gulf Caribb. Fish.

Loosanoff, V. L., and J. B. Engle. 1946.
Effect of different concentrations of
micro-organisms on feeding of oysters
(C_. virqinica). Fish. Bull. 42.

Loosanoff, V. L., and C. A. Nomejko.
1955. Growth of oysters with damaged
shell-edges. Biol. Bull. 108(2):
151-159.

Loosanoff, V. L., and F. D. Tommers. 1948.
Effects of suspended silt and other
substances on rate of feeding of oys-
ters. Science 107(2768) :69-70.

Lund, E. J. 1957a. Self-silting by the
oyster and its significance for sedi-
mentation geology. Publ. Inst. Mar.
Sci. Univ. Tex. 4(2) :320-327.

Lund, E. J. 1957b. Effect of bleedwater,
"soluble fraction" and crude oil on
the oyster. Publ. Inst. Mar. Sci.
Univ. Tex. 4(2):328-341 .

Lunz, G. R., Jr. 1943. The yield of cer-
tain oyster lands in South Carolina.
Am. Midi. Nat. 30(3):806-808.

Marshall, N. 1954. Factors controlling
the distribution of oysters in a neu-
tral estuary. Ecology 35(3):322-327.

Mathers, N. F. 1974. Some comparative
aspects of filter-feeding in Ostrea
edul is L. and Crassostrea
(Lam. ) (Mollusca'
Malacol. Soc. Lond. 41:89-97.

augulata

Bivalvia). Proc.

Mayou, T. V., and J. D. Howard. 1975.
Estuaries of the Georgia coast,
U.S.A.: sedimentology and biology.
VI. Animal sediment relationships of
a salt marsh estuary - Doboy Sound.
Senckenb. Marit. 7:205-236.

McFarland, W. N. and T. Prescott. 1959.
Standing crop chlorophyll content and
in situ metabolism of a giant kelp
community in southern California.
Publ. Inst. Mar. Sci. Univ. Tex.
6:109-134.

McKenzie, M. D., and Badger, A. C. 1969.
A systematic survey of intertidal
oysters in the Savannah River basin

area of South Carolina. Contrib.
Bears Bluff Lab., S.C. 50:3-15.

Menzel , R. W. 1955. Some phases of the
biology of Ostrea equestria Say and a
comparison with Crassostrea virqinica

(Gmelin). Publ. Inst.
Tex. 4(1):69-153.

Mar. Sci. Univ.

Menzel, R. W. 1968. Cytotaxonomy of spe-
cies of clams (Mercenaria) and oys-
ters (Cras^ostreaJ! Symp: Mollusca
Mar. Biol. Assoc. India. 1:53-58.

Mills, E. L. 1969. The community concept
in marine zoology, with comments on
continua and instability in some ma-
rine communities: a review. J. Fish.
Res. Board Can. 26(6):1415-1428.

Miner, R. W. 1951. Field book of sea-
shore life. G. P. Putnam's Sons,
New York. 888 pp.

Mishima, J. 1966. The respiration of
intertidal communities. Eleventh
Pacific Congress. Proc. 5-7:47.

Mobius, K. 1883. XXVII. The oyster and
oyster-culture. Translated by H. T.
Rice by permission of the author from
the book published in 1877, Die
Amster und die Amsterewesthschaft.
Verlag von Wiegandt, Hempel und
Parey, Berlin. 126 pp. Pages 683-751
in U.S. Commission of Fish and Fish-
eries, Part 8. Rep. of the Commis-
sioner for 1880, Appendix H.

Moore, D., and L. Trent. 1971. Growth and
mortality of Crassostrea virqinica in
a natural marsh and a marsh altered
by a housing development. Proc. Natl.
Shellfish. Assoc. 61:51-58.

Morton, B. 1973. A new theory of feeding
and digestion in the filter-feeding
lamellibranchias. Malacologia 14:
63-79.

Morton, B. S. 1977. The tidal rhythm of
feeding and digestion in the Pacific
oyster, Crassostrea qiqas (Thunberg).
J. Exp. Mar. Biol. Ecol. 26:135-151.

Nelson, T. C. 1925. Occurrence and feeding
habits of ctenophores in north Jersey
coastal waters. Biol. Bull. 55:69-78.

89

Newell, B. S. 1953. Cellulolytic activity
in lamellibranch crystalline style.
J. Mar. Biol. Assoc. U.K. 32:491-495.

Nicol, J. A. C. 1960. The biology of
marine animals. Wiley Interscience,
New York. 707 pp.

Nixon, S. W., C. A. Oviatt, C. Rogers, and
R. Taylor. 1971, Mass and metabo-
lism of a mussel bed. Oecologia
(Berl.) 8:21-30.

Odum, E. P. 1972. Fundamentals of ecol-
ogy. W. B. Saunders Company, Phil-
adelphia, Pa. 574 pp.

Odum, E. P., and A. A. de la Cruz. 1967.
Particulate organic detritus in a
Georgia salt marsh estuarine ecosys-
tem. Pages 383-388 in G.H. Lauff, ed.
Estuaries.Am. Assoc. Adv. Sci . Publ . 83.

Odum, H. T. 1971. Environment, power,
and society. Wiley Interscience,
New York. 331 p.

Odum, H. T., P. R. Burkholder, and J. A.
Rivero. 1959. Measurement of pro-
ductivity of turtle grass flats,
reefs, and the Bahia Fosforescente of
southern Puerto Rico. Publ. Inst.
Mar. Sci. Univ. Tex. 6:159-170.

Odum, H. T., B. J. Copeland, and E. A.
McMahan, eds. 1974. Coastal ecolo-
gical systems of the United States.
The Conservation Foundation, Wash-
ington, D.C. 4 vol.

Oertel, G. F. 1974. Hydrography and
suspended matter distribution pat-
terns at Doboy Sound estuary, Sapelo
Island, Georgia. Mar. Sci. Cent.
Tech. Rep. Series 74-4. 61 pp.

Oertel, G. F. 1975. Ebb-tidal deltas of
Georgia estuaries. Pages 267-276 vn_
L. E. Cronin, ed. Estuarine research.
Vol. 2. Academic Press, New York.

Oertel, G. F. 1976. Characteristics of
suspended sediments in estuaries and
nearshore waters of Georgia. South-
east. Geol. 18:107-118.

Paine, R. T. 1969. A note on trophic
complexity and community stability.
Am. Nat. 103:91.

Pamatmat, M. M. 1968. Ecology and meta-
bolism of a benthic community on an
intertidal sound flat. Intl. Gesam-
ten. Hydrobiol. 53:211-298.

Peterson, B. J., R. W. Howarth, F. Lips-
chutz, and D. A. Shendorf. 1980. Salt
marsh detritus: an alternative inter-
pretation of stable carbon isotope
ratios and the fate of Spartina
alterniflora. Oikos 34:173-177 .

Peterson, C. H., and N. M. Peterson. 1979.
The ecology of intertidal flats of
North Carolina: a community profile.
U.S. Fish and Wildlife Service, Of-
fice of Biological Services, Washing-
ton, D.C. FWS/OBS-79/39. 73 pp.

Pettijohn, F. J. 1975. Sedimentary rocks.
Harper and Row, New York.

Phillipson, J. 1966. Ecological energet-
ics, studies in biology. No. 1. Edward
Arnold, Ltd., London, England.

Pomeroy, L. R. 1959. Algal productivity
in salt marshes of Georgia. Limnol.
Oceanogr. 4:386-397.

Pomeroy, L. R., and R. G. Wiegert. 1980.
Ecosystems and population ecology of
a salt marsh. (In prep. )

Postma, H. 1967. Sediment transport and
sedimentation in the estuarine envi-
ronment. Pages 158-179 in G. H.
Lauff, ed. Estuaries. Am. Assoc.
Adv. Sci. Publ. 83.

Pritchard, D. W. 1955. Estuarine circu-
lation patterns. Proc. Am. Soc. Civil
Eng. 81(717):1-11.

Pritchard, D. W. 1967. Observations of
circulation in coastal plain estu-
aries. Pages 37-44 in G. H. Lauff,
ed. Estuaries. Am. Assoc. Adv. Sci.
Publ. 83.

Pritchard, D. W. 1971. Estuarine hydrog-
raphy, in J. R. Schubel, ed. The
estuarine environment, estuaries and
estuarine sedimentation. Am. Geol.
Inst, short course lecture notes,
Washington, D. C.

Puffer, E. L., and W. K. Emerson. 1953.
The molluscan community of the oyster

90

reef biotope of the central Texas
coast. J. Paleontol. 27(4):537-544.

Quayle, D. B. 1969. Pacific oyster cul-
ture in British Columbia. Fish. Res.
Board Can. 169:1-192.

Redfield, A. C. 1952. Report to the town
of Brookhaven and Islip, New York on
the hydrography of Great South Bay
and Moriches Bay. Woods Hole Ocean-
ogr. Inst., Ref. 52-26, April 1952.
80 pp.

Relini, G., and E. Giordano. 1969. Dis-
tribuzione verticale ed insediamento
delle quattro specie de Balani pre-
senti nel porto di Genora. Nature-
Soc. It., S. C, Nat., Museo Civ. St.
Nat. e Acquario Civ., Milano 60(4):
251-281.

Rhoads, D. C. 1973. The influence of
deposit-feeding benthos on water tur-
bidity and nutrient recycling. Am.
J. Sci. 273:1-22.

Rhoads, D. C, and D. K. Young. 1970.
The influence of deposit-feeding
organisms on sediment stability and
community trophic structure. J. Mar.
Res. 28:150-178.

Rodhouse, P. G. 1978. Energy transforma-
tions by the oyster Ostrea edulis L.
in a temperate estuary. J. Exp. Mar.
Biol. Ecol. 34(1):1.

Root, R. B. 1967. The niche exploitation
pattern of the blue gray gnatcatcher.
Ecol. Monogr. 37(4):334-349.

Roughley, T. C. 1933. The life history
of the Australian oyster, Ostrea com-
mercial is. Proc. Linn. Soc. N.S.W.
58(314):279-333.

Sanders, H. L. 1958.
Buzzards Bay.
relationships.
3:245-258.

Benthic studies in

I. Animal sediment

Limnol. Oceanogr.

Schelske, C. L., and E. P. Odum. 1962.
Mechanisms maintaining high produc-
tivity in Georgia estuaries. Pages
75-80 in Proc. Gulf Caribb. Fish.
Inst. 14th Annu. Session.

Schubel, J. R. 1968. Turbidity maximum
of the Northern Chesapeake Bay. Sci-
ence 161:1013-1015.

Schubel, J. R. 1971. Sources of sediments
of estuaries. Xn J. R. Schubel, ed.
The estuarine environment, estuaries
and estuarine sedimentation. Am.
Geol. Inst, short course lecture
notes, Washington, D. C.

Settlemyre, J. L., and L. R. Gardner.
1975. Chemical and sediment budgets
for a small tidal creek, Charleston
Harbor, S.C. Water Resources Research
Institue Report 57, Clemson Univer-
sity, Clemson, S.C.

Sikora, J. P., W. B, Sikora, C. W. Erken-
brecher, and B. C. Coull. 1977.
Significance of ATP, carbon, and
caloric content of meiobenthic nema-
todes in partitioning benthic bio-
mass. Mar. Biol. 44:7-14.

Sikora, W. B. 1977. The ecology of
Paleomonetes pugio in a southeastern
salt marsh ecosystem with particular
emphasis on production and trophic
relationships. Ph.D. Dissertation.
University of South Carolina, Colum-
bia. 122 pp.

Simberloff, D. S. 1974. Equilibrium
theory of island biogeography and
ecology. Annu. Rev. Ecol. Syst. 5,
161-182.

Smith, K. L. 1971. Structural and func-
tional aspects of a sublittoral com-
munity. Ph.D. Dissertation. Univer-
sity of Georgia, Athens. 160 p.

Sottile, W. S. 1973. Studies of microbial
production and utilization of dis-
solved organic carbon in a Georgia
salt marsh estuarine ecosystem. Ph.D.
Dissertation. University of Georgia,
Athens.

Stauber, L. A. 1950. The problem of
physiological species with special
reference to oysters and oyster
drills. Ecology 31 (1 ):109-118.

Stenzel, H. B. 1971. Oysters. Pages
N953-N1224 in K. C. Moore, ed.

91

Treatise on invertebrate paleontol-
ogy. Part N, vol. 3 (of 3), Mollusca
6. Geological Society of America
Inc. and the University of Kansas,
Boulder, Colo.

Stephens, D. G., Van Niewenhuise, P. Mul-
lin, C. Lee, and W. H. Kanes. 1975.
Destructive phase of deltaic develop-
ment: North Santee River Delta. J.
Sediment. Petrol. 45(1): 132-144.

Stommel, H. 1951. Recent developments in
the study of tidal estuaries. Woods
Hole Oceanogr. Inst., Ref. 51-33. 15
pp.

Teal, J. M. 1962. Energy flow in the salt
marsh ecosystem of Georgia. Ecology
43(4):614-624.

Teal, J. M., and J. Kanwisher. 1961. Gas
exchange in a Georgia salt marsh.
Limnol. Oceanogr. 6(4):388-399.

Teal , J. M. , and M.
death of the
Brown, and Co.

Teal. 1969. Life and
salt marsh. Little,
Boston, Mass.

Thorson, G. 1964. Light as an ecological
factor in the dispersal and settle-
ment of larvae of marine bottom in-
vertebrates. Ophelia 1:167-208.

Tomkins, J. R. 1947. The oystercatcher
of the Atlantic coast of North Amer-
ica and its relation to oysters.
Wilson Bull. 59(4).

Tripp, M. R. 1974. Effects of organophos-
phate pesticides on adult oysters
(Crassostrea virginica). Pages 225-
236 jm F. J. Vernberg and W. B. Vern-
berg, eds. Pollution and physiology
of marine organisms. University of
South Carolina, Columbia.

Turner, R. E. 1978. Community plankton
respiration in a salt marsh estuary
and the importance of macrophytic
leachates. Limnol. Oceanogr. 23(3):
442-451.

U.S. Geological Survey. National Atlas
of U.S.A. 1970. A.C. Gerlack, ed.
Washington, D.C. 417 pp.

Valiela, I., and J. R. Teal. 1979. The
nitrogen budget of a salt marsh

ecosystem. Nature 280:652-656.

Vallianos, R. J. 1975. A recent history
of Masonboro Inlet, North Carolina.
Pages 151-166 jj^ L. E. Cronin, ed.
Estuarine research. Vol. 2. Academic
Press, New York.

Van Sickle, V., B. B. Barrett, T. B. Ford,
and L. J. Gulick. 1976. Barataria
Basin: salinity changes and oyster
distribution. Louisiana State Univer-
sity, Center for Wetland Resources,
Baton Rouge. Sea Grant Publ. No.
LSU-T-76-002.

Walne, P. R. 1972. The influence of cur-
rent speed, body size, and tempera-
ture on the filtration rate of five
species of bivalves. J. Mar. Biol.
Assoc. U. K. 52:345:374.

Watling, H. 1978. Effect of cadmium on
larvae and spat of the oyster Cras-
sostrea qigas (Thunberg). Trans. R.
Soc. of South Africa 43(2): 125 -
134.

Wells, H. W. 1961. The fauna of oyster
beds, with special reference to the
salinity factor. Ecol. Monogr. 31:
239-266.

Wiedemann, H. V. 1971. Shell deposits
and shell preservation in quaternary
and tertiary estuarine sediments of
Georgia, U.S.A. Sediment. Geol.
7(2):103-125.

Wiegert, R. G. 1968. Thermodynamic con-
siderations in animal nutrition. Am.
Zool. 8(1):71-81.

Wildish, D. J., and D. D. Kristmanson.
1979. Tidal energy and sublittoral
macrobenthic animals in estuaries.
J. Fish. Res. Board Can. 36:1197-
1206.

Yonge, C. M. 1960. Oysters. killmer
Brothers and Haram, Ltd., Birtenhead,
London, England. 209 pp.

Zingmark, R. G., ed. 1978. An annotated
checklist of the biota of the coestal
zone of South Carolina. University
of South Carolina Press, Columbia.
364 pp.

92

APPENDIX: OYSTER BIOENERGETICS

Oysters, like all heterotrophic orga-
nisms, use energy in proportion to their
growth rate, their reproductive invest-
ment, and their efforts to obtain food,
remove waste, defend themselves against
parasites and predators, and maintain a
favorable osmotic balance. This section
discusses the rates and partitioning of
energy expenditures for individual inter-
tidal oysters and the oyster population as
a whole. The energy requirements of the
entire reef, a prerequisite for under-
standing the dynamics of the oyster reef
community, are estimated in Chapter 3.

Ecologists and environmental managers
are beginning to realize the value of
information regarding the rates and path-
ways of energy flow in communities of
organisms and entire ecosystems. Energy
units are interconvertible, and, there-
fore, the energy "cost" of totally dif-
ferent processes is the common denominator
by which these processes can be compared
objectively and ranked in terms of their
ecological importance. The first ecologist
formally to apply this principle to the
study of ecosystems was Raymond Lindemann,
who in 1942 published a landmark treatise
on the partitioning of energy flow through
an ecosystem (Lindeman 1942). Since then,
it has become common practice to include
energetics in ecological research. Good
review sources on bioenergetics include
Phillipson (1966) and Wiegert (1968).

The extant oyster literature includes
several compilations of energy budgets for
various species of oysters in different
areas. Extrapolations from some of these
studies are necessary to fill in energy
budget data gaps for intertidal oysters in
the study area.

The calculation of an energy budget
for a population of organisms involves the
use of one or another equation of the
general form:

P(net) = I-E-R-W

(1)

''(net) ~ "^^ secondary production
rate, or growth of the pop-
ulation in a given time
(including somatic growth,
gamete production, and mor-
tality losses)
I = ingestion rate
E = egestion and excretion rates
R = respiration or metabolic rate
W = the rate at which external work
is performed by the organisms

The term W is usually ignored (Wie-
gert 1968), but for some animals (such as
mound-building termites and reef oysters),
work may be substantial because these or-
ganisms build vertical structures against
gravity.

In mature populations, the production
equation may attain a steady state, in
which no net growth can be measured and
annual energy inputs equal losses. Oyster
reefs appear to attain this steady-state
maturity when they achieve a critical ver-
tical elevation relative to tidal stage or
when oyster growth is equal to maintenance
costs.

Before a rough energy budget for in-
tertidal oysters is presented, the prob-
lems involved in compiling such a budget
must be discussed. The terms in the
energy budget Equation (1) are measured
for an oyster population in the following
ways. Net production P(net) ""s sometimes
calculated by measuring the increase in
size of experimental animals over a unit
of time. This technique requires measur-
ing the individual oysters. Another tech-
nique calculates time elapsed between age
classes in the size-frequency distribution
of a natural population. The latter tech-
nique is tedious since age classes quickly
become indistinct because of continuous
waves of spawning over the warm season.

Total production P(nross) includes
gamete production (and release) as well as
mortality and predation (and harvesting)
between sampling periods. The growth rate

93

ts

of an oyster slows as its gamete produc
tion gradually begins to dominate its
energy budget and as its respiratory rate
"catches up" to its ingestion rate (Rod-
house 1978), as illustrated in Figure A-1.

Ingestion by oysters (I) is usually
estimated by measuring the rate of clear-
ance of particles in a suspension to which
test animals are exposed for a unit of
time. Walne's (1972) experiments using
Crassostrea qigas and Ostrea edulis are
exemplary in that realistic food concen-
trations and a wide range of sizes of oys-
ters were used. In addition, Walne used
flowing water conditions rather than the
usual standing water experiments. Haven
and Morales-Alamo (1970) also measured
oyster ingestion in a flowing water system
but did not use a wide size range of oys-
ters.

Egestion (E) is measured by holding
test oysters in trays in which feces and
pseudofeces are collected and measured
during a known time interval (Haven and
Morales-Alamo 1967; Bernard 1974).

The respiration rate of oysters (R)
is usually measured by documenting the
rate of decline in dissolved oxygen in
water in which oysters are immersed or by
measuring the change of dissolved oxygen
in water as it flows over a population of
oysters. The rate of change of CO2 is not
as convenient to measure with oysters,
partly because an infrared CO2 analyzer is
required, partly because oysters can fix
CO2 (Hammen 1969), and partly because they
can respire anaerobically and release COj
from the dissolution of shell carbonate
(Hochachka and Mustafa 1972).

One major problem in quantifying in-
dividual terms in the oyster energy budget
equation is that most terms change in a
nonlinear fashion as an oyster (or size
class) grows. Small animals operate at
higher metabolic rates than large animals.
Another problem is that at least five en-
vironmental variables affect each term:
(1) intertidal elevation, (2) water tem-
perature, (3) levels of food and other
suspended matter in the water column, (4)
dissolved oxygen levels, and (5) current
velocity. To further complicate the pic-
ture, the size of the animals and these
other variables are interrelated in com-
plex (nonlinear) ways.

Energy budgets are invariably simpli-
fied models because of these problems, and
the present budget is no exception. Some
comments about the variables used and
assumptions made follow.

VARIABLES

Tide Stage

Oysters obviously cannot pump water
to respire and feed unless they are im-
mersed. Intertidal reef oysters are
assumed to be inundated on the average of
only 50X of any 24-hr day. Other workers
have made similar assumptions on feeding
duration, even for subtidal oyster popula-
tions. Bernard (1974) assumed 50%; Rod-
house (1978) assumed 70% feeding time.

Water Temperature

Temperature affects all biochemical
reactions, including oyster energy con-
sumption. Intertidal oysters are exposed
to water temperatures that vary by a
factor of about three, from 9° to 31°C
(Dame 1970; Bahr 1974). The annual pat-
tern of water temperature variation in
coastal South Carolina is illustrated in
Figure A-2 (Dame 1970). Over this temper-
ature range oyster metabolism is estimated
to vary by a factor of about eight (Bahr
1976).

Food and Other Suspended Matter

Loosanoff (1962) showed that food and
other suspended matter significantly
altered oyster ingestion rate. Excess
turbidity, caused either by suspended
organic or inorganic matter, reduces "oys-
ter pumping." It can be assumed that sus-
pended matter in the study area is close
to optimum for intertidal oysters and that
they are exposed to about 0.01 gC/liter or
0.04 kcal/ liter when inundated (Odum and
de la Cruz 1967).

Dissolved 0-,

Oyster respiration rates are unaf-
fected by dissolved oxygen concentrations
unless the concentration decreases below
one-half saturation level (Ghiretti 1966).
In other words, dissolved oxygen in estu-
aries in the study area should normally
not affect respiration or feeding rates

94

20-

C/3
<

Figure A-1. Age-dependent annual production of soft tissue, shell organics,
gonad output, and respiration in an oyster (adapted from Rodhouse 1978).

95

AMJJ ASON

D (TIME IN ANGULAR DEGREES)

Figure A-2. Seasonal variation in water temperature affecting oyster reefs in
South Carolina (adapted from Dame 1970).

96

but it could become a factor in dredged
areas (Frankenberg and Westerfield 1968).

Current Velocity

A positive effect of current velocity
on oyster feeding could be surmised from
the fact that oyster reefs tend to grow
outward toward the middle and more rapidly
flowing portion of a tidal stream. En-
hancement of oyster feeding as a function
of increase in current velocity was demon-
strated by Walne (1972).

Given the above assumptions, the addi-
tional information most important for the
calculation of an energy budget for inter-
tidal oysters is the size-frequency (or
weight-frequency) distribution of reef
populations and the effect of weight on
the energy budget terms.

All of the terms in the energy budget
equation for oysters are presumably af-
fected by the size (or weight) of individ-
uals by the following general equation:

F = a W

(2)

where F =

W =

a and b =

in energy

the process rate

or matter units

the biomass of the oyster

(g or kcal )

constants (represent the

effects of temperature and

the surface area-to-volume

ratio, respectively)

It is generally known that small oys-
ters ingest, egest, respire, grow (and
die) at higher rates than do large oys-
ters, and that these rates increase in all
oysters with increased temperature. Un-
fortunately, no general agreement exists
in the bioenergetics literature concerning
units of biomass. Table A-1 lists some
conversion factors for oyster biomass that
were compiled from various sources. The
numbers are only approximate because the
allometric relationships can change with
gonadal state or with tidal elevation of
the population. Dame (1972a) found that
intertidal oysters in North Inlet, South
Carolina, had a significantly higher ratio
of shell weight to dry meat weight than
subtidal oysters had.

Because small oysters process energy
at relatively higher rates than large

ones, it is important to document the size
(biomass) frequency of intertidal oysters
in the study area. Bahr (1974) separated
reef oysters at Doboy Sound, Georgia, into
32 size classes at 5-mm intervals (2 to
157 mm). He found that the oyster popula-
tion in the central (higher) portion of
several old reefs typically showed a log
normal distribution, especially during the
late fall. Oysters in the smallest five
size classes (up to 19 mm) dominated the
population, and oysters above 100 mm were
rare. Dame (1976) reported a similar size-
frequency distribution of reef oysters in
South Carolina, but with generally lower
overall populations and reduced dominance
of small size classes. Figures A-3 and
A-4 illustrate the temporal changes in
size-frequency distributions of reef oys-
ters in these two respective studies.

The equation that describes the size-
frequency distribution of reef oysters in
Doboy Sound, Georgia (Bahr 1974) is as
follows:

log^Q Y = -0.02 X^. + 2.32

(3)

where Y = the number of oysters per

0.1

1^ in size class X,-

X. (i = 2, 7, 12. ..157) = 5-mm
^ size class

The relation between individual oys-
ter size and biomass from Bahr (unpub-
lished data) is described by another
regression equation as follows:

0.02 X -1.8

(4)

where Y = logjg afdw (g) of total

oysters including shell,

X = height of each oyster in mm

The r of this relationship is 0.84
with 78 degrees of freedom. The experi-
mental animals were collected at eight
different times, including all seasons.

To simplify the computation of the
energy budget of the reef oyster popula-
tion. Equations 3 and 4 were used to
describe a typical reef oyster population,
intermediate in both numbers and biomass.
Thus, the numerical dominance of small
oysters is offset by the higher biomass of
(rare) large oysters, and oysters from 40
to 80 mm in height (mean 60 mm, or 0.25 g
afdw) are functionally typical (See Figure

97

Table A-1. Conversion factors for oyster
biomass units (intertidal oysters).

Whole oyster

Total wet wt

100%

Total

dry wt

100%

Total

afdw^

Wet

shell wt

72%

Dry

shell wt

97.1%

Shell afdw*^

42%

Meal

: only

Dry

wt

Wet

meat wt

28%

Dry

meat wt

2.8%

Meal

; afdw*^

100% 42% 58%

Wet wt Dry wt afdw

100% 14.9%^ 12.0^

^Gametes may comprise up to 50% of this proportion,
afdw = ash-free dry weight.

98

HEIGHT IN MM

Figure A-3. Seasonal changes in size-frequency distribution of reef oysters in
Georgia (Bahr 1976) .

99

-I 2

Figure A-4. Seasonal changes in intertidal oyster size-frequency distribution
in South Carolina (adapted from Dame 1976).

100

A-5). The entire oyster biomass of the
reef population is therefore considered
here as divided among 0.25-g oysters.
Bahr (1974) reported that the average bio-
mass of the reef oyster population was 970
g/m2 afdw (total wt); thus one can postu-
late a hypothetical reef populated by
60-rnni oysters at a density of about 4,000
oysters/m^. The dry meat weight of an
oyster of 0.25 g total afdw would equal
approximately 0.18 g (from Table A-1).

Before one estimates the value of the
terms of Equation 1 for the "average" reef
oyster population, it is appropriate to
consider two independent studies that were
conducted at approximately the same time
and that attempted to measure certain
aspects of the energy budget of oyster
reefs. Bahr (1974, 1976) and Dame (1970,
1972a-, 1972b, 1976, 1979) studied oyster
reefs in Georgia and South Carolina,
respectively. Significant differences
between the studies are compared in Table
A-2.

Some differences between the two sets
of conclusions are explainable on the
basis that test reefs in Dame's studies
were significantly lower in the intertidal
zone than were the reefs in Bahr's work,
although the absolute elevation of Dame's
reefs with respect to mean low water (MLW)
was not reported. This elevation dif-
ference perhaps indicates a significant
difference in inundation time, which could
explain the higher production reported by
Dame. In Dame's studies, oyster produc-
tion estimates for large oysters were
based on holding oysters in trays beneath
a pier (presumably shaded) and therefore
not in as stressful a setting as on a
natural reef. A real difference probably
existed in intertidal oyster reef produc-
tion (higher in South Carolina). The ac-
tive commercial harvest of South Carolina
reef oysters is proof that net production
of large oysters occurs there. Lunz (1943)
reported that oysters can grow to 3 inches
in 2 years in South Carolina reefs. Using
a calorific coefficient of 3.3 kcal/g Oj,
one can estimate that reef oysters respire
the equivalent of 13,000 kcal/m^/yr. The
implication of this high metabolic rate is
that the total biomass turns over on the
average about once every 0.38 yr, or 2.6
times per year (13,000 kcal/m2 /yr t 5,000
kcal/m2).

Energy expended for gamete production
increases with the age of a particular
oyster but remains about half the respira-
tion rate (Figure A-1). Bernard (1974)
estimated that a subtidal population of C^.
gigas expended as much energy on gamete
production as on respiration (Figure A-6).
Thus, between 7,500 and 13,000 kcal/m^/yr
of the energy assimilated by reef oysters
would be converted to gametes and released
into the water column. At least 99% of
this energy "investment" would never reach
"maturity" but would be consumed by other
members of the salt marsh ecosystem.

The rate of external work (W) per-
formed by oysters is the rate at which a
unit weight of shell material is elevated
above the mud surface, multiplied by its
elevated distance. In energy terms this
translates into the cost to oysters of
producing the shell protein that comprises
1.3% of the total shell dry weight or
about 400 g protein/m^ (2,000 kcal/m^).
The maximum elevated distance is 1.5 m
(see Section 3.1), but unfortunately we
have no reliable estimate of reef growth
rates. Bernard (1974) estimated that sub-
tidal oysters (C^. gigas) in British Colum-
bia only expend about 10 kcal /m^/yr on
shell production. This is equivalent to
(30 kcal/m2/yr) for oysters in the study
area, calculated by using Bernard's data
but correcting for biomass differences
between the two different populations.
We suspect that this estimate is much too
low. The rate of predation on oyster
reefs is discussed in Section 3.4.

Energy Budget Summary

An energy budget for reef oysters is
presented in the following paragraphs, and
the rationale and values for the terms of
the equations are discussed. Because of
the method used in estimating net produc-
tion [P (net)^ '■'^ ^^^ studies discussed
above, we are inclined to agree with the
conclusions of the Georgia study. Charac-
teristically, net secondary production of
reef oysters is low in the upper portion
of high reefs and large oysters are quite
old, perhaps even 5 to 10 years or more.
In these reefs, somatic growth is balanced
by mortality. In lower "immature" reefs,
f'(netj ''^ undoubtedly significant. Because
the South Atlantic Bight includes large
areas of low "immature" reefs, especially

101

CO

(A

>-

o

o

450

400-

350-

300

■MEASURED OYSTER FREQUENCY (tt/O.lm^)

APPROXIMATE FREQUENCY (ft/O.lm^)

OYSTER BIOMASS CALCULATED

FROM SIZE CLASSES

(gafdw/O.lm^i

APPROXIMATE

BIOMASS

(gafdw/O.lm^)

u. 250-

200-

150

100-

50-

-11.0

10.0

-8.0

I I I I I ^ I I I I I I r

0 10 20 30 40 50

-6.0 2

m
O)

-4.0

75 100

SIZE (mm)

125

150

Figure A-5. Reef oyster height-frequency relationship and cumulative biomass
curves.

102

Table A-2. Comparison of two sets of oyster reef
energy parameters collected within the study area.

Sources

Bahr (1974, 1976) Dame (1976)

Parameter Georgia South Carolina

P/n..ce^^ — 4,500/yr

(gross)
'(net)

P,_.^ 0-1,000/yr '^ 3,460/yr

R 13,000/yr 6,000/yr

b'* 5,000 (total oysters) 2,050 (meat)

10,000-20,000 1,000-4,400

-6

^All figures unless otherwise noted represent kcal/m (rounded).

Includes growth, mortality, and gonadal products.
''Minimum P from "old" high reef, maximum P from "young" low reef.

B = biomass.

^F = oyster frequency (# /m ).

103

POTENTIAL
22052 Kcal

GAMETES

2%
502 Kcal

NOT RETAINED
89%

1545 Kcal

7%

DEPOSITED

Figure A-6. Schematic representation of percentage distribution of potential
food expressed in kilocalories for 1-year period in 1 m^ of subtidal
Crassostrea gigas population (adapted from Bernard 1974).

i04

in South Carolina, we will assume the
''(net) °^ 1,000 kcal/m^/yr is a conserva-
tive estimate.

The ingestion rate (I) of a reef pop-
ulation, as expressed by the "functionally
average" 60-mm oyster, approximates the
ability of oysters in the population to
filter about 100 ml of water per minute
(extrapolated from values reported by
Walne [1972] for C^. qiqas of the same
height). The feeding experiments by Walne
were carried out at temperatures approxi-
mating the median level for our study area
(19° C). During one day (12 hours of pump-
ing time), the oysters occupying a typical
square meter of reef could filter 288,000
liters of water (4,000 oysters x 0.1 li-
ter/mi n X 12 hr x 60 min). With an aver-
age POC load of 0.01 g/liter assumed (Odum
and de la Cruz 1967), this would equal a
potential maximum ingestion rate of 300
gC/m2/day, or 1 x 106gC/m2/yr (5 x 105
kcal/m^/yr) if the oysters filtered at
100% efficiency. If filtration is 40%
efficient (Haven and Morales-Alamo 1970),
ingestion of organic carbon would occur at
the rate of about 2 x 10^ kcal/m2/yr. Only
a small fraction of this cartjon would be
assimilable, however. The remainder would
be egested and biodeposited as feces or
pseudofeces, or excreted as organic nitro-
gen. Mathers (1974) reported that large
oysters of the species £. anqulata could
completely filter water at the- rate of
54 ml/g (wet wt)/hr or about 0.45 liter/g
(afdw)/hr. This translates to about
2 X lO^'gC/m^/yr or 1.0 x 10^ kcal/m Vyr
for reef oysters, twice the estimate of
Walne (1972). These two estimates illus-
trate the approximate nature of this meas-
urement.

Egestion, excretion, and pseudofecal
production (E) by reef oysters can be
expressed in terms of a reef population of
60-mm oysters. Bernard (1974) reported
that large specimens of C^. gigas ( '^10 g
dry wt of meat) produced about 5.9 x IC*
kcal per oyster per year as biodeposits.
If an extrapolation were made to the 60-mm
reef oyster (dry meat weight = 0.18 g), we
could conservatively predict that it would

biodeposit the equivalent of 1,000 kcal/
yr, or 4 x 10^ kcal/m^/yr for the entire
oyster population. If one judges by the
estimated maximum ingestion rate, however,
(see above) this estimate is equal to 80%
of ingestion, implying a 20% assimilation
rate (A = I-E). This estimate may be high
because only a small portion of the total
of all ingested carbon can be assimilated
by oysters.

Of the terms in Equation (1), respi-
ration rates (R) are best known for reef
oysters. Bahr (1974, 1976) calculated that
the reef oyster population accounted for
approximately 48% of the mean oxygen up-
take of the total reef community, or about
3,900 g02/m2/yr. This estimate was derived
by combining individual oyster respirome-
try experiments (carried out seasonally at
ambient temperatures and on different
sized animals) with the relative propor-
tion of the reef oyster biomass repre-
sented by each size class.

From data reported by Dame (1970) and
Bahr (1974), the following equation de-
scribes the relationship between oyster
oxygen uptake and biomass at the approxi-
mate median water temperature in the study
area (20° C).

0.53X

0.71

(5]

where Y = mg O2 used per hour and
X = total afdw

Solving this equation for a function-
ally typical oyster of 0.25 g afdw, one
would predict that a single oyster would
consume 0.20 mg 02/hr. When this figure is
multiplied by 12 hours of inundation time/
day, 365 days/yr, and 4,000 oysters/m^,
the resulting estimate of oxygen require-
ments is 3,500 g Oa/m^/yr, very close to
the above estimate of 3,900 g Oa/m Vyr
(Bahr 1974).

The final estimates of the parameters
in the energy budget Equation (1) are pre-
sented in Section 2.5 and illustrated in
Figure 12.

105

5027J -101

REPORT DOCUMENTATION
PAGE

1,_ REPORT NO.

FWS/OBS-81/15

3. Recipient's Accession No

4. Title and Subtitle

THE ECOLOGY OF INTERTIDAL OYSTER REEFS OF THE SOUTH ATLANTIC
COAST: A COMMUNITY PROFILE

5. Report Date

May 1981

7. Author(s)

8. Performing Organization Rept. No.

Leonard M. Bahr and William P. Lanier,

9. Performing Organization Name and Address

Louisiana State University
Baton Rouge, Louisiana 70803

10. Project/Task/Work Unit No.

11. Contract(C) or Grant(G) No.
(C)

(G)

12. Sponsoring Organization Name and Address

U.S. Fish and Wildlife Service
Office of Biological Services
Department of the Interior
W3':;hingtnn, D.C. 20240

15. Supplementary Notes

13. Type of Report & Period Covered

16. Abstract (Limit: 200 words)

The functional role of the intertidal oyster reef community in the southeastern Atlantic
coastal zone is described. This description is based on a compilation of published data,
as well as some unpublished information presented as hypotheses.

The profile is organized in a hierarchical manner, such that relevant details of reef
oyster biology (autecology) are presented, followed by a description of the reef
community level of organization. Then the reef community is described as a subsystem
of the coastal marsh-ecosystem (synecology) . This information is also synthesized in a
series of nested conceptual models of oyster reefs at the regional level, the drainage
basin level, and the individual reef level. The final chapter includes a summary
overview and a section on management implications and guidelines.

Intertidal oyster reefs are relatively persistent features of the salt marsh estuarine
ecosystem in the southeastern Atlantic coastal zone. The average areal extent of the
oyster reef subsystem in this larger ecosystem is relatively small (about 0.05%). This
proportion does not reflect, however, the functional importance of the reef subsystem
in stablizing the marsh, providing food for estuarine consumers, mineralizing organic
matter, and providing firm substrates in this otherwise soft environment.

17. Document Analysis a. Descriptors

Oysters, Reefs, Ecology, Intertidal zone, Food chain, Estuaries

b. Identifiers/Open-Ended Terms

Salt marsh, conceptual models

c. COSATI Field/Group

18. Availability Statement

Unlimited

19. Security Class (This Report)

Unclassified

20. Security Class ahis Page)

21. No. of Pages

105

(See ANSI-Z39.18)

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and providing for the enjoyment of life through outdoor recreation. The Department as-
sesses our energy and mineral resources and works to assure that their development is in
the best interests of all our people. The Department also has a major responsibility for
American Indian reservation communities and for people who live in Island territories under
U.S. administration.