PB83-189365
Submerged Aquatic Vegetation
Distribution and Abundance in the
Lower Chesapeake Bay and the Interactive
Effects of Light, Epiphytes and Grazers
Virginia Inst. of Marine Science
Gloucester Point
.-.M protect^ t-&-'i
Prepared for
Environmental Protection Agency
Annapolis, MD
Apr 83
J
Natioral Teclmc»l InformatiOA Servtce
EPA Report Collection
Information Resource Center
US EPA Region 3
Philadelphia, PA 19107
-------
EPA-600/3-83-019
April 1983
Regional Onte, lor Environmental Inlormat.on
US EPA Region 111
1650 Arch St
Philadelphia, PA 19103
SUBMERGED AQUATIC VEGETATION: DISTRIBUTION AND ABUNDANCE
IN THE LOWER CHESAPEAKE BAY AND THE INTERACTIVE
EFFECTS OF LIGHT, EPIPHYTES AND GRAZERS
Robert J. Orth
Kenneth A. Moore
Jacques van Montfrans
Virginia Institute of Marine Science
College of William and Mary
Gloucester Point, VA. 23062
Contract No. X003246
Project Officer
Dr. David Flemer
Chesapeake Bay Program
U.S. Environmental Protection Agency
2083 West Street
Annapolis, MD 21401
CHESAPEAKE BAY PROGRAM
OFFICE OF RESEARCH AND DEVELOPMENT
U.£. ENVIRONMENTAL PROTECTION AGENCY
ANNAPOLIS, MD 21401
•fraoucct ti
NATIONAL TECHNICAL
INFORMATION SERVICE
OS DCMDIMEim Of COMMERCE
SMMGflUO. V* 221(1
-------
TECHNICAL REPORT DATA
fPlcate read liumcituiu un ilic reverse bi-jorc complain*)
\. REPORT NO. |2. ——
bPA-60Q/3-b3-OI9
I! TITLE AND SUBTITLE
Submerged Aquatic Vegetation: Disfiibution ;nid Abundant:
in the Lower Chesapeake B.iv ami tlie Interactive Fffects
of Light, Epiphytes, and Grazers __
7. AUTMOHtS)
Orth, Moore, ami Mont trans
3. RECIPIENT'S ACCESSIOWNO.
1 39365
5. REPORT DATE
Apr i I
Apr!9
6. PERFORMIN
NG ORGANIZATION CODE
V I NK-
8. PERFORMING ORGANIZATION REPORT NO,
9. PERFORMING ORGANIZATION NAME AND ADDRESS
Virginia Institute of Marine Science
Gloucester Point, Virginia 2 U)b2
10. PROGRAM ELEMENT NO.
B44B2A
11. CONTRACT/GRANT NO.
X - 003246
12. SPONSORING AGENCY NAME AND ADDRESS
U.S. EPA - Clu-sapenke Hay Program
208J West Street, Suite 5G
Annapolis, M.irvKmd 21401
13. TYPE OF REPORT AND PERIOD COVERED
14. SPONSORING AGENCY CODE
EPA/600/05
IS. SUPPLEMENTARY NOTES
16. ABSTRACT
This final grant report is subdivided into two major sections.
the first section describes the distribution and abundance of
submerged aquatic vegetation (SAV) in the lower Bay. Baseline
information for SAV was collected in 1978 and supplemented with
additional information from 1979. Subsequently, in 1980 and 1981,
overflights were conducted of all polyhaline and mesohaline areas
mapped for SAV in 1978 and photographs were taken from which aerial
coverage of the vegetation was measured. The data from 1978 through
1981 were analyzed for short term changes in SAV distribution and
abundance. This information was combined with historical data from
six intensive study sites to provide a detailed description of changes
in distribution and abundance of SAV over Che last 50 years.
7.
KEY WORDS AND DOCUMENT ANALYSIS
DESCRIPTORS
b.IDENTIFIERS/OPEN ENDED TERMS C. COSATI Kicld/Gcoup
U.S. Environmental Protection Agency
Region III information Resoujcs
Center ('JFM5Z)
£41 ClisstnutStiset
rhiiadeipiiia, PA 19107
3. DISTRIBUTION STATEMENT
Unrestricted distribution
19. SECURITY CLASS (Thil Keport,
nnc lass if iecl
21. NO. OF PAGES
30. SECURITY CLASS (Thupagel
unc lassi f iei!
22. PRICE
• PA Form 2220-1 (»•»!)
-------
NOTICE
This document has been reviewed in accordance with
U.S. Environmental Protection Agency policy and
approved for publication. Mention of trade names
or commercial products does not constitute endorse-
ment or recommer.dation for use.
11
-------
CONTENTS
Page
ACKNOWLEDGEMENTS iii
PREFACE iv
SECTION I. Distribution and Abundance of Submerged Aquatic
Vegetation in the Lower Chesapeake Bay, 1978-1981
by R. J. Orth and K. A. Moore 1
Introduction 2
Materials and Methods 2
Results 9
Summary 20
Literature Cited 22
Appendix A 23
SECTION II. Interactive Effects of Light, Epiphytes and
Grazers 46
CHAPTER 1. Epiphyte-Seagrass Relationships With an
Emphasis on the Role of Micrograzing: A
Review by R. J. Orth and J. van Montfrans .... 47
Abstract 48
Introduction 49
I. Epiphyte-Se?grass Relationships 49
II. The Trophic lole of Periphyton in Seagrass
Beds 58
III. Periphyton Grazing: Consequences for the
Macrophyte Host 66
IV. Effects of Nutrient Enrichment on Macvophytes . 69
V. Management Implications 72
Literature Cited 74
CHAPTER 2. The Effects of Salinity Stress on the Activity
and Survival of Bittium varium Adults and
Larvae by R. J. Orth, J. Capelli and
J. van Montfrans 86
Abstract 87
Introduction 88
Materials and Methods 89
Results 93
Discussion 102
Literature Cited 105
CHAPTER 3. The Role of Grazing on Eelgrass Periphyton:
Implications for Plant Vigor by J. van Montfrans,
R. J. Orth and C. Ryer 108
Abstract 109
Introduction 110
Materials and Methods 112
Results 117
Discussion 131
Literature Cited 133
-------
ACKNOWLEDGMENTS
We would like to thank the following people for their
indispensable help in the completion of this project: Charlie Alston
who aided in the flight organization and aerial photography; Sam White
who piloted the VIMS aircraft; Anna Vascott, Linda Lee, Jamie Topping
and Glenn Markwith for their valuable assistance in the tedious work
made necessary in the grazing experiments; Cliff Ryer, who in addition
to aiding in laboratory experiments, provided expert assistance in the
data analysis; Judy Capelli, who was indispensible in all aspects and
provided more than just technical assistance; Shirley Sterling, Carole
Knox. N^nry White and the VIMS art, photographic and report center for
the ^reparation of this report. Finally, to all those individuals who
have played a role in the Chesapeake Bay Program and making it
possible for all the exciting research on submerged aquatic vegetation
to continue, we are forever indebted.
-------
PREFACE
This final grant report is subdivided into two major sections.
the first section describes the distribution and abundance of
submerged aquatic vegetation (SAV) in the lower Bay. Baseline
information for SAV was collected in 1978 and supplemented with
additional information from 1979. Subsequently, in 1980 and 1981,
overflights were conducted of all polyhaline and mesohaline areas
mapped for SAV in 1978 and photographs were taken from which aerial
coverage of the vegetation was measured. The data from 1978 through
1981 were analyzed for short term changes in SAV distribution and
abundance . This information was combined with Historical data from
six intensive study sites to provide a detailed description of changes
in distribution and abundance of SAV over the last 50 years.
Included in this section of the report are: Da comparison cf
SAV distribution and abundance for all topographic quadrangles
containing SAV in 1978, 1980 and 1981; 2) a complete analysis of
information from six historical sites including the most recent *980
and 1981 data; and 3) an append! which includes the topographic maps
with SAV bed outlines for the IS) inventory. These are directly
comparable; to maps produced from photography taken in 1978.
A separate report entitled "Distribution and Abundance of SAV in
the Chesapeake Bay: A Scientific Summary" was submitted to the
Chesapeake Bay Program previously. This report summarizes results
from research conducted over the last four years by the Johns Hopkins
University, The American University, Earth Satellite Corporation and
the Virginia Institute of Marine Science and strives to answer key Bay
management questions related to SAV.
Section two deals with the interactive effects of light,
epiphytes and grazers on SAV and has been written in three chapters.
The first chapter reviews the literature on epiphyte-seagrass
relationship with an emphasis on the role of micrograzing. The second
chapter examines the salinity tolerances of Bittium varium adults and
larvae and attempts to relate population changes of this important
epifaur.al grazer to salinity perturbations caused by Tropical Storm
Agnes. The third chapter of this section further studies the role of
the gastropod, Bittium varium, in an eelgrass community. The results
of preliminary laboratory experiments in a previously sponsored EPA
Chesapeake Bay Program study, "The Functional Ecology of Eelgrass''
(Orth and van Montfrans, 1982) revealed that B. variura substantially
reduced periphyton on eelgrass blades. The decline of eelgrass along
-------
the western shore of the Bay one year following the drastic decline of
JJ. varium in the same region during 1972 (Orth, 1977), suggested a
causal relationship between the removal of periphyton by this grazing
snail and the vigor of eelgrass (Zostera marina). We therefore
formulated and tested the hypothesis that the presence of Bittium
varium enhances the growth and vigor of eelgrass by removing
epiphytes, which are known to reduce photosynthesis through
restricting light and bicarbonate ion uptake (Sand-Jensen, 1977). If
the hypothesis is true, the presence of B. varium and other grazers
could be important for eelgrass distribution, particularly in areas
where light reaching the plant surface may be only marginally adequate
for phor.osynthetic maintenance. The results of oar experiments are
discussed in regard to this concept.
-------
'-- t
SECTION I
DISTRIBUTION AND ABUNDANCE OF SUBMERGED AQUATIC VEGETATION IN THE
LOWER CHESAPEAKE BAY 1978-1981
by
Robert J. Ofh
and
Kenneth J. Moore
-------
INTRODUCTION
Submerged aquatic vegetation (SAV) has been the subject of an
intensive research program funded by the U.S. Environmental Protection
Agency's Chesapeake Bay Program since 1978. One of the main elements
of the SAV research was an analysis of the distribution and abundance
of SAV. In 1978, a baywide survey of SAV using aerial photography was
conducted. The results provided scientists and resource managers the
first comprehensive look at the current distribution and abundance of
SAV in the Chesapeake Bay (Anderson and Macomber, 1980; Orth et al.,
1979). In addition, an historical analysis was made of several key
sites in the Bay by archival aerial photography dating to 1937.
Because of interest in the rapid changes that have occurred with
SAV in the last 15 years (Orth and Moore, 1981a,b), and the
relationship that this Chesapeake Bay Program project had with the
other projects funded by EPA for the study of Bay grasses, continued
observation was made of most areas with significant abundances of SAV
in the lower Bay in 1979. This effort was extended in 1980 and 1981
to include aerial photography of all areas mapped for SAV in 1978.
This provided complete coverage of SAV over a four year period for the
lower Bay. It also allowed for an intensive examination of changes in
the distribution and abundance on a short term basis.
MATERIALS AND METHODS
Mapping of Submerged Aquatic Vegetation
The mapping submerged aquatic vegetation is graphically depicted
in Figure 1. The method consists of acquiring photography,
transferring the SAV bed outlines to base maps and determining the
areas of the SAV beds. Each component of the procedure is more fully
described below. These procedures are similar to those used in the
distribution and abundance work conducted in 1978 (Orth, Moore and
Gordon, 1979).
Aerial photography
The first phase of the aerial photography effort was the planning
of flight lines for complete areal coverage- of all areas of SAV
contained within the designated quadrangles. All 27 quadrangles
(1:24,000 scale) mapped in 1978 from the polyhaline and mesohaline
areas of the lower Bay were examined in 1980 and 1981. Flight lines
were drawn on 1:250,000 scale USUS topographic sheets, 2* by 1*
series, using a cransparent framesize overlay for coverage at an
-------
CO
(4
00
o
o.
o
c.
oc
o
u
o
o.
E
O
Vi
o
o
u-i
C
c
o
la
4J
M
1-1
•a
v>
M-l
O
la
«
Ua
n
(0
hi
I-
QC
-------
altitude of 3660 m (12,000 feet). Flight lines were situated to
ensure both complete bed coverage and inclusion of land features as
control points for mapping accuracy. Lines were also oriented to
facilitate ease of flying where possible. Flight direction was
oriented such that the overall mission would progress in the same
direction as the tide propagation to ensure photography at the lowest
possible tidal stage.
The general guidelines used for mission planning and execution
were developed in discussions with EPA (Table 1). These quality
assurance guidelines address tidal stagt, plant growth, sun elevation,
water transparency and atmospheric transparency, turbidity, wind,
sensor operation, and plotting. Although it was the overall intent to
plan for optimum conditions in all items, some constraints are
necessarily more important than others and an order of priorities was
established to guide Mission planning.
The most critical of those items listed is plant growth stage.
At the wrong time of year, it would be possible to ily an otherwise
ideal mission and record little or no SAV. For the predominant
species of grass in the southern Chesapeake Bay, eelgrass, Zostera
marina, and widgeon grass, Ruppia maritima, early summer offers the
best chance of recording maximum plant coverage. This measurement of
maximum standing crop provides the best analysis of that year's
productivity at minimum cost.
Flight mission for acquisition of aerial photographs occurred on
May 19 and June 5 in 1980 and on June 8 and 28 in 1981. The
information ;n the distribution and abundance of SAV from these two
years was compared to the baseline information acquired for the
Chesapeake Hay Program in 1978 on June 7, 29 and July 6. Because the
aerial photography was taken at approximately the same time period,
representing a period when the growth of SAV in the lower Bay would be
similar, imagery from all three years should be directly comparable.
Aerial photographs of SAV were also taken in 1979. Because
flights were conducted in the fall, when SAV biomasa is reduced
compared to the early sunnier period when SAV biomass is high (Orth, et
al. , 1979), the seasonally biased 1979 information is not used in this
report.
The next most important condition affecting the value of the
imagery is water transparency. This variable is itself a function of
wind, tide, and turbidity (often related to weather during the
previous 12 hours). Atmospheric transparency is also important since
a high sunlight-to-skylight ratio yields the best SAV-bottom contrast.
Sun elevation is also a consideration since at high elevations (sun
too high in the sky) sun glint will appear in a portion of the frame,
masking the grass or other features used for mapping. This effect i"»
minimized, however, by the proper choice of frame overlap and flight
line side lap. Sun elevations were kept between 25* to 45*.
-------
TABLE 1. GUIDELINES FOLLOWED DURING ACQUISITION OF AERIAL PHOTOGRAPHS
1. Tidal Stage - Photography was acquired at low tide, +/- 0-1.5 ft., as
predicted by the National Ocean Survey tables.
2. Plant Growth - Imagery was acquired when growth stages ensured
maximum delineation of jAV, and when phenologic stage overlap was
greatest.
3. Sun Angle - Photography was acquired when surface reflection from sun
glint did not cover more than 30 percent of frame. Sun angle was
generally between 20° and 40° to minimize water surface glitter. At
least 60 percent line overlap and 20 percent side lap was used to
minimize image degradation due to can glint.
4. Turbidity - Photography was acquirea when clarity of water ensured
complete delineation of grass beds.
5. Wind - Photography was acquired during periods of no or low wind.
Off-shore winds were preferred over on-shore winds when wind
conditions could not be avoided.
6. Atmospherics - Photography was acquired during periods of no or low
haze and/or clouds below aircraft. There was no more than scattered
or thin broken clouds, or thin overcast above aircraft, to ensure
maximum SAV to bottom contrast.
7. Sensor Operation - Photography was acquired in the vertical with less
than 5 degrees tilt. Scale/altitude/film/focal length combination
permitted resolution and identification of one square meter area of
?AV (surface).
S. Plotting - Each flight line included sufficient identifiable land
area to assure accurate plotting of grass beds.
-------
Aircraft scheduling was done in advance around windows in Che
morning and afternoon (2 to 3 hours) near low tide for specific
regions in Chesapeake Bay. NOAA tide tables were used for prediction
of tidal stage throughout the Bay, and a table of suggested flight
windows was made for a one to two month period. The times from 1100
to 1300 EOT were generally avoided to minimize sun glint problems.
The actual decisions to fly on a particular day was made in the early
morning, based on forecasts of regional weather systems, previous
local weather (24 hours), and most important, current conditions.
Because of weather variation, it was generally not possible to pick an
"ideal" day for aerial photography in advance.
The camera used for all aerial photography of SAV was a Fairchild
CA-8 cartographic camera with a 152 mm (6 l/2-inch) focal length
Bausch and Lorab Metrogon lens. Film was Kodak 24 cm (9 1/2-inch)
square positive transparency Aerochrome MS, type 2448, loaded into
magazines in advance. The camera was mounted in a camera port in the
belly of the VIMS single-engine, fixed high wind beHavilland Beaver
aircraft. The aircraft provides a stable platform for vertial aerial
photography from 300 to 3700 m altitude (1,000 to 12,000 feet).
The camera was checked for vertical orientation before each
exposure, using two-axis leveling. Exposures were timed to insure 60
to 65% forward lap (standard frame spacing), and times were adjusted
according to flight line direction in relation to winds aloft. Where
adjacent parallel lines were flown, 301 side lap was planned to insure
mapable quality contiguous coverage. A Wratten 1A haze filter was
used inside the cone of the camera to reduce the degrading effect of
atmospheric haze on image quality.
Personnel on the aircraft during a mission included a pilot,
navigator, and a camera operator. While in the air, the navigator
recorded notes as to atmospheric conditions, flight line number,
altitude, heading, frame count, camera setting, and any unusual
observations on cassette tape with a portable battery operated
recorder. The navigator signaled line start and line stop and watched
for the flight line drift (making suggested corrections to the pilot)
during photography. The navigator was also experienced in the
recognition of SAV areas and modified flight lines or added more lines
during the mission to ensure better or more complete coverage.
Following exposure the 38 m rolls were refrigerated immediately
until they were processed. No more than two weeks elapsed between
exposure and processing. Each roll contained some test exposures to
permit selection of optimum transport speed and temperature during
processing. At the VIMS Remote Sensing Center, the film was carefully
reviewed for quality and adequacy of coverage and entered into the
Center's photo-index system. Cassette photo-logs were transcribed to
typed hard-copy and checked against the film.
-------
Mapping Process
Before mapping, the film was reviewed by photointerpretor and a
biologist to select individual frames for best SAV coverage. The SAV
beds were identified using all available information, including
knowledge of aquatic grass signatures on the film, areas of grass
coverage from previous flight, ground information, and aerial visual
surveys. An estimate of percent cover within each seagrass bed was
made visually in comparison with an enlarged Crown Density Scale,
similar to those developed for estimates of forest tree crown cover
from aerial photography (Figare 2). Bed density was classified into
one of four categories based on an objective comparison with the
density scale. These were: 1. very sparse, (<10%); 2. sparse (10 to
40%); 3. moderate (40 to 70%); or 4. dense (70 to 1002). Either the
entire bed, or sub-sections within the bed, were assigned a number (1
to 4) corresponding to the above density categories.
A Bausch and Lomb Zoom Transfer Scope, model ZT-4H, was used to
trace the delineated SAV bed boundaries from the aerial photography to
base maps of 1:24,000 scale USGS paper topographic (7 1/2-m minute
series) quadrangles. The Zoom Transfer Scope enables the operator to
view the photograph and the map simultaneously, adjust scale, rotate,
and translate one in relation to the other optically, draw the bed
outlines and grass density information directly onto the base map.
Non-changing features common to the imagery and the topograhic
quadrangle, such as road intersections, houses, creeks, etc., were
used for alignment and scaling purposes. After transfer of the bed
outlines onto the base maps the maps were reviewed with the aerial
photography to insure accurate coverage. The original paper
topographic quadrangles have been filed at VIMS for future reference.
Translucent, mylar stable-base topographic quadrangles were placed
over the original base maps, and SAV bed outlines and density
information were transferred with black ink for 1980 data only, based
on the original grant agreement. Data for the 1981 SAV distribution
and abundance which had not been specified in the original grant
agreement but was obtained that year was also placed on paper
topographic quadrangles. However, bed outlines were not transferred
to mylar stable-base quadrangles.
Area Measurement
Areas of SAV beds mapped in both 1980 and 1981 were derived from
the 1:24,000 scale topographic quadrangles. Measurements were made on
a Numonics Graphics Calculator, model 1224. The unit has a resolution
in x and y of 0.24 mm and has registers for scaling and unit
conversion so that areas can be read out in any units desired at map
scale. Accuracy, determined by repetitive measurements of test areas,
is better than 2%. Precision (standard deviation divided by the mean)
ranges from approximately 22 at 16 mm2 (10,000 m2 at a scale ™
1:24,000) to well under 1% at 160 mm2 (100,000 mm2) with an overall
average of 1.4Z,
-------
S6
OOl-O/
99
'*-
f
cc
LLJ
>
o
o
z
o
oc
o
H
z
HI
o
cc
LU
Q.
o
o
c
-------
Historical Sites
Orth, et al. (1979) mapped the changes in the distribution and
abundance of SAV over the last 40 years at six r.reas in the lower Bay:
Guinea Neck and Mumfort Island in the York River, East River in the
Mobjack Bay, Parrott Island in the Rappahannock River, Fleets Bay
which is located just north of che mouth of the Rappahannock River and
Vaucluse Shores on the baysida of the Eastern Shore of Virginia near
Cape Charles. The imagery from 1980 and 1981 allowed us to follow
each of these areas for continued alterations in the distribution and
abundance of SAV.
RESULTS
The aerial photography and subsequent mapping process in 1980 and
1981 resulted in the delineation of SAV presence or absence in 27
topographic quadrangles along the eastern and western shores of the
lower Chesapeake Bay (Fig. 3). These areas in the meso- an^
polyhaline regions were the principal areas mapped in the baseline
survey in 1978 (Orth, et al., 1979) and represent areas dominated by
eelgrass (Zostera marina) and widgeongrasj (Ruppia maritima). The
total area of SAV as represented on each quadrangle for 1980 and 1981
are presented in Table 2 along with data from 1971, 1974 and 1978 for
those quadrangles which were mapped for SAV in those years (Orth and
Gordon, 1975; Orth et al., 1979). Discussion of the distribution and
abundance of SAV in the lower Bay is presented below based on major
sections of the Bay rather than individual topographic quadrangles
(e.g. the York River rather than Clay Bank, Achilles, Yorktwon and
Poquoson West quadrangles) (Table 3).
James River Section (includes Newport News South and Hampton
Quadrangles)
Very little SAV had been observed in this area in the last 10
years (Tables 2 and 3). Most of the SAV was restricted to very patchy
beds distributed along the shoreline from Newport News Point to the
Hampton Roads Bridge Tunnel. These few areas that had SAV in 1978
showed no evidence of vegetation in 1980 and or 19*51.
Lower Western Shore (includes Hampton, Poquoson East and Poquoson West
Quadrangles)
The changes in t!ie distribution and abundance of SAV in the lower
Western Shore over the last 10 years (Tables 2 and 3) demonstrates a
pattern similar to that found in many other sites around the lower
Bay. This is, there was a marked decline observed between 1971 and
1974 followed by relative stability since then, with perhaps 3
moderate increase in density and expansion of the remaining beds since
1978.
Declines of vegetation between 1971 and 1974 occurred principally
in the most upriver, vegetated portions of the Back and Poquoson
River, where a complete loss was observed, and in the beds fringing
along the Chesapeake Bay where there was decrease in size and density.
-------
76° 00'
Figure 3. Locations of topographic quadrangles in Virginia which were
covered with aerial photography for SAV in 198U.
-------
o
oo
06
£
_)
o
1
Q
o-
a.
O
O
O
cfl
b.
O
V)
at
S
a
00 \O
O CM
csom
mOOO
OOOOO
(o o o o o
30
OOOOOOOOOOOOOOOOOCOOOO
OO 30000OOOOOOOOOOOOOOO
000
ooo
o o o o
o o o o
, o O
, o O
o
o
«•> I I I I I I I
!-• I I I I I I I
I I
I I
I I I I
I I I I
09
o
cr
o
a,
o o o •- o o o
0000
I i/*i/>o> 4i<"ii/>mmOvOf*im
o
u
I I
I I
00
c
tfl
, 2.
ID
or\X
« a>
U) 3
•f
•f
b
o
"s
o
a,
41
(« X
+ -f
Jt 4> 4J Jt
e c e c o) e . U — + 41 9J 3 <0 «
—i C 0) 1( 14 C'-'kiOO'-ICB
+ -*O93**0)-0,•-
Koacu>o
£ «j »j .^ uj -a -
a/i-cn/-ooooc<«^— •
I 09
a
90
(0
•o
18
e
jC
5
05
>,
O.
ki
00
o
o
o.
u
4)
eg
ig
t>
TJ
c
i
V
4.
•O
4.
a.
D.
Q
U
0)
41
e
o
09
11
00
TJ
-------
TABLE 3. NUMBERS OF HECTARES OF BOTTOM COVERED WITH SUBMERGED AQUATIC
VEGETATION IN 1971, 1974, 1978, 1980, and 1981 FOR DIFFERENT
SECTIONS IN THE LOWER BAY ZONE (NUMBERS OF HECTARES ROUNDED OFF TO
NEAREST WHOLE NUMBER) (* INDICATES SECTIONS THAT VJERE NOT MAPPED
THAT YEAR) (DATA FROM ORTH AND GORDON 1975; ORTH et al. 1979; AND
UNPUBLISHED DATA)
Year
Section
1971
1978 1980 1981
Tangier Island Complex
(Includes from MD-VA border to
Chesconessex Creek)
Lower Eastern Shore
(Chesconessex Creek, to Elliotts Creek)
Reedville
(Includes area from Windmill Pt. to
Smith Pt.)
Rappahannock River
(Includes Rappahannock and Piankatark
Rivers, and Mil ford Haven)
Nev Point Comfort Region
Mobjack Bay
(Includes East, North, Ware, and Severn
Rivers)
York River (Clay Bank to mouth of York)
Lower Western Shore
(Includes Poquoson and Back Rivers)
James River (Hampton Roads area only)
TOTAL FOR LOWER BAY ZONE
2814 2420 2794
1991 1370 1691
1273
168
1294
493
68
233
1593
141
364
93
271
1785
157
31
3
182
1317
135
133
43
207
1275
142
8409
12
-------
The photographic evidence indicates that although the vegetation in
this region nas not increased significantly in irea since 1978, the
beds have become somewhat more dense. However, there is little
evidence of regrowth to the former upriver limits of the distribution.
York River (includes Poquoson West, Yorktown, Clay Bank ayd Achilles
Quadrangles)
Between 1971 and 1974 significant declines of vegetation in the
York River section (Tables 2 and 3) occurred principally in the most
upriver beds. Most of these denuded areas were found in the region
bounded by the Clay Bank a.id Yorktown quadrangles (Table 2). By 1974
only scattered small patches of vegetation remained of the formerly
extensive beds of eelgrass and widgeon grass at these upriver sites.
By 1978, these too had largely disappeared.
Those beds of vegetation found closer to the mouth of the river
in 1971 (portions of the Achilles and Poquoson West quadrangles) also
declined significantly between 1971 and 1974. However, as proximity
to the mouth of the River increased, the dieback was less extensive,
such that there was an increase in the percentage of each bed
remaining. This partial reduction compares to the almost complete
decline experienced 5 to 10 km upriver during the same period. The
pattern of decline evident in these lower York River beds was one of
loss of vegetation in the deeper offshore sections of the beds with
survival of vegetation in the nearshore zone. However, these
differences in depth where the vegetati. i remained and where it
disappeared represent vertical distances of less than one meter. In
most cases the formerly vegetated areas consist of wide, shallow flats
100 m to 1000 M wide with little or only moderate slopes and depths
ranging from 0 to 1 meter below MLW.
Evidence indicates that the decline of SAV in the York River
occurred quite rapidly. Although comprehensive aerial photography of
the region is available only for the years 1971 and 1974, archival
search of photographic records revealed several other overflights
during the 1971-1974 period. They document the persistence of dense
beds of SAV rs late as April 1973 in areas showing significant losses
by the sunner of 1974. This would suggest that much of the loss
occurred within one year, between the summer of 1973 and the summer of
1974. Since recent studies of SAV biology and transplantation in the
Chesapeake Bay have revealed that the remaining vegetation in this
region undergoes significant annual late-summer diebacks, we feel it
is very possible that an extreme dieoff during July and August of 1973
related to high temperatures, low light levels and the absence of the
periphyton grazers may have been responsible for the lack of
vegetation in 1974.
There is no evidence as yet to suggest Lhe decline of the
vegetation occurred in one area of the river before another. In fact,
it appears that the decline of the vegetation occurred simultaneously
-------
in all the areas but that the severity of the decline varied from site
to site.
From 1978 to 1980 the vegetation in the York had remained
relatively stable in aerial distribution. Since 1980 however we have
observed -»ome regrowth by seedlings onto denuded sand flats in the
vicinity of remnant SAV beds in the lower York. During the spring of
1982 we observed that many of the seedlings evident in 1980 and 1981
had grown into small patches (1 m4-) of vegetation. There has been as
yet no regrowth into the completely denuded upriver sites. Eelgrass
transplanted into these upriver areas during 1980 and 1981 died during
the July-August period while those transplanted in areas where the
seedlings occur have survived (Orth and Moore, 1982).
SAV at two of the historical sites in the York River chosen for
intensive mapping, declined between 1971 and 1974 (Table 4. Fig. 4).
SAV at the Mumfort Island site was completely gone by 1978 while at
the Jenkins Neck site, some vegetation persisted through 1978 and now
has increased through 1981. Much of this increase, as mentioned
above, appears to be a result of successful recruitment from seeds and
their subsequent rapid growtb. This new growth is occurring in the
most shallow areas close to land while little or no revegetation is
occurring in the offshore, deeper areas, except for some replanted
areas adjacent Aliens Island (Orth and Moore, 1982).
Mobjack Bay and New Point Comfort (includes Achilles, New Point
Comfort, Ware Neck and Mathews Quadrangles)
The Mobjack Bay and it« adjacent New Point Comfort section of the
lower Chesapeake Bay have been characterized by a less severe decline.
SAV beds over the last 10 years compared to areas such as the York and
Rappahannock rivers (Tables 2 and 3). Where declines have oocuired
since 1971 they have primarily been in th«: offshore, deeper sections
of the broad beds fringing the Mobjack Bay and in the upstream
sections of its associated rivers (Severn, East).
The historically mapped site at the mouth of the East River
(Table 4, Fig. 4) typifies the pattern of the Offshore to inshore loss
of SAV. A detailed overlay of this site from 1974 to 1981 shows the
alteration of the SAV bed primarily along the outer fringe (Fig. 5).
This pattern of limited declines since 1971 in the areas fringing
along the bays and more severe changes in the tributaries follows that
of most of the other sections around the Virginia portion of the
Chesapeake (Orth and Moore, 19811)). This would seem to imply that
those factors limiting SAV growth were related to the salinity regime.
In those areas where runoff was greatest, thereby reducing salinity,
turbid water conditions also were associated representing additional
stress on the plants.
-------
TABLE 4. AREAS OF SAV AT HISTORICAL MAPPING SITES (LOWER BAY SECTION) 1937-1981
Parrott Islands
Date
1937
1951
1960
1968
1974
1978
1980
1981
<102
0
394,797
411,306
92,064
0
0
0
0
10-40*
297,024
778,146
631,566
1,354,110
2,922
22,872
0
0
Area m^
40-702
1,598,268
1,222,410
547,014
1,205,628
7,710
0
0
0
70-1002
0
1,158,384
1,947,372
124,374
0
0
0
0
Total
1,895,292
3,553,737
3,537,258
2,776,176
10,632
22,872
0
0
Fleets Bay
Date
1937
1953
1961
1969
1974
1978
1980
1981
<10X
0
1,488,258
1,572,612
1,436,403
105,714
167,688
0
0
10-40*
1,385,424
597,354
1,330,140
1,938,660
1,624,884
528,91*
121,890
683,250
Area a?
40-70*
548,076
591,018
1,643,892
1,592,170
1,325,040
33,592
26,040
9,816
70-100*
744,864
28'+, 232
884,280
270,372
0
0
2,':7/
13,986
Total
2,678,364
2,960,862
5,430,924
5,237,605
3,055,638
730,198
150,402
707,052
Mumfort Islands
Date
1937
1953
1960
1971
1974
1978
1"80
1981
<10*
0
151,728
0
0
0
0
0
0
10-40*
495,060
699,252
258,210
685,536
127,488
0
0
0
Area a?
40-70Z
397,368
106,356
1,880,238
1,088,976
23,826
0
0
0
70-1002
23,832
1 ,461 ,846
0
0
0
0
0
0
Total
916,260
2,419,182
2,138,448
1,774,512
151,314
0
0
0
15
-------
X
TABLE 4. (continued)
Date
1937
1953
1960
1971
1974
1978
1980
1981
Dace
1937
1953
19t>3
1971
1974
1978
1980
1981
Date
1938
1948
1955
1966
1972
1978
1980
1981
<102
0
426,480
140,448
0
93,972
132,714
60,810
0
<102
1,024,010
591,840
31,032
0
509,730
47,860
191,520
0
-------
nj
•o
ft
Ol
a.
«
n
OJ
o
01
g
X
•H
0)
00
n
kl
01
o
u
CO
ca
•o
V
kl
H
«o
S3HV1D3H
«»
01
60
U.
17
-------
o
.0
0)
fH
T3
en
c
cu
OC
rt
u
X
«
CO
.o
£
o
o
0.
<3
Vi
01
00
VM ON
O -«
O
a. o
§
oe
18
-------
Rappahannock River Section (inclftes Mathews, Wilton, Pelt ville and
Irvington Quadrangle^T
Like the York River, the lower Xappahannock R;vt- ano the
adjacent areas of the .'iankatank River and Milfoid Haven n the south
experienced a precipitous decline in SAV between 1971 and 1974 (Tables
2 and 3). Formerly wntensive beds of eo'gras? and widgeon grass, 100
m to 500 ra wide, found along most of the shoreline in this section
appeared as only scattered patches of • egetation in 1974. Between
1974 and the present, several sparse patches ot vegetation have
persisted but the abundance of SAV in this particular region may be at
the lowest level ever recorded. There has been as yet no evidence of
any significant regrowth of SAV in the entire region.
All the SAV at the Parrott Island historical site was gone by
1978 (Orth, et al., 1979) with no regrowth of any SAV between 1978 and
1981 (Table '», Fig. 4).
Reedville (includes Fleets Bay and Reedville Quadrangles)
Although the aerial photography record is less complete for this
section of the lower Bay, extensive beds of SAV are evidenced
throughout much of the shoreline until 1974 (Table 2 and 3). By 1978,
only relatively sparse areas of SAV represented the remnants of the
formerly dense beds of eelgrass and widgeon grass. Between 1978 and
1980 significantly fewer of even these sparse areas were observed,
suggesting a gradual loss of the remaining grasses. Some increase in
density and area of the remaining beds was observed in 1981 but no
widespread recovery was evident.
The Fleets Bay historical site (Orth, et al., 1979) represent the
changes that have occurred in this section (Table 4, Fig. 4). The
changes at this site differ in one major aspect from the other
intensively mapped sites where SAV has declined. The decline in the
York River and Parrott Island historical sites occurred between 1971
and 1974. Although 1971 data are lacking for the Fleets Bay site, SAV
appeared to undergo a major decline between 1974 and 1980 with a
slight increase in area in 1981.
Eastern Shore (includes Elliotts Creek, Townsend, Cape Charles,
Cheriton, Franktown, Jamesville, Nandua Creek, Pungoteagae, Tangier
Is lard, Chesconessex, Parksley, Ewell and Great Fox Island
Quadrangles)
Although quantitative mapping of the entire Eastern shore of the
Bay was not done prior to 1978, qualif :• e analysis of available
information as well as the mapping of one historical site at Vaucluse
Shores (Table 4) suggest that many of th*> SAV beds found along this
sec'.ion have not changed appreciably since 1970. Quantitative data
since 1978 reveal little significant change over the last few years,
especially in the extensive beds in the vicinity of Tangier Island and
Snith Islands where much of the vegetation is located (Tables 2 and
-------
3). Some of the variability observed in the vegetation of the more
northern topograpnic quadrangles in this section (i.e. Great Fox
Island) may be due to the abundance of widgeongrass associated with
the eelgrass. This species reaches a maximun standing crop slightly
later in the summer than eelgrass and its coverage as viewed from the
air in June appears more variable from year to year than eelgrass.
Additional variation is due to the extensive areas of relatively
sparse vegetation «10Z cover) found from Nassawadox Creek north. The
observable bed outlines of many of these areas of viewed from the air
may vary considerably from year to year. If converted to biomass
however, the impact of these changes in aerial coverage would be
greatly reduced.
Many of the SAV beds found along this Eastern shore section are
protected by offshore sandbars from the dominant northwest winds. As
the sandbars migrate, portions of the existing beds become covered
with sand (Orth, et al. , 1979). Presumably, as other bar migration
forms suitably protected habitat, new SAV beds are formed. The
Vaucluse Shore historical site (Fig. 4) is indicative of this
phenomenon. We feel that without the protection afforded by these
sandbars, SAV would not persist along much of this shoreline (Orth, et
al., 1979).
SUMMARY
Beds of submerged aquatic vegetation in the lower Chesapeake Bay
were mapped from aerial photography obtained in 1980 and 1981 onto
U.S.G.S. topographic quadrangles (1:24,000 scale). Aerial photography
was acquired using similar techniques and film and under constraints
observed in the acquisition of the 1978 photography to insure maximum
delineation of the SAV beds and to obtain comparable data. Only those
topographic quadrangles in the polyhaline and mesohaiine areas of the
lower Bay were monitored in 1980 and 1981, resulting in the mapping of
27 quadrangles. The dominant vegetation consisted of eelgrass and
widgeongrass.
In 1980 and 1981, 6460 hectares and 7281 hectares of SAV were
mapped, respectively. Tnis compared to 8409 hectares for a similar
area in 1978. Reductions of SAV from 1978 to 1980 occurred in all
sections of the lower Bay except in the lower western shoreline.
Almost no vegetation was found in the Rappahannock River section in
1980 with only a slight increase in 1981. The SAV in the James River
in 1978, which exi?t.^d in a narrow band between Fort Eustis and
Newport News Point, was completely absent by 19UO.
The predominant SAV beds in 1980 and 1981, were still found in
Chose major areas identified in 1978: 1. along the western shore of
the lower Bay bPtween Back River and York River; 2. along the
shoreline of the Mobjack Bay and immediately adjacent to the Guinea
Marshes at the mouth of the York River; 3. the shoal area between
Tangier and Smith Island (this represented the largest and most
extensive SAV bed in the entire Bay); 4. behind large protective
-------
sandbars near Hungar's Creek and Cherrystone Creek along the Bay's
eastern shoreline.
Comparison of the 1980 and 1981 data at the six historical SAV
sites mapped in 1978 showed no recovery of any SAV at the Parrott
Island (Rappahannock River) and Mumfort Island (York River) site.
These two sites remained devoid of any SAV. SAV at the Fleets Bay
site continued to decline from 1978 ato 1980 but showed a slight
rebound in 1981. At Vaucluse Shores, SAV beds remained relatively
stable during this time period. SAV at the East River (Mobjack Bay)
site, declined both in 1980 and 1981 from 1978 levels. A comparison
of SAV bed formations from 1974 through 1981 (four complete surveys)
showed the decline of SAV to have occurred primarily in the deeper,
offshore areas rather than the inshore, more "hallow locations. This
pattern was repeated in many other locations in the lower Bay region.
Although total SAV area showed a slight decline in 1980 and 1981 at
the Jenkins Neck (York River) site, recruitment by eelg-ass seedlings
was observed in the vicinity of Aliens Island both year* and primarily
in the more inshore, shallower areas. These seedling grew vigorously
and resulted in numerous patches measuring up to one nr. This pattern
was also observed along the York River shoreline from Aliens Island to
Sarah's Creek.
Since 1978 then, although there has been some overall decrease in
the area vegetated with SAV in the lower section of the Bay, the
declines we noted between 1978 and 1981 were not as great as the
declines that occurred between 1971 and 1978. Indeed, SAV in some
areas, for example in the lower York River, have actually increased in
abundance between 1980 and 1981. Aerial photography obtained in 1982
(but not mapped) indicate that this trend of increasing SAV abundance
continued into 1982. Continued annual mapping will allow us to better
define these rapid changes. We therefore strongly recommend ,-n annual
monitoring program for SAV using aerial photography. In addition
because of the rapid, large scale changes in SAV distributions which
can occur within one growing season the shorter the interval between
the data the better.
The low cost, efficiency and accuracy of using aerial photography
for mapping bAV distribution and abundance are the main advantage of
this technique compared to ground surveys. Because of the importance
of SAV in the Bay, an annual inventory of this resource should be
considered a high priority by state management agencies.
21
-------
LITERATURE CITED
Anderson, R. R. and R. T. Macomber. 1980. Distribution of
submerged vascular plants, Chesapeake Bay, Maryland. Final
Report. U.S. E.P.A. Chesapeake Bay Program. Grant No. R805970.
126 pp.
Orth, R. J. and H. H. Gordon. 1975. Remote sensing of sumberged
aquatic vegetation in the lower Chesapeake Bay, Virginia. Final
Report NASA-10720. ',2 pp.
Orth, R. J. and K. A. Moore. 1981 a. Submerged aquatic vegetation
in the Chesapeake Bay: Past, present and future. Trans. 46th
North American Wildlife and Natural Resources Conf. pp. 271-283.
Orth, R. J. and K. A. Moore. 1981b. Distribution and abundance of
submerged aquatic vegetation in the Chesapeake Bay: A scientific
summary. VIMS SRAMSOE No. 259. 42 pp.
Orth, R. J. and K. A. Moore. 1982. The biology and propagation of
eelgrass, Zostera marina, in the Chesapeake Bay, Virginia. Final
Report. U.S. E.P.A. Grant No. R805953 and Virginia Institute of
Marine Science SRAMSOE No. 265. 195 pp.
Orth, R. J., K. A. Moore and H. H. Gordon. 1979. Distribution and
abundance of submerged aquatic vegetation in the lower Chesapeake
Bay, Virginia. U.S. E.P.A. Final Report, Chesapeake Bay Program.
EPA-600/8-79-029/SAV1.
-------
/-
APPENDIX A
TOPOGRAPHIC QUADRANGLES SHOWING THE DISTRIBUTION
AND ABUNDANCE OF SAV WHERE SAV WAS PRESENT (1 - <1J%;
2 - 10-40%; 3 - 40-70%; 4 = 70-100%).
QUADRANGLES FOR 1981 ARE NOT PRESENTED AS THIS WAS NOT PART OF THE
GRANT OBLIGATIONS. PLEASE REFER TO ORTH, MOORE AND GORDON (1979) FOR
COMPARISON OF WE 1978 TOPOGRAPHIC QUADRANGLES.
-------
;..••-.-..-
-••--. \ •{/•vv.^.m
. \ ~V N Vl r'—: •••'••}'
i \\ i. \ • \ .~ .' ic •• ,/
-------
» 4 V
-------
H*. 'H » »W,il
» " • I
*•;•$<
•:•! -• J
-^j^^S^^^i" "••-
& '^".7*^/7 - ' V^T V
,-NK. vfifTw^^-^. '. . ... f . ..... V
--•-->;• -v r •*. .-• --. ^
1 -•* ^ -> ^"i,.
^aferfS*'.^-.^ M ^:'' -
^"i<^ '^je- ^\-Vc
&fe\^.-' ;;v?.^~i- '- ?* ^'.. 7
•>2>w. - .1 , '' >» -*<. ••••"' /
^,- ^J<,' • .••• v -..,' j, ^- %«j,
1 •• 'VrV > ' •' ' v ,«•«•'' ^*-/r
• ^f^^^'-f^^. \'f'..K •
-------
/>?v- \,<:- ..--'/
-~ •• . , , . \ \- »
« \ f \ \
\- r •.-. i \ t.
,- -v-,^'-
h"Y ^ .-.". .. — V : »
27
-------
-------
'. /I
^ ^**~' •' /j'
-------
.. f 'i'i '4 •'
*•"
:•'..*- -
-tft
. . ,
, -i »• L /- • • • >*•
:; :» ; \ .-./-
-• ,; • . "N'
.' / ••-, . ,:-. i
.
-------
*
i.% • «•.
-------
\Mvno «r*m
tmaumm o»n« «
MOLOQKM. m«in
, .• ' - 7" ' ' "-» ^ '
}f /" ~ •£ ' ' -'.'.
.
t •»
*• W
32
-------
•' ••• /
•. /
•/ V
>• •
• . -
V - •
-• V
(1
-------
V \
N '
UHlTtP »I»T»»
MTMINT <* -M« iMIt
OIOUKMCA4. »U»*i
1»LTW Of VlflQINl
KUJOTO f«(* QUAOKftNOlt fjf
•-
-------
fVw flL ™^."*^ «*— . __ ^v
-------
-------
1 ;
-------
-------
CHfSAFfAh t.
BAY
•" tlrf
; 'i
-------
.;«*"
M u / =
-------
f- ./
X '""
-------
-• • /
-------
-------
-------
* /
«• I
-------
SECTION II
INTERACTIVE EFFECTS OF LIGHT,
EPIPHYTES AND CRAZi-RS
-------
CHAPTER 1
EPIPHYTE-SEAGRASS RF'.ATIONSHIPS WITH AN EMPHASIS
ON THE ROLE OF MICROGRAZING.
A REVIEW1
Robert J. Orth
and
Jacques van Montfrans
Virginia Institute of Marine Science
and
School of Marine Science
of the College of William and Mary
Gloucester Point, Virginia 23062
^Contribution No. 1040 from the Virginia Institute of Marine Science
-------
ABSTRACT
Despite the recent advances in seagrass ecology over the last 10
years, there are still numerous aspects on the ecological and
biological interactions that occur in seagrass ecosystems that remain
poorly understood. We have attempted to place into perspective one
interrelationship that could have important implications in the
production and vigor of seagrasses. This is the relationship between
epiphytic fouling by macroalgae and periphyton and the grazers which
consume them as a food source while leaving the leaves intact. Our
approach to this review was to first describe the relationships
between macroalgae, periphyton and the seagrass host in terms of
physical benefits, biochemical interactions, factors which reduce
fouling on the host and effects of epiphytism on seagrass
photosynthesis. We then examined the importance of epiphytes as a
food source for those herbivores found in seagrass beds and then
looked at the consequences of this grazing and removal of epiphytes
for the seagrass host. Based on the potential impact of epiphytes on
seagrasses and grazers on epiphytes, we developed a hypothetical model
that describes the effect of increasing epiphytic fouling on seagrass
production in the presence and absence of grazers. From this model,
we made predictions on the direction of seagrass decline with
diminishing light along depth and estuarine gradients. Lastly, we
briefly touched on the problem of eutrophication and how it affects
the balance of these interrelationships and the management options to
insure the health and survival of seagrass habitats in the face of
increasing stress by man on these critically important areas.
Aft
-------
INTRODUCTION
Recent emphasis on seagrass research has shifted from a primarily
descriptive approach to attempt to understand the functional ecology
of such habitats. Books containing review papers on seagrass
ecosystems (McRoy and Helfferich, 1977; Phillips and McRoy, 1980) as
well as the large number of articles appearing in many scientific and
popular journals, attest to the progress made in understanding
seagrass habitats on a worldwide basis. There are, however, numerous
aspects of the functional ecology of these complex systems that still
remain poorly understood. One such area involves the
interrelationship between epiphytic fouling by both macrualgae and
periphyton (loosely defined here as the community of diatoms,
microfauna and particulate material [Weitzel, 1979]) adhering to
seagrass blades and the grazing organisms which rely on these as
important food sources. The grazing community associated with
seagrasses consists of a variety of organisms whose activities range
from consumption of the leaf blade with the epiphytes to removal of
only the epiphytic assemblage. We have limited our discussion to
grazers, such as gastropods, crustaceans and some species of fish,
whic^ consume only macroalgae and/or periphyton found on the surface
of the leaf blade while leaving the leaf intact.
The main emphasis of this review concentrates on the: 1)
relationships between macroalgae, periphyton and the seagrasses which
they colonize; 2) importance of epiphytes as a food source for
numerous herbivores found in seagrass beds; 3) consequences of grazing
on epiphytes for the host plant; and 4) ways in which eutrophication
affects the balance of these complex interrelationships. We will also
briefly touch on the management implications of these inter-
relationships for the health and survival of seagrass habitats based
on the current level of knowledge.
I. EPIPHYTE-SEAGRASS RELATIONSHIPS
Seagrasses grow in a variety of sediment types in shallow water
and frequently provide the only available solid substrate for the
attachment of macroalgae (Huram, 1973). Their presence can increase
the surface area of the bottom available for colonization by epiphytic
or epibenthic diatoms by a factor of 5 to almost 19 (Kita and Harada,
1962; Reyes-Vasquez, 1970; Gessner, 1974). The total primary
productivity of the seagrass habitat is substantially increased (Wood
et al., 1969) because seagrass provides a suitable substrate for other
photosynthetic organisms.
A diverse assemblage of microflora and macroflora is associated
with the seagrass blades (Harlin, 1980). The presence of these
AQ
-------
organisms on these blades results from a number of complex
interrelationships that not only have important implications for the
growth of the seagrass but also may have led t- the evolution of
internal mechanisms to suppress eniphytic growth. For the purpose of
discussion, we have divided the relationships into those which a)
provide physical benefits to the epiphyte or seagrass, b) involve
biochemical interactions, c) are concerned with factors which reduce
fouling, and d) involve implications of epiphytism on seagrass
photosynthesis.
a. Beneficial Effects of the Relationship: Physical
Few beneficial effects for seagrasses of this epiphyte-host-
relationship nave been discussed in the literature. Penhale and Smith
(1977) suggested that the presence of epiphytes can reduce the effects
of desiccation when Zostera marina is exposed at low tide. Richardson
(1980) surmised that seeds of Ruppia maritima which were released
under mats of epiphytic algae were more resistant to desiccation when
water levels dropped and the exposed seeds were protected from drying
out by the overlying algae. Halophilia engelmanni was found to have a
low tolerance to ultraviolet-B radiation and it was postulated that ti.
engeImanni relied on periphyton shielding as well as shade provided by
other seagrasses to reduce photoinhibition (Trocine et al., 1981).
Its congener Halophilia stipulacea also exhibited photoinhibition at
lower light intensities than Cymodocea nodosa, Pbyllospadix torreyi,
Posidonia oceanica, Zostera angustifolia and Z. marina (Drew, 1979).
Perhaps the former specs.ss relies on shading by epiphytes and
surrounding vegetation to reduce light intensities as well.
Epiphytes of submerged vascular plants are believed to benefit
from the association by their enhanced proximity to light and water
currents carrying dissolved nutrients (Hariin, 1980). The swaying
motion of seagrasses caused by wave action and currents may be
important in producing steep chemical diffusion gradients and removing
potential growth inhibiting substances as well as accumulated
sediments. The results of this physical movement alone enhances the
exchange of nutrients and epiphytic growth (Conover, 1968; Hariin,
1975, 1980).
b. Biochemical Interactions
Several studies have been conducted which enumerate the diverse
macro- and microflora assemblages associated with submerged vegetation
(Hariin, 1980, partial review). Although some macroalgal species
(e.g. Punctaria orbiculata and Smithora naiadum) are believed to bft
more dependent on their raacrophyte host for the completion of their
life cycle (Hariin, 1975), the vast majority are thought to merely
utilize the host as a substrate for attachment. Similarly, most
diatom species found on marine angiosperms are classified as obligate
epiphytes (Mclntire and Moore, 1977) although their occurrence is by
no means restricted only to angiosperms (Brown, 1962; Main and
Mclntire, 1974; Jacobs and Noten, 1980). Some diatom assemblages of
-------
macrophytes were found to be essentially the same as those colonizing
the surrounding bottom (Sullivan, 1977). It is likely, however, that
under nutrient limited conditions, microalgae, such as unicellular
diatoms, which are more intimately associated with the macrophyte host
epithelium, are influenced to a greater extent by host metabolism (and
vice versa) than the larger multicellular erect forms. Because of
their large surface area to volume ratio, unicells have a more
intimate relationship wi'.h their microcellulai plants (Wood, 1972).
This fact may be partially responsible for the observation that
periphyton productivity or biomass have been shown to track that of
the seagrass substrate (Penhale, 1977; Sullivan, 1977; Jacobs and
Noten, 1980). Indeed, it has been shown that the dissolved organic
carbon (DOC) released by marine macrophytes (Penhale and Smith, 1977),
although small, is assimilated by algal and bacterial populations
associated with the macrophytes (McRoy and Goering, 1974; Brylinsky,
1977; Penhale and Thayer, 1980; Smith and Penhale, 1980). The low
molecular weight (500-10,000 mw) fraction of DOC released from the
leaves of three marine angiosperms (Thalassia testudinum, Zostera
marina and Halodule wrightii) was differentially assimilated by
bacteria in the periphyton of epiphytized plants whereas the high
molecular weight (mw 10,00) fraction was not appreciably utilized
(Wetzel and Penhale, 1979). Thus, release of DOC may enhance the
growth of bacteria while converting dissolved carbon into particulate
material that is subsequently incorporated into the marine food web by
grazing organisms (Smith and Penhale, 1980).
Nutrient uptake by the roots of seagrasses and subsequent release
of these nutrients via the leaves (McRoy and Barsdate, 1970; McRoy
et al., 1972) bathe the periphyton in a nutrient-rich medium.
Although net transfer of phosphorus from the roots via the leaves to
the epiphytes of Zostera marina is small, 15 to 1002 of the released
phosphorus was assimilated by the associated epiphytes (Penhale and
Thayer, 1980). Similarly, epiphytes of "I, marina take up nitrogen
released by the seagrass (McRoy and Goering, 1974) even though
bluegreen algae in the periphyton community were shown to fix large
amounts of nitrogen (Goering and Parker, 1972). Both processes may
play an important role in nitrogen cycles of seagrass habitats. It
appears that dense epiphyte communities can be indirectly maintained
by the uptake of nutrients released from the seagrass leaves as
postulated by several workers (Harlin, 1971; McRoy and Goering, 1974).
The overall response of the periphyton to various metabolic
exudates of marine phanerogams is poorly understood. Individual
diatom species exhibit a highly varied response to different nutrients
(Lee et al., 1973; Saks et al., 1976). Biochemical interactions nay
be partially responsible for the observation that the pennate diatom
Cocconeis scuteHum is the sole pioneer species on Zostera marina,
formifg an unialgal mat over newly formed blades (Sieburth and Thomas,
1973). The mat is in turn colonized by a variety of micro-organisms,
primarily bacteria and other species of diatoms, all of which are
incorporated in a thick mucous matrix (Fig. P (Sieburth and Thomas,
1973; van Montfrans et al., in press). The peri|->byt.m, harrier slows
51
-------
en
3
V4
O
m
in oi
•H O
•o
0)
V C
4J O
« -H
C 4J
C I*
41 O
O. D.
O IK 41
W J= O.
Q u CX
•H O 3
' 4)
ac .H
c 01
•H f
3 j-i
O -H
^ o,
Bl 41
w CO
CO B
3 -H
o . oi
j: w
O. en
•H O
M N
41
a 4)
*i O
4-1
IM
o >>
iH
f *->
a u
C
IH
C /-N
aj CM
1) 00
ca at
•H
M 0)
X) C
oi *
JS ^
52
-------
the diffusion of chemicals and nutrients into the surrounding water.
Detritus (up to 80% volume, Kita and Harada, 1962) becomes
incorporated in the mucous matrix as the periphyton community
develops. It originates from the abundant epifauna associated with
j£. marina (Marsh, 1973) although much of it also settles from the
water column. This material further increases the surface area
available for bacterial colonization and adds to the biochemical
complexity of the periphyton crust. Although numerous abiotic factors
including salinity, temperature, pH (Brown, 1962; Lee et al., 1975a,
b), insolation (Main and Mclntire, 1974; Borum and Wium-Andersen,
1980; Jacobs aad Noten, 1980), nutrients released from the surrounding
sediments (Reyes-Vasquez , 1970) and various environmental factors
associated with tide levels (Penhale, 1977) affect the microcommunity ,
biochemical interactions between the seagrass substrate and the
periphyton should not be overlooked.
c . Factors Which Reduce Fouling
Numerous factors reduce fouling on seagrasses. Some are strictly
size related, whereas others involve complex biochemical mechanisms
and growth responses evolved by the seagrass host. Ingestion of the
periphyton crust on grass blades by the numerous grazers present in
seagrass habitats also reduces fouling.
Macroalgae are restricted in their ability to successfully
colonize submerged angiosperms by the size and nature of their
attachment organ or basal disc (den Hartog, 1972). Algae with smaller
basal discs are therefore able to colonize a greater variety of
macrophytes than those with larger discs. It stands to reason that
the broader leaved genera of marine vascular plants such as Zostera
and Posidonia have a greater diversity of associated macroepiphytes
than narrow leaved genera like Ruppia and Syringodium. May et al.
(1978) found a greater diversity of epiphytes on Posidonia australis,
a larger plant with a larger leaf area, than on Zostera capricorni and
Z^. tasmanica with less leaf surface area. Wood (1959) states that
narrow leaved Ruppia had few epiphytes in a study of Australian
macrophytes.
Like macroscopic algae, diatoms appear to be specific in their
selection of a suitable sized substrate. Species such as Cocconeis
s cute Hum which have a large surface area for attachment were shown to
avoid finely branched algal thalli in preference for more thickly
branched species (Raram, 1977). It is possible that similar
preferences exist for seagrasses with genera such as Posidonia and
Zostera housing a greater complement of diatom species having a large
attachment site than narrow bladed seagrass genera such as Ruppia and
Syringodium. The genus Cocconeis is dominant on Zoatera marina
(Sieburth and Thomas, 1973; Jacobs and Noten, 1980T and Thalassia
testudinum (Reyes-Vasquez, 1970; DeFelice and Lynts, 1978) whereas
Navicula povillardi , a narrow diatom, accounted for one of every three
individuals encountered on Ruppia maritima (Sullivan, 1977).
Ruppa
(1980
Howard-Williams and Liptrot (1980) reported that Zostera capensis
53
-------
supported a considerably greater biomass of diatoms per unit mass of
host tissue than Ruppia cirrhosa did in South Africa estuaries.
Macroalgae can also be excluded from successively colonizing
marine phanerogams by the ephemeral nature of the macrophyte
substrate. It is known that epiphytes of ephemeral nature are rare
whereas perennial algae have a much greater association of
macroepiphytes (den Hartog, 1972). A successfully colonizing epiphyte
species must complete its life cycle according to a time scale that
corresponds to the presence of the seagrass substrate. Similarly,
Jacobs and Noten (1980) stressed the importance of seasonal growth
patterns of Z_. marina in determining community structural differences
of the periphyton. They pointed out that seasonal growth ultimately
regulated the average life time ot the seagrass substrate and this in
turn had an influence on epiphyton community structure.
Many seagrasses are known to rapidly produce new photosynthetic
tissue. Zostera marina in Danish waters produced a new leaf every 14
days which had an average life span of 56 days (Sand-Jensen, 1977).
Jacobs and Noten (1980) indicated that shoots of Z,. marina along the
coast of France produced a new leaf every 13 days in May when
insolation was at a maximum and every 28 days in December when
insolation was lowest. The average leaf turnover time for these
months was 67 and 140 days, respectively. Rapid leaf growth (x "
1.22 cm per day) of the seagrass Enhalus acoroides was thought to
enhance overall photosynthetic activity in this species (Johnstone,
1979). The photosynthetically useful life of E_. acoroides blades was
determined to be less than 25 days because of excessive fouling.
Thus, it appears that the rapid production of new photosynthetic
tissue had evolved in numerous seagrass species as a means of
counteracting epiphytic loading (Sand-Jensen, 1977; Johns tone, 1979).
Seagrasses, in addition to evolving a rapid growth strategy to
combat fouling, have also evolved chemical defenses. Phenolic
substances which frequently act as growth inhibitors are found in a
number of seagrasses (Zapata and McMillan, 1979). Although leaf
extracts of Posidonia oceanica were found to stimulate the growth of
the bacterium Staphylococcus aureus (Cariello and Zanetti, 1979),
Harrison and Chan (1980) demonstrated growth inhibitory and lethal
effects of extracts from recently dead (a few days to 2 weeks) Zostera
marina leaves on microalgae and bacteria. These effects were
inversely related to the age of the "L_. marina leaves and at 35 and 90
days, antibacterial and antialgal activity, respectively, was
completely lost. Phenols could determine the composition of the
periphyton community by excluding some species of microalgae and
bacteria and inhibiting the growth of others (Harrison and Chan,
1980). Their effects may be greater on the periphyton and encrusting
algae than erect macroalgae because of the intimate association of the
former two groups with the leaf surface. Although to our Knowledge
phenolic substances from seagrasses have not been demonstrated to be
lethal or inhibitory to macroalgae, it would not be surprising to find
that some algal sporelings are adversely affected by these compounds.
-------
Biological interactions between epiphytes and grazers can have a
great impact on the structure and function of both macroalgal and
periphyton associations. Studies on macroalgae colonizing inert
substrates have shown that grazers have a dramatic effect on biomass
and species composition of macroalgal assemblages (Southward, 1964;
Kain and Svedsen, 1969; Dayton, 1971; Lein, 1980). Herbivore-plant
interactions involving microalgal communities indicate that grazing
moHusks can drastically reduce the biomass of intertidal epilithic
diatoms (Castenholz, 1961). Some periphyton grazers maintain
community dominance by tightly adhering diatoms by removing the outer,
loosely adhering portions of the diatom mat (Nicotri, 1977) and others
feed on a mixed diet of two encrusting algal species in a fixed
proportion even over a wide range of availability of the two foods
(Kitting, 1980). Few studies have elucidated the role of epiphyte
grazing in seagrass habitats. These interactions will be discussed
more thoroughly in a la^er section.
d. luplicat ions of Epiphytism for the Seagrass Host
Both beneficial and adverse effects of epiphytes on macrophytes
have been mentioned in the scientific literature. Most are based
primarily on observational information, however, and quantitative data
are generally lacking.
Algal mats are frequently found associated with grass beds in
some parts of the world. These mats, while still attached to
seagrasses, are formed by intertwined algal filaments and create a
canopy over the grass bed. They can have a profound affect on the
associated community (Wood, 1972) under conditions of minimal water
circulation. Due to increased photosynthesis by the algae, the
ambient pH level rises to 9.4 in extreme cases. The bicarbonate ion
becomes limiting at such a high pH and photosynthesis ceases. A c*rop
in pH to less than 7.0 occurs during night time respiration with a
concurrent drop in the redox potential to negative values. Mortality
of some animals occurs and the growth of many plants is limited due to
such fluctuations (Wood, 1972). Algal mats have been shown to have a
limiting effect on the growth of Ruppia maritima and observed to cause
temperature stratification in the water column due to shading
(Richardson, 1980). Such stratification can postpone flowering,
fruiting and seed production in Jl. maritima. If shading by algal mats
is severe, active photosynthesis is restricted to the upper layer of
the water column. As a result of thermal stratification also due to
shading, the photosynthetically oxygenated water does not reach the
lower portions of the water column. Because of the high oxygen demand
of the benthos, and night time plant respiration, anaerobiasis occurs
below the upper stratum (Richardson, 1980) in a manner similar to that
reported by Wood (1972). Grass beds exhibiting such extreme
characteristics are associated with environments having little water
circulation. The instability of conditions associated with Si-ch
systems results in generally depressed levels of abundance and
diversity of the associated fauna. When the macroalgal mats detach
from the host plants and float off of the grass beds, stressful
55
-------
conditions are alleviated and resistant plants and animals are once
again able to flourish.
Algal epiphytes can have more subtle yet equally important
effects on marine phanerogams. Breakage of leaf tips, heavily
encrusted by calcareous algal epiphytes, has been reported to occur in
Thalassia testudinum. This is primarily caused by leaf decay beneath
epiphytes and is a characteristic feature of T_. testudinum beds at
Barbados (Patriquin, 1972). Similar encrustations occur on T_.
testudinum in Florida Bay (Ginsburg and Lowenstarn, 1958; Humm, 1964)
and serpulid worms, in addition to calcareous algae, are commonly
found in Jamaica growing on the blades of T_. testudinum (Land, 1970).
Both calcareous red algae (generally melobesoids) and serpullid worms
have a similar detrimental effect on the macrophyte host as that
reported by Patriquin (1972). Upon death, these carbonate-secreting
organisms can contribute significantly to the carbonate sediments of
Z- Cestudinum beds (Land, 1970; Patriquin, 1972). The depositional
environments of grass beds is well documented (Daetwyler and Kid well,
1959; Guilcher, 1965; Scoffin, 1970; Burrell and Schubel, 1977) and a
portion of this phenomenon is directly attributable to the presence of
a multitude of epiphytes which not only produce carbonate sediments
upon their death but also trap fine suspended sediments that are
subsequently added to those of the grass bed (Gin'bur and Lowenstam,
1958; Swinchatt, 1965; Scoffin, 1970; Taylor and Lewis, 1970).
More severe effects of epiphyte fouling are attributed to shading
of the macrophyte host. In New Guinea, fouling of Enhalus acoroides
by epiflora and epifauna occurs rapidly and new growth of leaf tissue
is no longer visible through the mass of colonists after only 10, and
occasionally up to 25, days (Johnstone, 1979). Such shading can
' severely reduce the amount of light when reaches the host. Taylor and
Lewis (1970) studied six species of marine angiosperms of the
Seychelles Archipelago and reported that "there is often such a thick
coating of epiphytes on the grass leaves that they appear to be
covered by a thick brown fur. They render so much of the
photosynthetic surface of the plaits non-functional that the growth of
the angiosperms must be affected." Borum and Wium-Andersen (1980)
determined that epiphyte biomass increased exponentially from the
youngest leaf of Z_. marina to the oldest leaf and that on any single
blade a similar increase occurred from the basal (or youngest) portion
to the tip or oldest part of the blade. Furthermore, they
demonstrated that less than 102 of the incoming light was transmitted
through the dense epiphyte cover growing on the oldest blade tips of
Zostera marina. In contrast, more than 90X of the ambient light was
available for photosynthesis to the lightly epiphytized basal portions
of the blades. Since the wavelength of light absorbed by the
periphyton growing on Z_. marina is virtually identical to that
utilized by the host (Fig. ,2), the amount of usable light reaching the
Z. marina blade can be severely reduced by periphyton fouling (Caine,
7980K
56
-------
13
nj
M TJ T3
> CO -<
t- .0
3 K
o j: «j
*•* c
o/ oc VH
£ C k.
*J 0; CO
H_ o
o > •
« N:
E •-•
•H i- j:
Bl IB O
I
0
o
1 1
o
If)
1
y
/\
i
O
-o
-8
«0
(9
O >
•O
SNVH1 %
c
•s.
c
c/
•^ 1C
TJ
o re
O 1-1
re kp
k< re
><
tr, —<
N: I o
= i
"O *J
N|g §
O
C C E
c z n
oc
c .
01
£
O U VI
w-
C
01
OC D. U
3
.r -X3
cue
^1 00
c o-
t- O —
a *j
c a c
O er —! i-
«j u kp re
£ ra a.
a u E
— : ex.
TJ
c
ri
01
3
-------
The effects of epiphytes on eelgrasa (Zostera marina)
photosynthesis has been further documented by Sand-Jensen (1977). He
found that diatoms, primarily Cocconeis scutellum, formed a crust over
the leaves of "L. marina and considerably reduced photosynthesis by
both limiting the available light and acting as a barrier to carbon
uptake. Photosynthesis was reduced 312 by epiphytes under optimal
light conditions and ambient (about 1.7 meg-l~M HCC>3~ concentrations
(Fig. 3). Beer et al. (1977) demonstrated that HC03~ is the rajor
carbon source for photosynthesis in seagrasses and that uptake occurs
readily across the leaf surface. The diffusion of HCC>3~ was depressed
by the epiphyte crust causing reduced photosynthesis (Fig. 4) at
varying HCOi" concentrations and a constant light intensity of
14.7 mW-cnT^ (Sand-Jensen, 1977). Light attenuation experiments using
shades have confirmed the impact of reduced light on seagrass growth.
Backman and Barilotti (1976) reduced dovmwtlling illumination over
Zostera marina by 632 and found a significant reduction in numbers of
both vegetative and flowering shoots. Similar shading experiments
have shown that production of Ruppia mar it ima is substantially reduced
by decreased illumination. Light reductions of 802 or more for 100
days completely precluded JJ. maritima and light reductions of 202 for
250 days significantly decreased its biomass (Congdon and McCorab,
1979). Heavy epiphytic loading was attributed to the cause for
earlier dieback and lower production estimates in one Ruppia cirrhosa
bed than that found for an adjacent epiphyte free stand of JR. cirrhosa
(Kirfrbe, 1980a). Furthermore, it is thought that light most likely
controls the lower depth distribution of marine macrophytes
(Burkholder and Doheny, 1968; Phillips, 1972; Thayer et al. 1975;
Jacobs, 1979; Mukai et al. 1980). Since epiphytes diminish the amount
of light reaching the macrophyte, they may partially and indirectly
influence plant distribution, biomass, productivity, and both asexual
and sexual reproductive capability.
II. THE TRO°HtC ROLE OF PERIPHYTON IN SEAGRASS BEDS
It is well known that the direct consumption of seagrasses by
marine organisms is minimal (<52 of the total production) and that
most of the carbon fixed by marine angiosperms is transferred to
higher trophic levels via a detrital pathway (Fenchel, 1977; Klug,
1980; and references contained therein). However, some macrophyte
carbon can be transferred indirectly through the ingestion of
periphyton which, as discussed earlier, assimilates some of its carbon
from DOC released by the host macrophyte (Thayer et al., 1978).
Furthermore, the highly productive diatom and bacterial component of
the periphyton is responsible for a considerable percentage of Che
production of grass bed ecosystems. On a per unit area basis,
epiphytes contribute an average of from 182 (Penhale, 1977) to 502
(Borum and Wium-Andersen, 1980) of the combined Zostera marina leaf
and epiphyte production and 222 of the production in a Thalassia
testudinum bed (Jones, 1969). This production is available for
consumption by the numerous grazers found in seagrass habitats.
58
-------
"D 01
C <•>
E
u
x-» (0
0> V
C hi
•rt ft.
.-. 0)
hi
0, ID
JC 3
O -H
hi ra
^ >
' SI
• u
<~> «J
U
B!
4/
e. •*
•*-! en
c. C
& &)
X C
» 4J £*
' ol r-
t; T-I o-.
e "o c
C K
c c
3 C
>»-. tr
o m
>- a) c
^ (C hi
O «-
M —. /^ ^
_. OJ
* -o e tn
E i- *
x. c.
-i it
e, — tn
/: o
*-* tr. h>
3
*— • C
O C «-
VI V-
•" tn •
(T O/
t u x-,
X > UJ
<-« X 0-.
C Q.
C
H 'S "5
01
U
3
Of
-------
•O
C
ll
C
0)
w
O 3
o *->
- .c
.O O &
« .C
tf! C
41 C
O
o
X
<-• x;
c. c
4, 4,
C ^
m t-.
I X 6lU X
I-
sisagtuAsotOMd }031
S-
4J
••H
3
flj
C
M-H
t*
i
s
Ul
o
4-1
C
JC
CL
C
O
o
1
r^i
C
|^-
•~
C
c
c
M-l
4-1
u
c
3
re
K
ra
^^
&-
c
..^
1— • 1
T)
•t^
^^
O
o;
*
c
s_^
tr.
0.
>
£
a
a
41
4-<
3
C
*-*
IT.
C
C
o
c
c
*r+
t-t
n
u
^
*-j
(B
w;
U-.
t— •
^
*c
a>
-C
H
.
W
5^
*-^
c.
E
TO
cr.
k.
3
C
u-
u-
O
U^
t/3
+_!
c
<0
4<
E
r^
er
^«
»
c
a.
x
c
^!
r
•o
c
re
in
E
C
V.
s^-
rsj
'E
O
^
i —
•
-*
-^
»
>
4^
•(-<
(f.
C
4/
4J
C
AJ
X
6C
f-t
_1
C
Of
-
-------
Although the productivity of the periphyton in seagrass habitats
appears to be substantial, few quantitative data on the utilization
and importance of this food resource are available. For limnetic
environments, the trophic importance and ecological relationships of
the periphyton are somewhat better understood (see Hutchinson, 1975,
for i^view). Brook (1952, 1955) brought to light the substan'.ial
impact of grazers on aquatic filamentous algae and diatoms growing
both on inert substrates and macrophytes of freshwater systems. The
nutritional value of periphyton based on carbon to nitrogen ratios was
substantially higher than that of freshwater macrophytes. In marine
and estnarine habitats, studies on the trophic dynamics of the
meiofauna indicated that diatoms in a salt marsh aufwuchs (=
periphyton) community were important food for numerous protozoans (Lee
et al., 1966; Lipps and Valentine, 1970; Lee et al., 1975a, b).
Certain species of diatoms, chlorophytes and bacteria constituted the
bulk of material eaten by foraminiferans and could apparently be
selectively grazed from among numerous other species present in the
periphyton (Lee et al., 1973). Some species such as the harpacticoid
copepod Nitocra typica feed on periphyton and were shown to have very
complex nutritional requirements depending on and influencing N_.
typica's different life cycle stages (Lee et al., 1976). Similar
importance of diatoms and bacteria in the feeding behavior of marine
nematodes was demonstrated by Tietjen and Lee (1977). Comparable
studies in seagrass habitats are limited although the nutritional role
of the periphyton is probably similar.
Numerous authors mention the importance of the periphyton as a
food source to resident consumers in grass beds (Wood, 1959; Marsh,
1973; Brasier, 1975; Kikuchi and Perez, 1977; Harlin, 1980; Ogden,
1980). One of the dominant groups of the epifaunal community in many
vegetated habitats are gastropod mollusks (Marsh, 1973). Taylor and
Lewis (1970) estimated that the prosobranch molluscan fauna associated
with a Thalassia hemprichii bed is primarily epifaunal and, of these,
approximately 30X were composed of algal feeders which rely primarily
on the microepiphytes that coat the blades of T_. hemprichii. However,
no quantitative data were presented to support their contention.
Kikuchi and Perez (1977) mentioned that the primary dietary component
of the sea hare, Aplysia sp., was the epiphytic algae associated with
seagrass blades. Stomach content analyses of the large and
economically important tropical gastropod Strombus gigas revealed that
this species also relied primarily on epiphytic algae found growing on
the blades of Thalassia testudinum although it also ingested algae and
some macrophyte 'tissue (Randall, 1964). A similar role in T_.
testudinum and Halodule wrightii beds is played by the small
prosobranch Modulus modulus which is commonly encountered in tropical
Atlantic vegetated habitats. M. modulus feeds primarily on epiphytic
algae and accumulated detritus of marine macrophytes and, through its
grazing activity, it may also dislodge newly settled larvae of otner
epifaunal organisms thereby reducing the overall fouling on graas
blades (Mook, 1977). Bittium varium, the small, dominant epifaunal
gastropod of Chesapeake Bay Zostera marina beds (Marsh, 1976), can
reduce periphyton weight (g'dry wt per cnr) on polypropylene ribbon
-------
resembling "L_. marina by a factor of almost 63% (van Montfrans et al.,
in press). Scanning electron micrographs of IJ. varium feeding trails
revealed that in some instances removal of the periphyton crust was
complete (Fig. 5), although in other cases feeding appeared to be
mechanically selective for the upper layers of the periphyton crust
leaving behind the loosely attached bacteria which were too small to
be removed and the more tightly adhering diatom Cocconeis scute Hum
(Fig. 6). The importance of diatoms in the diet of both Bittium
alternatum, a sympatric congener of _B. varium in the Chesapeake Bay,
and the mud snail Nassarius obsoletus was illustrated by Lee et al.
(1975c) who showed that together these snails ingest about 10' algal
cells per day. Another species of gastropod, Littorina saxatalis, is
abundant in "L_. marina meadows along the coast of Nova Ccotia. This
species was found to inhabit live vegetation during the warmer months
from March to November and to rely primarily on periphyton as its food
source (Robertson, 1981). The population dynamics of L_. saxatalis
were closely linked to the limited food supply (i.e. periphyton)
growing on Z. marina leaves and intraspecific competition for this
resource was shown to be responsible for post recruitment mortalities.
The role of micro- and macroepiphytes in the trophic dynamics of
crustaceans has also been demonstrated to a limited degree. Brawley
and Adey (1981) showed that amphipod grazing had a substantial effect
on the biomass of microalgae in a coral reef microcosm. They also
demonstrated the effect of grazing in changing the community structure
of algal species present. Amphipods are a particularly diverse
component of seagrass habitats (Marsh, 1973; Nelson, 1980). As a
group they exhibit varied feeding habits including both macrophagy and
microphagy of algae associated with the macrophytes and seagrass
detritus (Zimmerman et »l., 1977). Resource partitioning studies of
four amphipods species inhabiting Thalassia testudinum and Halodule
wrightii beds in the Indian River region of Florida showed that
between 29 and 66% of the food ingested by all four species was
composed of microepiphytes and between 2 and 35% was made up of
macroalgae (Zimmerman et al., 1979). High assimilation efficiencies
of carbon-14 labeled microalgae further emphasized the relative
importance of microepiphytes in the diet of these amphipods. The
importance of microalgae in the diet of the caprellid amphipod,
Caprella laeviuscula, was illustrated by Caine (1980). This species
scrapes periphyton from the blades of £. marina (Caine, 1979).
Laboratory grazing experiments have shown that control blades of Z^.
marina without Caprella laeviuscula had over four times the periphyton
biomass than those upon which C_. laeviuscula was allowed to graze
(Caine, 1980). Although no nutritional data were presented, C_.
laeviuscula appears to depend heavily on the presence of periphyton as
a food source. A decapod crustacean, Palaemonetes pugio, was shown to
voraciously consume epiphytes attached to Halodule wrightii rather
than the grass itself (Morgan, 1980). Epiphytes constituted an
important part of the diet in P_. pugio although larger shrimp (>19 mm)
preferred rays ids as a food source when present. Microepiphytes were
assimilated at rather high mean efficiencies of 83X by P_. pugio.
Species of Palaemonetes are among the most numerous components of the
-------
63
-------
01
5 c,
M
U-< O
O 43
01
o
E en u
o) E cj
v- o o
•u u
01 CO
01
•H C
3 i-l
O
43 i-l B 4J
4J TJ O
oo cu
e <->
-H CO
§g
.c 01
co a.
CO
e
•H
14
C
CO
w
01
4J
tn
o
ts]
b
01
•o
c
01
<— i
CO
cu
4=
4-1
M-l
O
c »•>
O 4J
•H
45 V"
U 0
*J i-l
4J
CO
•H
•o
CU
4=
E-
•O
a>
3
CO
c
o
u
01
i-i
ii
3
4J
CO
3
V4
y
14-1
O
I4H
i— 1
at
Si
M
01
I
r-t
01
.c
4-1
CO
CO
JZ
•1
•H
i— 1
01
£
4J
CO
.<:
o
«
*
^1 X-N
O CN
cn
CO
4J
e
CD
•o
•H
>
01
cn
•H
e
•3
f— t
iH
01
4J
3
U
CO
oo
c*
*«l
•
i-H
CO
4J
01
cn
C
CO
1-
U-l
1-1
c
s
c
CO
•H >
•a oi 4J
cu j= at
N H >•<
14-1 VJ 1-1 ft
o u o u
ax
£ C M
a o wi 1-1
CO 4J 01 4J
^ x a
ocj= a ca
o ex. 3 *
|J 1-1 V4
u i-i « 01
•H ai j= J=
E a 4J -a
CO
C 0) C
o
i-H M
CO /-»
oi e
CD a
o o
4J O
a*
oo n
co
e ^
CO CO
•a ^i
C i-l
o ca
M 4-1 U i-l X
4J /-s -H -O O
U <4* CO
01 O i-l
fl X
CU M-l O
t-4 0)
etc co N
C J= 4J
•H 1-1
C h Z
j= •« o
» < cn
\^
*
g
p
i— i
iH
01
CO) 4J
co at} 3
u o. e u
co s co co
• CO
•a cu
CD tH
£ 3
y 4J
CO CO
4J 3
U P
CO "4-1
\o
01
Id
s>
64
-------
vagile epifauna in seagrass beds of the northeastern U.S. coast (Heck
and Orth, 1980). These species and ecological equivalents in other
parts of the world could play a role similar to that of P_. pugio in
other seagrass habitats.
A third major group of organisms which occur epifaunally on
seagrasses are polychaetes. Because of their generally high
fecundity, polychaetes exhibit seasonal pulses of abundances in
temperate and cold water areas. Little is known about their diets,
however, although a recent interest in polychaete feeding habits is
evident in tho literature (Fauchald and Jumars, 1979). To our
knowledge, there is no information on the utilization of seagrass
periphyton by polychaetes. It seems likely, however, that species
which exhibit a surface deposit feeding mode could ingest some
periphyton.
Some fish have been shown to directly ingest microscopic algae
(Hiatt, »944; Wood, 1959; Bell et al., 1978). A detailed study oi
leather jackets (Class: Pisces, Family: Monacanthidae) in an
Australian estuary showed that although large amounts of seagrasses
were ingested, the fish were highly dependent on the encrusting fauna
and epiphytic algae for their nutrition (Bell et al., 1978). Wood
(1959) further emphasized the role of direct grazing on epiphytes by
phytophagous fish and suggested that seasonal variation in the weight
of epiphytes on Zostera capricorni might partially be influenced by
the extent of fish movements and seasonal food preferences.
The exact amount of periphyton carbon produced by and later
removed from grass bed habitats is poorly understood but it appears
that it is an important component of energy flow patterns in seagrass
ecosystems. The trophic importance of mollusks, crustaceans and
polychaetes is well established in the literature although a thorough
review is beyond the scope of this paper. It is generally thought
that predation, which can be mediated by grass density, is an
important structuring force in determining the composition of the
epifaunal community associated with seagrasses (Kikuchi, 1974; Young
and Young, 1978; Conacher et al., 1979; Nelson, 1979a, b; Stoner,
197'', 1980; Wilkins, pers. comm.). By feeding heavily on epifaunal
organisms, many of which are periphyton grszers, predators such as
fish, crabs, and birds cycle carbon fixed by the periphyton to higher
trophic levels. Trophic relationships in a west Florida mixed bed of
vegetation indicated that peracaridan crustaceans and polychaetes were
the main sources for energy transferred from primary consumer levels
to higher trophic levels (Carr and Adams, 1973). Similar trophic
links were found in a southeastern Florida Thalasia testudinum bed
(Brook, 1977) and based on a study of the feeding ecology of a Zostera
marina fish community, 56% of the diet by weight of food items such as
eelgrass, crustaceans, gastropods, and detritus originated in grass
beds (Adams, 1976).
Benthic pelagic coupling was demonstrated during a study of
seagrass habitats in Australia. Robertson and Howard (1978) found
-------
that benthic amphipods and ostracods exhibited vertical migration into
the water column at night and were therefore actually facultative
zooplankters. These amphipods and ostracods were heavily preyed upon
by midwater planktivorous fish when nocturnal switching in prey
selection occurred in response to the abundance of facultative
zooplankters. Thus, numerous invertebrates in grass beds, many of
which are grazers, provide links with species in higher trophic
levels.
III. PERIPHYTON GRAZING: CONSEQUENCES FOR THE MICROPHYTE HOST
The secondary effect', of periphyton grazing in iriergy flow and
nutrient cycling patterns of vegetated habitats is virtually unknown.
Obviously, much of the material ingested by periphyton grazers
enhances detrital pathways and recycles nutrients through the
production of feces. A more subtle consequence of grazing, however,
may be seen in the macrophyte host's response to the removal of the
periphyton crust. Few studies have addressed this concept with a
quantitative approach although several inferences can be made from
published literature regarding the positive effects of such grazing
activities.
During an extensive study of Ruppia maritima in New Hampshire
tidal marshes, Richardson (1980) observed that, "numerous small snails
of the genus Hydrobia were seen grazing the epibiota present on Ruppia
plants under the algal mats to the extent that the plants were nearly
free of epibiota throughout most of the season." These plants were
considered to be healthy and vigorous. Mook (1977) observed reduced
fouling of tiles due to the grazing activities of Modulus modulus, a
gastropod which is common in tropical Atlantic grass beds. He
suggested that the presence of the snail minimizes fouling on seagrass
blades although he did not emphasize the significance of such activity
in terms of host plant responses. Similarly, Robertson (1981) showed
by grazer exclusion experiments that the snail Litforina saxatilis
controlled the amount of periphyton on Zostera marina leaves. Several
authors have discussed the implications of grazing on periphyton for
the macrophyte host by removing this barrier to light, van Montfrans
et al. (in press) suggested that loss of the dominant periphyton
grazer, Bittium varium, a prosobranch gastropod, from Zostera marina
beds in the Chesapeake Bay, USA, may have had important implications
for the recent decline of £. marina in the Bay (Orth and Moore,
1981a, b). Caine (1980) stated that the presence of the caprellid
amphipod Caprella laeviuscula "allowed £. marina to grow in areas
where it would otherwise have been excluded by periphyton." In
experimental tanks with the seagrass Heterozostera tasmanica, Howard
(in press) showed that the presence of gammaridean amphipods had a
significant impact on epiphytic fouling compared to tanks without the
amphipods. He suggested that the secondary effects of grazing
ultimately influenced macrophyte productivity and energy flow pathways
in seagrass habitats. We have further experimental evidence that
transplanted plugs of Z_. marina produced a significantly greater
number of new shoots, had a greater leaf biomass and leaf area index
66
-------
and were less fouled by periphyton when the grazer J5. varium was
present than did control plugs in the absence of graz°rs (unpublished
data). Thus, it seems very likely that periphyton grazers, when
present, can have a substantial, though indirect, impact on the
proliferation, biomass and reproductive potential and, possibly, the
persistence of seagrasses.
We recommend that researchers be critically aware of the indirect
influence of periphyton grazers on seagrass productivity. Comparisons
of productivity measurements betuaen both local grass beds and those
separated latitudinally must consider biological interactions that
influence primary production as well as abiotic variables. Reported
causes for spatial and temporal differences in seagrass productivity
due to insolation, temperature, and nutrients may be only partially
valid if those systems harbor dense assemblages of periphyton grazers.
We have developed a very simplified model that attempts to place
the role of periphyton grazers into their functional perspective. We
have generated a series of hypotheses based on this model that will
ultimately have predictive value when considering the effect of
increased fouling on seagrass productivity and the role that
periphyton grazers play in influencing this relationship.
In our model we assume that species of seagrasses occur from very
shallow water where light is never limiting to deeper areas where
light levels are so low that phanerogams are only minimally sustained.
Under these conditions there will generally be a decrease in seagrass
productivity as periphyton production (i.e. fouling) increases.
Seagrass production relative to the degree of epiphytic fouling may
vary somewhat with depth (i.e. light).
Under light saturated conditions and when photoinhibition does
not occur, seagrass production varies with the degree of epiphytic
fouling as depicted in Fig. 7. Initially, seagrass production would
be minimally affected by fouling since the plants receive adequate
light to achieve high primary production. However, as epiphytic
fouling increases, seagrass productivity declines more rapidly because
of diminished light levels. Ultimately, fouling would cause net
seagrass productivity to be negative and the' plants would die. The
presence of grazers in this situation would shift the seagrass
production curve to the right by removing the light barrier. Thus, at
a particular level of epiphytic fouling (point a), the same seagrass
habitat would exhibit higher levels of primary production when grazers
are present (point b) than in the absence of grazers (point c).
Conversely, two seagrass beds having the same level of primary
productivity (points d and e) may be similar in this regard primarily
because one experiences greater fouling (point a) than the other
(point f). These relationships may be important in systems receiving
moderate nutrient enrichment. Fouling by epiphytic algae in such
systems would increase and without grazers to keep fouling in check,
the macrophytes would experience death due to light reduction below
the compensation point.
67
-------
CO
CO
- C T
x: o c
O 4J >
•«' >- C
a j=
01 o •-
•H f
14- ^ E
O Oi i-
a >
Ui C
u O
Ol k
01
01
>
^ a
u-
O Oi a
u c
«-• e c
O> Ol f
•O 03 4.
O JQ T
E « t
« C t.
o n
•rt T
Ol
O
a
OllAHdld3 JO 33d93Q
3
bf
-------
.x
- -/
• .s. -
One aspect of seagrass-fouling relationships not depicted in our
model concerns the beneficial effects of epiphyte cover under certain
circumstances. Plants which grow in shallow water or are very
sensitive to high light: levels may be subject to photoinhibition.
Som may also experience desiccation if exposed at low tide. In these
situations, epiphytic fouling may actually be responsible for or at
least enhance the productivity of the seagrass. Removal of this
protective crust by grazing would result in reduced seagrass
productivity due to photoinhibitory effects and also increase the
susceptibility to desiccation. Of course, extremely dense growths of
attached algae and fouling organisms would have similar effects as
those already discussed.
We recognize that our hypothetical model represents an
oversimplification of a complex system. Any number of factors, acting
independently or synergistically, may affect seagrass productivity.
The timing of epiphyte fouling in relation to seagrass production
and/or life history stage, interference of chemical diffusion across
the leaf surface caused by periphyton, the effects of light reduction
due to phytoplankton and periphyton, the ability of a seagrass to
rapidly regenerate new photosynthetic tissue and slough off
epiphytized leaves, differences in light requirements of individual
seagrass species, and the density of periphyton grazers, all either
indirectly or directly affect seagrass productivity. However, the
actual quantity and quality of light reaching the plant surface will
be the ultimate factor affecting the survival of an established
seagrass species. Therefore, periphyton grazers may represent a very
important interactive element in affecting light penetration to the
leaf surface in those areas where they are abundant.
Based on the relationships depicted in our model, we can make
some predictions on the effect of environmental perturbations which
diminish the light reaching the plant surface. Light reductions
resulting from greater fouling, increased suspended particulates in
the water column, or a reduction of periphyton grazers will cause a
decline of seagrasses along a depth gradient with reductions occurring
first in deepest areas and progressing inshore depending on the amount
of light reduction. We also predict that the horizontal distribution
of seagrasses along an estuarine turbidity gradient will shift away
from areas of greatest turbidity. Furthermore, these shifts will not
be as pronounced in seagrass systems with a large component of
periphyton grazers.
IV. EFFECTS OF NUTRIENT ENRICHMENT ON MACROPHYTES
The nutrient composition of estuaries varies considerably from
one system to another depending on numerous factors, including the
type of estuary, the amount of freshwater discharge into the estuary,
geological and geochemical characteristics of each drainage basin,
storm events, biological uptake of nutrients and anthropogenic inputs
(Briggs and Cronin, 1981). In most estuaries, nitrogen is commonly
the most limiting nutrient (Nixon, 1981) and changes in nutrient
69
-------
composition from anthropogenic sources are known to have numerous
effects. However, very little is known about the consequences of such
changes on macrophyte distribution and abundance. The proceedings of
a recent international symposium on the effects of nutrient enrichment
in estuaries (Neilson and Cronin, eds., 1981) included 33 papers, none
of which addressed the effects of eutrophication on submerged
angiosperms. Liranologists have a better understanding of such effects
and although the nutrient kinetics in estuaries may be more complex
than in lakes, some insight into eutrophication-macrophyte
relationships might be derived from examining the freshwater
literature .
During a study of progressive nutrient enrichment in Norfolk
Broads, a series of lakes in England, Phillips et al. (1978)
formulated an hypothesis to explain the disappearance of dense
macrophyte stands. It was postulated that epiphytic algae (mainly
diatoms) were initially favored by the eutrophication process and
responded by increased proliferation. As a consequence,
macrophyte-epiphyte complexes ultimately declined and were replaced by
phytoplankton populations. Thus, shading by epiphytes due to
progressive eutrophication appeared to be the causative agent in
macrophyte declines and phytoplankton increases were a subsequent
development. This hypothesis was further substantiated by Moss (1979)
whose study of two centuries of diatom records from the sediment in
one of the lakes confirmed that epiphytic diatoms reached very high
abundances over time and then began to disappear as fouling caused the
demise of the host substrate. Subsequently, sediment cores showed an
increase in planktonic diatoms which persisted to the present. This
sequence of events might be predicted based on previous research.
Hasler and Jones (1949) demonstrated that aquatic macrophytes had a
growth inhibiting effect on microalgae (i.e. epiphytes and
phytoplankton) but based on Fitzgerald's (1969) work this was shown to
be the case only when nutrients were limiting. Fitzgerald (1969)
demonstrated that under nutrient limited conditions the filamentous
green algae Cladophora sp. remained relatively free of epiphytes but
when surplus nitrogen was available, excessive epiphytic fouling
occurred. Additional evidence from freshwater studies indicated that
nutrient enrichment influences community composition of periphytic
diatoms (Eminson and Moss, 1980). When nutrients in the external
environment are limiting, macrophytes exert a chemical influence on
colonizing diatoms causing a host specific relationship. Under more
fertile conditions, host specificity breaks down and all periphytic
/ communities are alike in composition. This is accomplished by
'' favoring faster growing diatom species which, unlike slow growing
; diatoms, which are adapted for uptake of nutrieats at low
concentrations under infertile conditions (Moss, 1973; Eminson and
Moss, 1980;), are more chemically dependent on open water for their
nutrients (Eminson and Moss, 1980).
j
Similar relationships in estuaries have not been demonstrated
t although it is very likely that the periphyton community as well as
'' plankton populations rather than macrophytes are favored by
f
70
-------
anthropogenic nutrients. Marine raacrophytes derive most of their
nutrition from the soil in which they grow and thus incorporation of
nutrients into the sediments would be a prerequisite for enhanced
macrophyte growth. Epiphytes and phytoplankton, on the other hand,
respond more immediately to nutrient enrichment by dissolved
nutrients. Consequences of such responses in estuaries would be the
same as in freshwaters, ultimately reducing the light available to
macrophytes thereby causing their demise.
Numerous studies in the marine environment have documented
changes in macroalgal community composition due to eutrophication.
Generally, increased nutrients disrupt the competitive balance between
perennial algae such as fucoids and ephemeral green algae by favoring
the latter (Bokn and Lain, 1978). Low production of macrophytes has
been attributed to urbanization although the exact mechanism for this
phenomenon was not discussed (West and Larkum, 1979). Macroalgae
epiphytic on Zostera marina were favored by eutrophication which
caused an increase in both the growth and numbers of individuals on
the host plants (Larkum, 1976). These responses were shown to
ultimately cause the disappearance of the grass beds in the polluted
portion of the estuary. Larkum (1976) also pointed out that once
degeneration of seagrasses is begun, the processes become
autocatylitic as the sediment binding and water clarifying
characteristics of the habitat are destroyed.
In a more detailed study, Posidonia spinosa was shown smothered
by dense epiphytic fouling caused by eutrophication. Transplants of
healthy Posidonia shoots from unpolluted to polluted areas resulted in
rapid fouling by algae causing death while similar transplants into
unpolluted waters remained healthy (Cambridge, 1979). It was
concluded that the major effect of eutrophication on macrophytes was
indirect by enhancing epiphyte growth and plankton biomass, thereby
reducing available light. Cambridge (1979) further discussed the
implications of particulate matter in the water column to macrophytes.
She stated that, "If particles are suspended through the water column,
the seagrass meadow will contract vertically, as plants die at the
deeper limit. However, if particles such as silt or algae coat the
leaves consistently over a time, then plants are likely to die
throughout the depth range depending more on the density of the
coating than the incident light intensity." Thus, epiphytic fouling
and the accumulation of material on seagrass leaves can be enhanced by
increased nutrients and ultimately cause the destruction of the host
plant.
In sstuarine systems which are becoming increasingly enriched
with nutrients, not only epiphytic fouling but also phytoplankton
production would increase. This would result in more light stress on
the seagrasses and, eventually, if severe enough, would totally
eliminate the plants. If periphyton grazers of seagrass habitats
decline in abundance while periphyton and/or phytoplankton populations
increase, seagrass productivity may decline even more rapidly than in
systems where periphyton grazing is not important. Unfortunately, a
71
-------
complete understanding of many of these complex interactions are still
undetermined and await future research by the scientific community.
V. MANAGEMENT IMPLICATIONS
Seagrasses are natural resources which by serving multiple
functional roles substantially increases coastal zone productivity.
The value of submerged vegetation can be expressed in ecological
(productivity, habitat complexity), aesthetic (bird watching),
recreational (hunting, fishing, crabbing) or economical terms
(contributions to a commercial fisheiy) and when compared to that of
nonvegetated habitats the value of grassbeds is considerably higher.
Human activities such as industrialization, development of
coastal areas because of recreational appeal, agricultural land usage
and dredge and fill operations are increasing in many parts of the
world. Such activities have lead to well documented declines of
seagrass beds in both temperate and tropical areas (Taylor and
Saloman, 1968; Maggi, 1973; Cambridge, 1975, 1979; Peres and Picard,
1975; Zieman, 1975, Larkum, 1976).
Natural perturbations such as hurricanes, diseases, overgrazing
and the rapid encroachment of sand waves can also be responsible for
seagrass declines although they do not seem to be as widespread as
man-induced changes (Cottam, 1934; Cottam and Munro, 1954; Camp
et al., 1973; Patriquin, 1975; Zieman, 1976; Kirkman, 1978).
Two of the major results of human activities that appear to be
correlated with seagrass declines are to decrease water transparency
t and to increase nutrients, thereby enhancing epiphytic growth.
. Although examples of causal factors from detailed field and laboratory
experiments are few, there is a growing body of information that
t focuses on nutrient enrichment of coastal waters (Neilson and Cronin,
• 1981). Since numerous undesirable effects of eutrophication such as
red tide outbreak, the production of noxious odors, and the occurrence
of fish kills caused by lowered dissolved oxygen levels have been
documented in addition to declines of seagrasses, emphasis is being
placed on reducing both point and nunpoint sources of pollution with a
t goal towards improving land management practices.
f
I Managers face a difficult task in striking a balance between
•. recreational, industrial, agricultural and ecological uses of a
{ watershed. When making ecologically related decisions land managers
[ must be fully aware of the complexities and natural variations that
occur within a particular ecosystem and how these factors might be
influenced by human induced perturbations. Reducing nutrient loading
in coastal areas may be exceedingly difficult, if not impossible,
particularly if management strategies require exorbitant funding.
However, when the overall contribution to the economy of an area by
valuable habitats such as beds of submerged vegetation is assessed,
the alternatives to inadequate management may be more economically
desirable overall. Adoption of good land use practices to reduce or
72
-------
eliminate nutrients in the watershed as well as strict enforcement of
these procedures may ultimately be the most desirable choice of
alternatives for the economy and welfare of future generations.
73
-------
I
LITERATURE CITED
Adams, S.M. , 1976. Feeding ecology of eelgrass fish communities.
Transactions of the American fisheries Society, '05(4): 514-519.
Backman, T.W. and Barilotti, D.C., 1976. Irradiance reduction:
effects on standing crops of the eelgrass Zostera marina in a
coastal lagoon. Marine Biology, 34: 33-40~
Bell, J.D., Burchmore, J.J. and Pollard, D.A. , l';»78. Feeding ecology
ot three sympatric species of leather jackets (Pisces:
Monacanthidae) from a Posidonia seagrass habitat in New South
Wales. Australian Journal of Marine and Freshwater Research, 29:
631-643.
Beer, S. , Eshel, A. and Waisel , Y., 1977. Carbon metabolism in
seagrasses. I. The utilization of exogenous inorganic carbon
species in photosynthesis. Journal of Experimental Botany, 28:
1180-1189.
Biggs, R.B. and Cronin, L.E., 1981. Special characteristics of
estuaries. In: B.J. Neil son and L.E. Cronin (Editors),
Estuaries and Nutrients. Humana Prfss, Clifton, New Jersey, pp.
3-23.
Bokn, T. and Lein, T.E., 1978. Long-term changes in fucoid
a«sociation of the inner Oslofjord, Norway. Norwegian Journal of
Hocany, 25(1): 9-14.
?orom, J. and Wiura-Anderson , S. , 1980. Biomass and production of
epiphytes on eelgrass (Zostera marina L.) in the 0resund,
Denmark. Ophelia, Supplement, 1: 57-64.
Brasier, M.D., 1975. An outline of seagrass communities.
Paleontology, 18: 681-702.
Brawley, S.H. and Adey, W.H., 1981. The effect of micrograzers on
algal conmunity structure in a coral reef microcosm. Marine
Biology, 61: 167-177.
Brook, A. J., 1952. Some observations on the feeding of protozoa on
freshwater algae. Hydrobiologia, 4: 281-293.
Brook, A. J., 1955. The aquatic fauna as an ecological factor in
studies of the occurrence of freshwater algae. Revue
Algologique, 3: 141-145.
74
-------
Brook, I.M., 1977. Trophic relationships in a seagrass community
(Thalassia testudinum), in Card Sound, Florida. Fish diets in
relation to macrobenthic and cryptic faunal abundance.
Transactions of the American Fisheries Society, 106(3): 219-229.
Brown, C.L., 1962. On the ecology of aufwuchs of Zostera marina in
Charles town Pond, Rhode Island. M.S. Thesis, Univ. of Rhode
Island, 52 pp.
Brylinsky, M., 1977. Release of dissolved organic matter by some
marine macrophytes. Marine Biology, 39: 213-220.
Burkholder, P.R. and Doheny, T.E., 1968. The Biology of Eelgrass.
Lamont Geol. Observatory, Contribution 1227, 120 pp.
Burrell, D.C. and Schubel, J.R., 1977. Seagrass ecosystem
oceanography. In: C.P. McRoy and C. Helfferich (Editors),
Seagrass Ecosystems, A Scientific Perspective, (Marine Science;
Volume 4). Marcel Dekker, Inc., New York and itsel, pp. 195-232.
Caine, E., 1979. Population structures of two species of caprellid
amphipods (Crustacea). Journal of Experimental Marine Biology
and Ecology, 40: 103-114.
Caine, E.A., 1980. Ecology of two littoral species of caprellid
amphipods (Crustacea) from Washington, USA. Marine Biology, 56:
327-335.
Cambridge, M.L., 1975. Seagrasses of Southwestern Australia with
special reference to the ecology of Posidonia austral is Hook f.
in a polluted environment. Aquatic Botany, 1: 149-161.
Cambridge, M.L., 1979. Cockburn Sound environmental study: technical
report on seagrasses. Department of Conservation and
Environment, Western Australia, Report Number 7, 99 pp.
Camp, O.K., Cobb, S.P. and van Breedveld, J.F., 1973. Overgrazing of
seagrasses by a regular urchin, Lytechinus variegatus.
Bioscience, 23: 37-38.
Cariello, L., and Zanetti, L., 1979. Effect of Posidonia oceanica
extracts on the growth of Staphylococcus aureus. Botanica
Marina, 22: 129-131.
Carr, W.E.S. and Adams, C.A., 1973. Food habits of juvenile marine
fishes occupying saagrass beds in the estuarine zone near Crystal
River, Floridi. Transactions of the American Fisheries Society,
102(3): 511-540.
Castenholz, R.W., 1961. The effect of grazing on marine littoral
diatom populations. Ecology, 42: 783-794.
-------
\ t
Conacher, M.J., Lanzing, W.J.R. and Larkum, A.W.D., 1979. Ecology of
Botany Bay. II. Aspects of the feeding ecology of the fanbellied
leatherjacket, Monachanthus chinenis (Pisces: Monacanthidae), in
Posidonia australis seagrass beds in Quibray Bay, Botany Bay, New
South Wales. Australian Journal of Marine and Freshwater
Research, 30: 387-400.
Congdon, R.A. and McComb, A.J., 1979. Productivity of Ruppia:
seasonal changes and dependence on light in an Australian
estuary. Aquatic Botany, 6: 121-132.
Conover, J.T., 1968. Importance of natural diffusion gradients and
transport of substances related to benthic marine plant
metabolism. Bot. Mar. 11:1-9.
Cottam, C. , 1934. Past periods of eelgrass scarcity. Rhodora, 36:
261-264.
Cottam, C. and Munro, D.A., 1954. Eelgrass status and environmental
relations. Journal of Wildlife Management, 18: 449-460.
Daetwyler, C.C. and Kidwell, A.L., 1959. The Gulf of Batabona, a
modern carbonate basin. Proc. 5th Wld. Petrol. Congr. Sec. 1:
1-21.
Dayton, P.K., 1971. Competition, disturbance and community
organization: the provision and subsequent utilization of space
in a rocky intertidal community. Ecological Monographs, 41:
351-389.
DeFelice, D.R. and Lynts, G.W., 1978. Benthic marine diatom
associations: Upper Florida Bay (Florida) and associated sounds.
Journal of Phycology, 14: 25-33.
den Hartog, C., 1972. 7. Substratum, 7.22 Multicellular plants. In:
Otto Kinne (Editor), Marine Ecology. A Comprehensive, Integrated
Treatise on Life in Oceans and Coastal Waters, Volume I,
Environmental Factors, Part 3. John Wiley and Sons, New York,
pp. 1277-1289.
Drew, E.A., 1979. Physiological aspects of primary production in
seagrasses. Aquatic Botany, 7: 139-150.
Eminson, D. and Moss, B., 1980. The composition and ecology of
periphyton communities in freshwaters. I. The influence of host
type and external environment on community composition. British
Phycological Journal, 15: 429-446.
Fauchald, K. and Jumars, P.A., 1979. The diet of worms: a study of
polychaete feeding guilds. Oceanography and Marine Biology
Annual Review, 17: 193- 284.
7f>
-------
Fenchel, T., 1977. Aspects of the decomposition of seagrasses. In:
C.P. McRoy and C. Helfferich (Editors), Seagrass Ecosystems, A
Scientific Perspective. Marine Science, Volume 4. Marcel
Dekker, Inc., New York and Basel, pp. 123-145.
Fitzgerald, G.P., 1969. Some factors in the competition or antagonism
among bacteria, algae, and aquatic weeds. Journal of Phycology,
5: 351-359.
Gessner, F., 1971. The water economy of the seagrass Thalassia
testudinum. Mar. Biol. 10:258-260.
Ginsburg, R.N. and Lowenstam, H.A., 1958. The influence of marine
bottom communities on the depositional environment of sediments.
Journal of Geology, 66: 310-318.
Goering, J.J. and Parker, P.L., 1972. Nitrogen fixation by epiphytes
on sea grasses. Limnology and Oceanography, 17: 320-323.
Guilcher, A., 1965. Coral reefs and lagoons of Mayotte Island, Comoro
Archipelago, Indian Ocean, and of New Caledonia, Pacific Ocean.
In: W. F. Whittard and R. Bradshaw (Editors), Submarine Geology
and Geophysics. Butterworths, London, pp. 21-45.
Harlin, M.M., 1971. Epiphytic marine algae: interactions with their
hosts. Thesis, Univ. of Washington, Seattle, Washington, 194 pp.
Harlin, M.M., 1973. Transfer of products between epiphytic marine
algae and host plants. Journal of Phycology, 9: 243-248.
Harlin, M.M., 1975. Epiphyte-host relations in seagrass communities.
Aquatic Botany, 1: 125-131.
Harlin, M.M., 1980. Seagrass epiphytes. In: R.C. Phillips and C.P.
McRoy (Editors), Handbook of Seagrass Biology: An Ecosystem
Perspective. Garland STPM Press^JJew_York
117-131. -
Harrison, P.G. and Chan, A.T., 1980. Inhibition of the growth of
microalgae and bacteria by extracts of eelgrass (Zostera marina)
leaves. Marine Biology, 61: 21-26.
Hasler, A.D. and Jones, E. , 1949. Demonstration of the antagonistic
action of large aquatic plants on algae and rotifers. Ecology,
30:359-364.
Heck, K.L. and Orth, R.J., 1980. Structural components of eelgrass
(Zostera marina) meadows in the lower Chesapeake Bay - decapod
Crustacea. Estuaries, 3(4): 289-295.
Hiatt, R.W. , 1944. Food chains and the food cycle in Hawaiian fish
ponds. Part I. The food and feeding habits of mullet (Mugil
77
-------
cephalus), milkfish (Chanos chanos). and the ten-pounder (Elops
machnata). Transactions of the American Fisheries Society, 74:
250-261.
Howard, R.K., in press. The impact of feeding activities of
epibenthic amphipods on surface fouling of eelgrass leaves.
Aquat. Bot.
Howard-Williams, C. and Liptrot, M.R.M., 1980. Submerged macrophyte
communities in a brackish South African estuarine lake system.
Aquat. Bot. 9:101-116.
Humm, H.J., 1964. Epiphytes of the seagrass, Thalassia testudinum in
Florida. Bulletin of Marine Science of the Gulf and Caribbean,
14: 306-341.
Hurara, H.J., 1973. Seagrasses. In: J.I. Jones, R.E. Ring, M.O.
Rinkel, and R.E. Smith (Editors), A Summary of Knowledge of the
Eastern Gulf of Mexico. (Coordinated by the State University
System of Florida, Institute of Oceanography, St. Petersburg.)
American Petroleum Institute, Washington, D.C., pp. IIIC-1 -
IIIC-10.
Hutchinson, G.E., 1975. The algal benthos. In: G. E. Hutchinson, A
Treatise on Limnology, Volume III, Limnological Botany. John
Wiley and Sons, New York, pp. 509-571.
Jacobs, R.P.W.M., 1979. Distribution and aspects of the production
and biomass of eelgrass, Zostera marina L., at Roscoff, France.
Aquatic Botany, 7: 151-172.
Jacobs, R.P.W.M. and Noten, T.M.P.A., 1980. The annual pattern of the
diatoms in the epiphyton of eelgrass (Zostera marina L.) at
Roscoff, France. Aquatic Botany, 8: 355-370.
Johnstone, I.M., 1979. Papua New Guinea seagrasses and aspects of the
biology and growth of Enhalus acoroides (L.f.) Royle. Aquatic
Botany 7: 197-208.
Jones, A.J., 1969. Primary productivity by the tropical marine turtle
grass, Thalassia testudinum Konig, and its epiphytes. (Abstract,
Ph.D. Dissertation, Univ. of Miami, 1968), Dissertation
Abstracts, The Sciences and Engineering, 29(10-Botany):
3637B-3638B.
Kain, J.M. and Svendsen, P., 1969. A note on the local distribution
of Patina pellucida (L.) (Gastropoda) in Britain and Norway.
Sarsio, 38: 25-30.
Kikuchi, T., 1974. Japanese contributions on consumer ecology in
eelgrass (Zostera marina L.) beds, with special reference to
78
-------
\
trophic relationships and resources in inshore fisheries.
Aquaculture, 4: 145-160.
Kikuchi, T. and Peres, J.M., 1977. Consumer ecology of seagrass beds.
In: C.P. McRoy and C. Helfferich (Editors), Seagrass Ecosystems,
A Scientific Perspective. Marine Science, Volume 4. Marcel
Dekker, Inc., New York and Basel, pp. 147-193.
Kiorboe, T., 1980a. Production of Ruppia cirrhosa (Petagna) grande in
mixed beds in Ringkobing Fjord (Denmark). Aquatic Botany, 9:
135-143.
Kiorboe, T., 1980b. Distribution and production of submerged
macrophytes in Tipper Grund (Ringkobing Fjord, Denmark), and the
impact of waterfowl grazing. Journal of Applied Ecology, 17:
675-687.
Kirkman, H., 1978. Growing Zostera capricorni Ashers in tanks.
Aquatic Botany, 4: 367-372.
Kita, T. and Harada, E., 1962. Studies on the epiphytic communities,
I. Abundance and distribution of microalgae and small animals on
the Zostera blades. Publications of the Seto Marine Biological
Laboratory, Kyoto University, 10(2): 101-113.
Kitting, C.L., 1980. Herbivore-plant interactions of individual
limpets maintaining a mixed diet of intertidal marine algae.
Ecological Monographs, 50: 527-550.
Klug, M.J., 1980. Detritus-decomposition relationships. In: R.C.
Phillips and C.P. McRoy (Editors), Handbook of Seagrass Biology:
An Ecosystem Perspective. Garland STPM Press, New York and
London, pp. 225-245.
Land, L.S., 1970. Carbonate mud: production by epibiont growth on
Thalassia testudinum. Journal of Sedimentary Petrology, 40(4):
1361-1363.
Larkum, A.W.D., 1976. The ecology of Botany Bay. I. Growth of
Posidonia australis (Brown) Hook, f. in Botany Bay and other Bays
of the Sidney Basin. Australian Journal of Marine and Freshwater
Research, 27: 117-127.
Lee, J.J., McEnery, M.E., Kennedy, E.M. and Rubin, H., 1973. Educing
the functional relationships among the diatom assemblages within
sublittoral salt marsh epiphytic communities. Bulletins from the
Ecological Research Committee (Stockholm), 17: 387-397.
Lee, J.J., McEnery, M.E., Kennedy, E.M. and Rubin, H., 1975a. A
nutritional analysis of a sublittoral diatom assemblage epiphytic
on Enteromorpha from a Long Island salt marsh. Journal of
Phycology, II: 14-49.
79
-------
Lee, J.J., McEnery, M., Pierce, S. , Freudenthal, H.D. and Muller,
W.A. , 1966. Tracer experiments in feeding littoral foraminifera.
Journal of Protozoology, 13(4): 659-670.
Lee, J.J., Tietjen, J.H., arid Garrison, J.R, 1976. Seasonal switching
in the nutritional requirements of Nitocra typica, a harpacticoid
copepod from salt marsh aufwuchs communities. Transactions of
the American Microscopical Society, 95(4): 628-637.
Lee, J.J., Tietjen, J.H. and Mastropaolo, C., 1975b. Trophic
relationships at lower and intermediate steps in a salt marsh
detritus-based food web. The Biological Bulletin, 149(2): 435.
Lee, J.J., Tietjen, J.H., Saks, N.M., Ross, G.G., Rubin, H. and
Muller, W.A., 1975c. Educing and modeling the functional
relationships within sublittoral salt-marsh aufwuchs communities
- inside one of the black box*,s. Estuarine Research, 1: 710-734.
Lein, T.E., 1980. The effects of Littorina littorea L. (Gastropoda)
grazing on littoral green algae in the inner Oslofjord, Norway.
Sarsia, 65:87-92.
Lipps, J.H. and Valentine, J.W., 1970. The role of foraminifera in
the trophic structure of marine communities. Lethaia, 3:
279-286.
Maggi, P., 1973. Le probleme de la disparition des herbiers a
Posidonies dans le Golfe de Giens (Var). Science et Peche,
Bulletin Inst. Peches marit., 221: 7-20.
Main, S.P. and Mclntire, C.D., 1974. The distribution of epiphytic
diatoms in Yaquina Estuary, Oregon (USA). Botanica Marina, XVII:
88-99.
Marsh, G.A., 1973. The Zostera epifaunal community in the York River,
Virginia. Chesapeake Science, 14(2): 87-97.
Marsh, G.A., 1976. Ecology of the gastropod epifauna of eelgrass in a
Virginia estuary. Chesapeake Science, 17(3): 182-187.
May, V., Collins, A.J. and Collett, L.C. , 1978. A comparative study
of epiphytic algal communities on .two common genera of seagrasses
in eastern Australia. Australian Journal of Ecology, 3: 91-104.
Mclntire, C.D. and Moore, W.W., 1977. Marine littoral diatoms:
ecological considerations. In: D. Werner (Editor), The Biology
of Diatoms. Blackwell, Oxford, pp. 333-371.
McRoy, C.P. and Barsuate, R.J., 1970. Phosphate absorption in
eelgrass. Limnology and Oceanography, 15(1): 6-13.
80
-------
McRoy, C.P., Barsdate, R.J., and Nebert, M., 1972. Phosphorus cycling
in an eelgrass (Zostera marina L.) ecosystem. Limnology and
Oceanography, 17(1): 58-67.
McRoy, C.P and Goering, J.J., 1974. Nutrient transfer between the
seagrass Zostera marina and its epiphytes. Nature, 248: 173-174.
McRoy, C.P and Helfferich, C. (Editors), 1977. Seagrass Ecosystems,
A Scientific Perspective. Marine Science, Volume 4. Marcel
Dekker, Inc. New York and Basel, 314 pp.
Mook, D. , 1977. Studies on fouling invertebrates in the Indian River,
Florida, 2: effect of Modulus modulus (Prosobranchia: Modulidae).
The Nautilus, 91(4): 134-136.
Morgan, M.D., 1980. Grazing and predation of the grass shrimp
Palaemonetes pugio. Limnology and Oceanography, 25(5): 896-902.
Moss, B., 1973. The influence of environmental factors on the
distribution of freshwater algae: an experimental study. III.
Effects of temperature, vitamin requirements and inorganic
nitrogen compounds on growth. Journal of Ecology, 61: 179-192.
Moss, B., 1979. Algal and other fossil evidence for major changes in
Strumpshaw Broad, Norfolk, England in the last two centuries.
British Phycological Journal, 14: 263-283.
Mukai, H., Aioi, K. and Ishida, Y., 1980. Distribution and biomass of
eelgrass (Zostera marina L.) and other seagrasses in Odawa Bay,
central Japan. Aquatic Botany, 8: 337-342.
Neilson, B.J. and Cronin, L.E. (Editors), 1981. Estuaries and
Nutrients. Humana Press, Clifton, New Jersey, 643 pp.
Nelson, W.G., 1979a. Experimental studies of selective predation on
amphipods: consequences for amphipod distribution and abundance.
Journal of Experimental Marine Biology and Ecology, 38: 225-245.
Nelson, W.G., 1979b. An analysis of structural pattern in an eelgrass
(Zostera marina L.) amphipod community. Journal of Experimental
Marine Biology and Ecology, 39: 231-264.
Nelson, W.G., 1980. The biology of eelgrass (Zostera marina L.)
amphipods. Crustaceana, 39(1): 59-89.
Nicotri, M.E., 1977. Grazing effects of four marine intertidal
herbivores on the microflora. Ecology, 58: 1020-1032.
Nixon, S.W., 1981. Remineialization and nutrient cycling in coastal
marine ecosystems. In: B.J. Neilson and L.E. Cronin (Editors),
Estuaries and Nutrients. Humana Press, Clifton, New Jersey, pp.
111-138.
-------
Ogden, J.C., 1980. Faunal relationships in Caribbean ccagrass beds.
In: R.C. Phillips and C.P. McRoy (Editors), Handbook of Seagrass
Biology: An Ecosystem Perspective. Garland STPM Press, New York
and London, pp. ]73-198.
Orth, R.J. and Moore, K.A., 1981a. Submerged aquatic vegetation of
the Chesapeake Bay: past, present and future. In: L. Jahn
(Editor), Transactions 46th North American Wildlife and Natural
Resources Conference, 1981. Wildlife Management Institute,
Washington, D.C., pp. 271-283.
Orth, R.J. and Moore, K.A., 1981b. Distribution and abundance of
submerged aquatic vegetation in the Chesapeake Bay: A scientific
summary. Special Report Number 259 in Applied Marine Science and
Ocean Engineering. Virginia Institute of Marine Science, 42 pp.
Patriquin, D.G., 1972. Carbonate mud production by epibionts on
Thaiassia: an estimate based on leaf growth rate data. Journal
of Sedimentary Petrology, 42(3): 687-689.
Patriquin, D.G., 1975. "Migration" of blowouts in seagrass beds at
Barbados and Carriacou, West Indies, and its ecological and
geological implications. Aquatic Botany, 1: 163-189.
Penhale, P.A., 19~7. Macrophyte-epiphyte biomass and productivity in
an eelgrass (Zostera marina L.) community. Journal of
Experimental Marine Biology and Ecology, 26: 211-224.
Penhale, P.A. and Smith, W.O., 1977. Excretion of dissolved organic
carbon by eelgrass (Zostera marina) and its epiphytes. Limnology
and Oceanography, 22(3): 400-407.
Penhale, ?.A. and Thayer, G.W., 1980. Uptake and transfer of carbon
and phosphorus by eelgrass (Zostera marina L.) and its epiphytes.
Journal of Experimental Marine Biology and Ecology, 42: 113-123.
Peres, J.M. and Picard, J., 1975. Causes de la rarefaction et de la
disparition des herbiers de Posidonia oceanica sur les cotes
Francaises de la Mediterranee. Aquatic Botany, 1: 133-139.
Phillips, G.L., Eminson, D.F. and Moss, B., 1978. A mechanism to
account for macrophyte decline in progressively eutrophicated
freshwaters". Aquatic Botany, 4: 103-125.
Phillips, R.C., 1972. Ecological life history of Zostera marina L.
(eelgrass) in Puget Sound, Washington. Ph.D. Thesis, 1972,
University of Washington, Seattle, Washington, 153 pp.
Phillips, R.C. and McRoy, C.P., 1980. Handbook of Seagrass Biology:
An Ecosystem Perspective. Garland STPM Press, New York, 353 pp.
82
-------
Ramm, G., 1977. Structure of epiphytic diatom populations of the
phytal of the Kiel Bight (Western BaltiO. In: R. Siraonsen
(Editor), Fourth Symposium on Recent and Fossil Marine Diatoms,
Proceedings. Beihefte zur Nova Hedwigia, 54: 379-387.
Randall, J.E., 1964. Contributions to the biology of the queen conch,
Strombus gigas. Bulletin of Marine Science of the Gulf and
Caribbean, 14(2): 246-295.
Reyes-Vasquez, G., 1970. Studies on the diatom flora living on
Thaiassia testudinum Konig in Biscayne Bay, Florida. Bulletin of
Marine Science, 20: 105-134.
Richardson, F.D., 198'J. Ecology of Ruppia marieima L. in New
Hampshire (U.S.A.) tidal marshes. Rhodora, 82(831): 403-439.
Robertson, A.I., 1981. Population dynamics of the snail Littorina
saxatalis in an eelgrass ;adow in Nova Scotia. (Abstract),
Program of the Australia.. Seagrass Workshop, p. 15.
Robertson, A.I. and Howard, R.K., 1978. Diel trophic interactions
between vertically-migrating zooplankton and their fish predators
in an eelgrass community. Marine Biology, 48: 207-213.
Saks, N.M., Stone, R.J. and Lee, J.J., 1976. Autotrophic and
heterotrophic nutritional budget of salt marsh epiphytic algae.
Journal of Phycology, 12(4): 443-448.
Sand-Jensen, K., 1977. Effects of epiphytes on eelgrass
photosynthesis. Aquatic Botany, 3: 55-63.
Scoffin, T.P., 1970. The trapping and binding of subtidal carbonate
sediments by marine vegetation in Bimini Lagoon, Bahamas.
Journal of Sedimentary Petrology, 40(1): 249-273.
Sieburth, J.M. and Thomas, C.D., 1973. Fouling on eelgrass (Zostera
marina L.). Journal of Phycology, 9(1): 46-50.
Smith, W.O. and Penhale, P.A., 1980. The heterotrophic uptake of
dissolved organic carbon by eelgrass (Zostera marina L.) and its
epiphytes. Journal of Experimental Marine Biology and Ecology,
48: 233-242.
Southward, A.J., 1964. Limpet grazing and the control of vegetation
on rocky shores. Br. Ecol. Soc. Symp., 4: 265-274.
Stoner, A.W., 1979. Species-specific predation on amphipod Crustacea
by the pinfish Lagodon rhomboides: mediation by macrophyte
standing crop. Marine Biology, 55: 201-207.
Stoner, \.W., 1980. Feeding ecology of Lagodon rhomboides (Pisces:
83
-------
' ;aridae): variation and functional responses. Fishery Bulletin,
73(2): 337-352.
Sullivan, M.J., 1977. Structural characteristics of a diatom
coiwnunity epiphytic on Ruppia maritima. Hydrobiologia, 53(1):
81-86.
Swinchatt, J.P., 1965. Significance of constituent composition,
texture ard skeletal breakdown in some recent carbonate
sediments. Journal of Sedimentary Petrology, 35: 71-90.
Taylor, J.D. and Lewis, M.S., 1970. The flora, fauna and sediments of
the marine grass beds of Mahe, Seychelles. Journal of Natural
History, 4: 199-220.
Taylor, J.L. and Saloman, C.H., 1968. Some effects of hydraulic
dredging and coastal development in Boca Ciega Bay, Florida.
Fisheries Bulletin, 67: 213-241.
Thayer, G.W., Parker, P.L., LaCroix, M.W. and Fry, B., 1978. The
stable carbon isotone ratio of some components of an eelgrass,
Zostera marina, bed. Oecologia, 35: 1-12.
Thayer, G.W., Wolfe, D.A. and Williams, R.B., 1975. The impact of man
on seagrass systems. American Science, 63: 288-296.
Tietjen, J.H. and Lee, J.J., 1977. Feeding behavior of marine
nematodes. In: B.C. Coull (Editor), Ecology of Marine Benthos.
University of South Carolina Press, Columbia, pp. 21-35.
Trocine, R.P., Rice, J.D. and Wells, G.N., 1981. Inhibition of
seagrass photosynthesis by ultroviolet-B radiation. Plant
Physiology, 68: 74-81.
van Montfrans, J., Orth, R.J. and Vay, S.A., 1982. Preliminary
studies of grazing by Bitcium variant on eelgrass periphyton.
Aquatic Botany, (in press).
Weitzel, R.L., 1979. Periphyton measurements and applications. In:
R.L. Weitzel (Editor), Methods and Measurements of Periphyton
Communities: A Review. American Society for Testing and
Materials, Philadelphia, pp. 3-33.
West, R.J. and Larkum, A.W.D., 1979. Leaf productivity of the
seagrass, Posidonia australis, in eastern Australian waters.
Aquatic Botany, 7: 57-65.
Wetzel, R.G. and Penhale, P.A., 1979. Transport of carbon and
excretion of dissolved organic carbon by leaves and
roots/rhizomes in seagrasses and their epiphytes. Aquatic
Botany, 6: 149-158.
I
a/.
-------
Wood, E.J.F., 1959. Some aspects of the ecology of Lake Macquarie,
N.S.W. with regard to an alleged depletion of fish. VI. Plant
communities and their significance. Australian Journal of Marine
and Freshwater Research, 10: 322-340.
Wood, E.J.F., 1972. 7. Substratum, 7.21 Unicellular p'ants. In: Otto
Kinne (Editor), Marine Ecology. A Comprehensive, Integrated
Treatise on Life in Oceans and Coastal Waters. Volume I,
Environmental Factors, Part 3. John Wiley and Sons, New York,
pp. 1272-1276.
Wood, E.J.F., Odum, W.E. and Zieman, J.C., 1969. Influence of
seagrasses on the productivity of coastal lagoons. Lagunas
Costeras, un Simp. Merra. Simp. Intern. Lagunas Costeras.
UNAM-UNESCO, Mexico, pp. 495-502.
Young, O.K. and Young, M.W., 1978. Regulation of species densities of
seagrass associated macrobenthos: evidence from field experiments
in the Indian River estuary, Florida. Journal of Marine
Research, 36: 569-593.
Zapata, 0. and McMillan, C., 1979.
Aquatic Botany, 7: 307-317.
Phenolic acids in seagrasses.
Zieman, J.C., 1975. Tropical seagrass ecosystems and pollution.
E.J.F. Wood and R.E. Johannes (Editors), Tropical Marine
Pollution. Elsevier Oceanography, Series 12, pp. 63-74.
In:
Zieman, J.C., 1976. The ecological effects of physical damage from
motor boats on turtlegrass beds in southern Florida. Aquatic
Botany, 2: 127-139.
Zimmerman, R.J., Gibson, R.A. and Harrington, J.B., 1977. Gammaridean
amphipod feeding strategies in a Florida seagrass bed.
Contributions, Department of Marine Science, University of Puerto
Rico, 15(262): 59.
Zimmerman, R., Gibson, R. and Harrington, J., 1979. Herbivcr-y and
detritivory among gammaridean amphipods from a Florida seagrass
community. Marine Biology, 54: 41-47.
85
-------
CHAPTER 2
THE EFFECT OF SALINITY STRESS ON THE SURVIVAL AND
BEHAVIOR OF BITTIUM VARIUM ADULTS AND LARVAE
Robert J. Orth
Judith Capelli
Jacaues van Montfrans
86
-------
-
ABSTRACT
The effects of salinity reductions on the activity and survival
of Bittium varium adults and larvae were examined under laboratory
conditions. Five salinity tests, three tests using adults and two
tests using newly hatched larvae were conducted by either rapidly or
gradually reducing the salinity. The results of the tests showed that
salinities lower than 10 °/oo are stressful for adult _B. varium.
Adult JJ. varium died at 6.9 °/oo when exposed to a rapid reduction in
salinity. With a gradual reduction, they survived to 6.9 °/oo but
individuals were sluggish in their behavior. Veliger larvae were more
susceptable to salinity stress than adults. Larvae did not survive in
salinities of 11 °/oo while some development occurred between 11 and
16 °/oo. However, metamorphosed individuals were found only at 22 and
16 °/oo.
The greater susceptability of larvae to salinit> reductions
compared to adults suggests that the loss of _B. varium from western
shore grass beds following Tropical Storm Agnes in June 1972, may have
been due to reduced or no recruitment during peak spawning periods.
The virtual absence of juveniles in these beds late in 1972, further
substantiates this hypothesis. Loss of ji. varium and alterations of
the grazer populations in many of these areas may have important
implications for the decline of eelgrass in these areas since Ihe
passage of Tropical Storm Agnes.
87
-------
-
INTRODUCTION
The eelgrass (Zostera marina L.) epifaunal community in the
Chesapeake Bay is a diverse assemblage of species from nume-ous
taxonomic groups, e.g. hydrozoans, nemerteans, amphipods, isopods,
polychaetes, gastropods, nudibranchs, cirripeds and bivalves (Marsh,
1973, 1976). Functionally, it comprises herbivores, carnivores, and
omnivores.
One numerically dominant herbivorous gastropod, Bittium varium
Pfeiffer (Cerithiidae), is the subject of the present study. Found in
densities of up to 200 individuals per gram of eelgrass (Marsh, 1976),
JJ. varium may be an important consumer. Experiments witn B. varium
grazing on eelgrass periphyton showed that leaves with JJ. varium had
63X dry weight less periphyton than leaves without JJ_. varium (van
Montfrans et al., 1982). This grazing action may have important
implications for the distribution of eelgrass, especially for those
plants living in habitats where light levels reaching the plant
suiface may be only marginally adequate for photosynthetic maintenance
(van Montfrans et al., 1982).
In June 1972 a major hurricane (Tropical Storm Agnes) affected
the Chesapeake Bay. The extensive rainfall that accompanied Agnes
rapidly and drastically reduced salinities Baywide, especially in
surface waters in the western portion of the Bay and its tributaries
(Davis and Laird, 1977). Adult JJ. varium were observed in the York
River soon after Agnes in July and August 1972 but juveniles, normally
present in the population at this time, were not (Orth, 1977, and
•J pers. obs., 1972). Juveniles normally replace adults in the
* population by late summer so that Ji. varium present each breeding
* season are those produced the preceding season (unpublished data).
J Surveys of the eelgrass epifauna in 1973 revealed relatively few
JJ. varium in waters along the western shore of the Bay where they had
„ been abundant before Agnes, suggesting that the 1972 year class may
| have been detrimentally affected by the salinity reduction (Orth,
J 1977). Since the storm occurred during the time JJ_. varium reproduces,
"I it was hypothesized that it may have somehow interfered with breeding
i success or increased juvenile mortalities.
*t
Between 1972 and 1974 eelgrass in some areas of the Chesapeake
Bay also declined dramatically (Orth, 1976; Orth and Moore, 1982).
The decreased abundance of JJ. varium in 1973, and the subsequent
coincidental decline of eelgrass in 1973 suggested a causal
relationship. It was hypothesized that nuch reduced Bittium varium
88
-------
populations may have been ineffective in grazing periphyton from
eelgrass leaves resulting in increased periphyton biomass which was
thought to have been detrimental to the eelgrass in this %'jserved
decline (van Montfrans et al., 1982).
The studies described herein are designed to study the effects of
salinity reductions on Bittium varium adults and larvae and to
preliminarily assess the conseouences of such reductions for Z_. varium
activity and survival under experimental conditions. Based on an
analysis of data from experimental work, the effects of Tropical Storm
Agnes on J^. varium populations in the lower Chesapeake Bay were
re-evaluated in light of the declines of Zostera marina over the last
decade.
MATERIALS AND METHODS
Bittium varium used in this study were collected from a natural
population occurring with eelgrass near Vaurluse Shores on the
Chesapeake Bay side of the Eastern Shore of Virginia (37*25'N
latitude, 75*59'W longitude). The eelgrass bed in that area
represents one of the largest (140 hectares) and most persistent beds
on that shore (Orth et al., 1979). Eelgrass is found there from mean
low water (MLW) where it occurs with wideongrass, Ruppia maritima, to
a depth of 1.5 m where it occurs in monospecific stands.
Collections were made on eight dates: May 4, 1981; May 20,
June 9, June 17, July 9, August 26, October 15 and January 6, 1982.
Two methods of sampling were used. In the first, a fine mesh net
(0.5 mm) attached to a D-frame sled was pulled through the eelgrass
bed. Net contents were sieved to separate Bittium varium from the
rest of the material. These snails were immediately transported to
the laboratory in coolers (70 1.) and placed in a large holding tank
(1360 liters) with flow-through York River water. The salinity of the
water at the collecting site and at the laboratory on the York River
were similar (22-24 °/oo). Mean temperature ir. the holding tank in
June, when adult B. varium were removed from use in Tests 1, 2, and 3,
was 26.4*C. Browse for the JJ. varium consisted of the abundant
periphyton that grew either o.i the walls of the holding tank or on
large pieces of the alga, Ulva lactuca, collected in the shoal areas
near the laboratory.
In the second method, eelgrass with attached Bittium varium was
hand clipped near its base and placed in fine mesh (0.5 mm) collecting
bags. These bags were placed in buckets with water and returned to
the laboratory. The eelgrass leaves were gently washed to remove
—• var:*-um which were either preserved in an alcohol solution and
measured at a later date or placed in the holding tank. All IK varium
that were collected were used either in the laboratory experiments or
in growth estimates.
Before each experiment, a sample of Bittium varium was removed
from the holding tank. The length of each snail was measured from the
«o
-------
apex of the shell to the lip, to the nearest 0.01 mm using Wild M-3
dissecting stereomicroscope with an ocular micrometer, and the average
length of the tank population was determined. Enough JJ. varium for a
test were then removed from the holding tank. The correct number for
each bowl were counted and temporarily placed in small jars of York
River water prior to being gently transferred to each bowl when the
test was initiated.
Estimating Bittium varium Growth from a Natural Population
At each sampling period, a number of Bittium varium (15-350
depending upon their availability) were randomly chosen from samples
collected primarily by the second method. Individuals were measured
as described above. Numbers of JJ. varium occurring in 0.50 mm size
class categories were tabulated. These categories corresponded to
those used in previous work with JJ. varium (Marsh, 1970, 1976).
Bittium varium larvae for salinity tolerance tests were
laboratory reared and were obtained from egg masses deposited on
pieces of live Ulva lactuca and glass plates pliced in the holding
tank. Egg masses were placed in two 38 liter aquaria with bag
filtered York River water (22 °/oo salinity) on 13 July 1981. Veliger
larvae were first observed in both aquaria on 15 July. Larvae were
fed daily with several railliliters of cultured phytoplankton
consisting of Monochrysis lutheri, Isochrysis galbana, Pseudochrysis
paradoxa, Chlorella sp. and Tetraselmis specie a grown in filtered
(0.1 u and 1.0 u) pasteurized York River water (approximately
22 °/oo).
Aquaria water for the tests of salinities less than 22.4 °/oo was
made by diluting b»^-filtered water from the York River with
appropriate amounts of deionized water. Initially, large volumes of
test solutions were made and stored in 48 liter carboys to insure
suffici'.rt supplies for water changes throughout the course of the
test. Carboys were stored at room temperature (approximately 26 °C),
similar to that of the incubators and the holding tank. All salinity
samples were analyzed using a Beckman Induction Salinometer, Model
RS-7B, calibrated with standard sea water (35.00 +_ .01 °/oo S) at
laboratory temperature. Samples were brought to approximate
laboratory temperature and read in duplicate.
ly placed finger bowls were maintained in three Precision
dual programmed incubators, Mix! el 815. Lighting provided by a bank of
fluorescent lights along the length of the door simulated natural
diurnal conditions in onset and length of daylight hours. Incubators
were programmed to provide a temperature of 24 +_ 2*C.
Salinity Tolerance Test 1 - Effect of Rapid Salinity Reduction and
Return Lo Ambient Salinity on Adult Activity and Survival
The first -.alinity test was designed to study effects of rapid
salinity reduction on adult activity and survival. Active snails were
-------
considered Co be those which were able to adhere to any surface of a
bowl and were capable of locomotion. Inactive individuals were those
that were retracted or extended but not able to adhere to 'he glass.
Because of the inherent difficulty of determining mortality in snails
in the "inactive" category, especially in retracted or immobile
individuals, a determination of survival was made only at the
termination of the test after snails had been returned to ambient
(22.4 °/oo salinity) water. Those snails still inactive after 72 hrs
in 22.4 °/oo salinity water were considered to have died. Four
salinities were tested: 1.7, 6.9, 10.8, and 22.4 (ambient).
Chemically clean glass finger bowls (18 cm x 6.5 cm deep), each with
1200 mis of test water were used as aquaria. There were nine
replicates of 22.4, 10.8, and 6.9 °/oo water and three replicates of
1.7 water. Air was continuously pumped to each bowl through capillary
tipped pipettes. Each bowl was covered with plastic wrap to reduce
evaporation.
Glass plates (7.6 x 12.7 cm) covered with periphyton were
introduced to each bowl as a food source for Bittium varium during the
test. The plates had been taped to bricks and placed in an existing
eelgrass bed to become fouled. Prior to each test, plates were
brought to the laboratory, removed from bricks, and suspended
horizontally in each experimental bowl approximately 2.5 cm above the
bottom by monofilament threads. One hundred B_. varium, average length
3.7 mm (N=150), were then gently transferred onto each plate and bowls
were placed in incubators.
At 24, 48 and 72 hours, Bittium varium in all bowls were examined
using a dissecting stereomicroscope at 6.4X magnification and
categorized as either active or inactive. After the 72 hours
examination, a salinity sample was taken and water in each bowl was
replaced with 22.4 °/oo York River water. Snails were examined after
an additional 72 hours.
Salinity Tolerance Test 2 - Effect of Rapid Salinity Reduction on
Adult Activity
Because the results of the first test showed a large difference
in survival between snails in 6.9 and 10.8 °/oo salinity water, a
second test was designed to further examine intermediate salinity
tolerances with one control salinity. Nine replicates of 21.3, 11.3,
9.2, and 6.9 °/oo salinity water were tested with 50 Bittium varium,
average length 3.9 mm (NS50), in each finger bowl. Methodology was
similar to Test 1 except that plastic petri dishes (90 x 15 mm deep)
fouled with periphyton were used instead of glass plates.
Observations of the snails were made every 24 hours for 12 days using
the same criteria as in Test 1. Water in each bowl was changed after
96 and 216 hours with clean water of the original salinity. At this
time a sample of the old water from each bowl was taken for salinity
determination. Additional food for JJ. varium was added to the petri
dishes by scraping periphyton from the walls of the holding tanks,
sieving and concentrating the material, and placing a small portion
-------
(approximately 2 mis) in the dish. The test was terminated at 264 hrs
and a sample of water from each bowl was taken for a final salinity
determinat ion.
Salinity Tolerance Test 3 - Effects of a Gradual Salinity Reduction on
Adult Activity
This experiment was designed to test the activity of Bittium
varium under gradual salinity reductions. Fifty adult ]J. varium,
average length 4.0 mm (N=149), from the holding tank were initially
placed in each of three bowls with York River water (21.9 °/oo
salinity). Plastic petri dishes fouled with periphyton were used as
in Test 2. Every 24 hours JJ. varium were counted and examined for
activity using the same criterion as in Test 1. Water in each bowl
was then replaced with water of a lower salinity. On five consecutive
days salinity was reduced from 21.9, 15.4, 11.3, 9.2 to 7.3 °/oo,
respectively. B^. varium remained in the 7.3 °/oo salinity water for
14 days, at which time it was replaced with water of 3.4 °/oo salinity
for an additional 6 days. Snails were observed and counted
periodically. Water was changed regularly and food added daily
following the procedures described for Test 2.
Salinity Tolerance Test 4 - Effect of Rapid Salinity Reduction on
Larval Survival and Metamorphosis
Three nlinities were used in this experiment, 22.3, 11.1 and
6.6 °/oo, with three replicates per salinity. Small finger bowls
(11.5 cm in diameter x 4.5 cm deep) were filled with 200 ml of water
of the appropriate salinity. Methodology for handling the finger
bowls was similar to Test 1.
The test began on 7/20 when veliger larvae hatched since 7/15
were concentrated by siphoning water from the i.wo hatching aquaria
(see Methods) through a 35 y mesh sieve held in a water bath to
cushion the larvae. Larvae were rinsed into a 500 ml graduated
cylinder and brought up to 500 ml volume with 22.3 °/oo salinity York
River water. The mean number of live larvae per ml (24) was
determined from five counts using a Sedgewick-Rafter cell. Water in
the cylinder was gently stirred, and one ml was transferred to the
cell with a 1 ml volumetric (TD) pipette. One drop of dilute Clorox
was added to the cell to kill the larvae which were subsequently
counted. The remaining water and larvae in the cylinder were gently
stirred before approximately 10 mis (i.e. 240 live veliger larvae)
were transferred to each finger bowl with a 10 ml volumetric (TO)
pipette. Bowls were then placed in the incubators. Thereafter water
was changed periodically (after observations were completed) to new
water of the same salinity. Larvae were retained by screening through
a 35 urn sieve. Treatment was the same for all bowls on a given day.
The larvae were fed daily with severe! mis of appropriate dilutions of
the stock algae culture (described in the Methods section) in order to
avoid altering the salinities in the bowls. Dilutions were made with
deionized water. The volume of a dilution added to each bowl was
-------
adjusted so that all bowls received approximately equal amounts of
algae. At each feeding the addition of algal culture to the test
bowls was as follows: 2 ml of undiluted stock culture (approximately
22 °/oo salinity) was added per bowl at 22,3 °/oo salinity; 4 ml of a
1 part stock culture to 1 part deionized water dilution (approximately
11 °/oo salinity) per bowl at 11.1 °/oo salinity; and 8 ml of a 3:1
dilution (approximately 6 °/oo salinity) per bowl at 6.6 °/oo
salinity. Dilutions of the stock culture were checked before addition
to bowls to insure viability of algae. Bowls were monitored fro the
presence of viable larvae, either veligers or pediveligers, using a
dissecting microscope as in Test 1 beginning on 7/'21, one day after
larvae were introduced to bowls. Metamorphosed individuals were
counted in each bowl and a total compiled at the termination of
observations. Observations on a given bowl were terminated when
viable larvae were no longer present: the test ran for 17 days.
Salinity Tolerance Test 5 - Effect of Gradual Salinity Reduction on
Larval Survival and Metamorphosis
Effects of five salinities (22.3, 16.3, 11.1, 9.5, and 6.6 °/oo)
with six replicates per salinity were studied. This test was
initiated and run concurrently with Test 4. Initially, snail finger
bowls were set up with 200 ml of 22.3 °/oo salinity water in six bowls
and 200 ml of 16.3 °/oo salinity water in 24 bowls. Using the
techniques described in Test 4 approximately 240 veliger larvae in
10 ml of 22.3 °/oo salinity water were transferred to each of the 30
bowls. After each 24 hour period all water was changed. The
technique for changing water was the same as in Test 4. Bowls with
22.3 °/oo salinity remained at that salinity while six of the 24 bowls
with 16.3 °/oo salinity were kept at 16.3 °/oo and the remaining 18
bowls were filled with 11.1 °/oo salinity water. This procedure was
followed again at 48 and 72 hours with six bowls remaining at the
lowest prior salinity and all remaining bowls changed to the next
lowest salinity. After 72 hours, 6 bowls remained at 6.9 °/oo, the
lowest salinity being tested. Larvae were fed daily following the
procedure described in Test 4. Prior to each water change, 6 bowls
were examined under a dissecting microscope for presence of viable
larvae, either veligers or pediveligers. Metamorphosed individuals
were counted in each bowl and a total compiled at the termination of
observations. Observations on bowls with 11.1, 7.5 and 6.6 °/oo
salinity were terminated on 7/29. Those on 16.3 and 22.3 °/oo were
terminated on 8/7. Periodic salinity samples were taken. The test
continued for 17 days until all larvae had either died or
metamorphosed.
RESULTS
Bittlum varium Growth
Of the initial May 5, 1981 sample of Bittium varium from Vaucluse
Shores, 562 were between 2.50-2.99 mm in shall length while 892 were
between 2.50 and 3.49 mm (Fig. 1). The tendency for the population to
-------
60-
50-
40-
30-
20-
10-
MAY 5
\ \ \
m
60-1
20
10
0
60
50
40
30
20
10
0
-Pi-
1
I rill
0 10 20 30 40 50
JULY
T" r
II
,640
AUG. 26
li
OCT 15
(ZZZ^
I I I I
JAN 6
n
I I T \ I
0 10 20 30 40 50
LENGTH (mm)
Figure 1. Length-frequency histograms for Bittium varium collected from
Vaucluse Shores from May 5, 1981 to Jan. 6, 1982.
-------
be distributed in one or two size classes was evident in all eight
sampling periods indicating not only synchronous growth but evidence
of distinct year classes. By June 10, 1981, 902 of the individuals
were between 3.50 and 4.49 tarn shell length. One week later the
largest individuals were recorded wi.:h 112 of all individuals between
4.50 and 5.49 mm. On August 26, the new year class w?s evident with
772 of the individuals between 0.50 and 1.49 mm and with & notable
reduction in the larger size class categories that were abundant
previously. On October 15 and January 6, 98-100% of the individuals
were between 1.50 and 2.49 mm with the absence of individuals greater
than 3.00 mm. There appeared to be little growth of JJ. varium between
October 15 and January 16 as there was no significant difference in
the percentage of individuals in the size class represented.
Salinity Tolerance Test 1
Table 1 presents the results of the first salinity tolerance test
in which JJ. varium (average length 3.7 mm, n=150) were exposed to a
rapid salinity reduction. There were no active Bittium varium in the
1.7 °/co salinity after 72 hrs or after snails were placed back in
22.4 °/oo water for 72 hours. At the 6.7 °/oo salinity, only a few
survived while at the 10.8 and 22.4 °/oo salinities, 1002 were active
after 24 hours with only 1-2 described as not active after 72 hours.
There were no differences in the percentages of active snails at these
two latter levels. The major result in this test was the significant
difference (p<0.05) in survival of snails at the 6.7 and 10.8 °/oo
salinities.
Salinity Tolerance Test 2
Table 2 presents the results of the second salinity tolerance
test in which Bittium varium (average length 3.9 mm, n=50) were
exposed to a rapid salinity reduction. Shown is the mean percentage
of active snails for each salinity interval every 24 hoars, and also
salinity tests representing subsets with means that are not
significantly different (p>0.05, one-way ANOVA with a Student-Newman-
Keuls test for significant differences among the means; all tests were
performed on arc-sine transformed data. Almost no snails were active
in the 6.9 °/oo salinity after the first 24 hours. The numbers of
snails active at this salinity were signifiantly less (p<0.05) than
those active at the other salinities. The mean percentage of active
snails at the 9.2 °/oo salinity was always significantly greater
(p<0.05) than the 6.9 °/oo salinity but significantly less (p<0.05)
than the mean percentage of active snails in 11.3 and 21.3 °/co
salinities (except at 144 hours, when the 9.2 and 11.3 °/oo salinities
were not significantly different, p>0.05). There was no significant
difference (p>0.05) in the mean percentage of active snails between
th? 11.3 and 21.3 °/oo salinities. Table 3 presents mean salinity and
standard deviation at 96, 216, and 264 hours for four of the test
salinities.
-------
TABLE 1. THE MEAN PERCENT AND STANDARD DEVIATION OF ACTIVE SNAILS IN
EACH TEST AFTER 24, 48 AND 72 HOURS AND THE Z SURVIVING
AFTER BEING PLACED IN AMBIENT SALINITY (22.4 Z) FOR AN
ADDITIONAL 72 HOURS. NUMBERS IN PARENTHESIS AFTER TEST
SALINITY INDICATE NUMBERS OF REPLICATES FOR THAT TEST. MEAN
SALINITY AND STANDARD DEVIATION AT FIRST 72 HOURS FOR FOUR
TEST SALINITIES ARE GIVEN.
Test
Salinity
1.7
6.7
10.8
22.4
(3)
(9)
(9)
(9)
X Active and S.D .
24 hrs
0+0
0.8+0.9
100+0
100+0
48 hrs
0+0
1.4+2.1
100+0
100+0
72 hrs
0+0
1.4+_2.
99.9+0.
99.9+0.
2
3
3
Mean Salinity and 72
S.D. at 72 hrs 22
2
7
12
24
.2+0.
.4+0.
.8+0.
.4+0.
3
1
6
7
C.
98.
99.
hrs. in
.4 °/oo
0+0
8+1
2+2
.6
.3
7+0.5
nt.
-------
TABLE 2. THE MEAN PERCENT OF ACTIVE SNAILS IN EACH SALINITY TEST
(n-9) EVERY 24 HOURS FOR 288 HOURS. NUMBER IN PARENTHESIS
GIVES PL.RCENT ACTIVE SNAILS AND HORIZONTAL LINES BELOW THE
SALINITIES INDICATES HOMOGENOUS SUBSETS WHOSE MEANS ARE NOT
SIGNIFICANTLY DIFFERENT (p>0.05).
Time (hrs . )
24
48
72
96
120
144
168
192
216
240
264
288
Salinity
6.9(2.4) 9
6.9(0.4) 9
6.9(0.9) 9
6.9(1.1) 9
9
9
Terminated- 9
snails 9
decayed 9
9
9
9
.2(94
.2(92
.2(92
.2(93
.2(91
.2(91
.2(92
.2(93
.2(93
.2(91
.2(90
.2(74
(mean
.9)
.7)
.7)
.3)
.8)
.8)
.0)
.6)
.1)
.1)
.9)
.4)
percent
11
11
11
11
11
11
11
11
11
11
11
11
active)
.3(100)
.3(100)
.3(100)
.3(96
.3(96
.3(91
.3(96
.3(95
.3(95
.3(95
.3(95
.3(95
.4)
.0)
.8)
.0)
.3)
.3)
.3)
.6)
.2)
21
21
21
21
21
21
21
21
21
21
21
21
.3(100)
.3(100)
.3(100)
.3(99
.3(99
.3(99
.3(99
.8)
.8)
.8)
.3)
.3(100)
.3(99
.3(99
.3(98
.3(99
.3)
.6)
.9)
.8)
97
-------
TABLE 3. MEAN °/oo SALINITY AND STANDARD DEVIATION AT THE 96, 216,
AND 264 MRS FOR THE FOUR TEST SALINITIES.
Test
Salinity
6.9
9.2
11.3
21.3
96 hrs
7.4 +
9.8 -f
12.1 +_
22.0 +
(6/19)
0.2
0.3
0.3
0.3
Mean Salinity + S.D.
216 hrs (6/24)
—
10.0 +_ 0.2
11.8 +_ 0.5
22.4 •«• 0.3
264 hrs (6/26)
—
9.5 +_ 0.1
11.6 +_ 0.1
22.3 + 0.1
-------
Salinity Tolerance Test 3
The results of Test 3 indicated there was no significant
difference (p>0.05; one-way ANOVA) in the daily percentage of active
snails from the start of the experiment until 456 hours later, one day
after they were placed in 3.4 °/oo salinity water (Table 4). Data
from the last 3 observation periods were significantly different from
the preceding period, after the snails had been in 3.4 °/oo salinity
water for more than 24 hours. A one-way ANOVA of percent active
snails by salinity indicated a significant difference in the 3.4 °/oo
level (p<0.05) from the five other levels which were not significantly
different (p>0.05).
Salinity Tolerance Test 4
Table 5 presents the results of the number of veliger larvae that
metamorphosed at the three salinity levei. . used in this test. In
salinity test 4, metamorphosed individuals were found only in 22.3
°/oo salinity water. Larvae at this salinity survived up to 17 days
after the experiment was initiated when the last metamorphosed snail
was recorded. Although no individuals metamorphosed in 11.1 °/oo
salinity water, some larvae in all three bowls did reach pediveliger
stage by 7/22. Viable larvae were not observed in 11.1 °/oo salinity
bowl« after 7/23. Larvae in 6.6 °/oo salinity bowls were not alive at
the first observation on 7/21, one day after the larvae had been
introduced.
Salinity Tolerance Test 5
Larvae metamorphosed and survived after 18 days only in 22.3 and
16.3 °/oo salinity water in both tests (Table 5) and there was no
significant diference between the two salinities (p>0.05).
Considerable variation was observed among the six bowls at these two
salinities with regard to the total numbet of metamorphosd individuals
in both tests.
Observations made during the gradual salinity reduction test(s)
indicated that the 11.1 °/oo larvae were active for 48 hours while at
72 hours larvae were alive but inactive. After 170 hours, all larvae
had experienced mortality. Larval development was observed to occur
at this salinity as some advanced from the veliger to the pediveliger
stage and some had metamorphosed for up to 96 hours after the
experiment started, but those which remained at 11.1 °/oo salinity
died soon thereafter. Some Larvae transferred to the 9.5 °/oo level
were still active at 48 hours but at 72 hours all larvae were dead.
Larval development was observed to occur at 11 °/oo salinity as some
advanced from veliger to pediveliger stage and one metamorphosed
within the first 24 hours but none survived. By the time the larvae
were placed in 6.9 °/oo water the number of larvae were reduced
-------
TABLE 4. PERCENT ACTIVE SANILS AT EACH OBSERVATION PERIOD AND THE
SALINITY °/oo AT WHICH SNAILS WERE PRESENT DURING THAT
PERIOD. VERTICAL LINES TO THE LEFT OF THE HOURS COLUMN
INDICATE SUBSETS OF DATA ON SNAIL ACTIVITY WHOSE MEANS ARE
NOT SIGNIFICANTLY DIFFERENT (SNK, p>0.05).
Time (hours) Salinity Percent Active
Bowl 1 Bowl 2 Bowl 3
24
48
72
96
120
168
192
216
240
360
432
456
528
552
600
21.9
15.4
11.3
9.2
7.3
7.3
7.3
7.3
7.3
7.3
7.3
3.4
3.4
3.4
3.4
100
100
100
100
96
94
100
100
100
100
94
90
86
70
36
100
100
100
100
98
98
100
100
100
98
98
91
10
10
2
100
100
98
100
98
100
100
100
100
100
96
94
78
84
52
-------
TABLE 5. TOTAL NUMBER AND MEAN +^1 S.D. OF METAMORPHOSED JJ. VARIUM
OBSERVED PER TEST SALINITY IN THE TWO TESTS WHERE VELIGER
LARVAE WERE EXPOSED TO KAPID SALINITY SHOCK (TEST 4) AND A
GRADUAL SALINITY REDUCTION (TEST 5) OVER AN 18 DAY PERIOD.
ALL TESTS STARTED WITH APPROXIMATELY 240 LARVAE IN EACH
BOWL. VERTICAL LINES TO THE LEFT OF THE SALINITY COLUMN
INDICATE SUBSETS OF DATA WHOSE MEANS ARE NOT SIGNIFICANTLY
DIFFERENT (SNK, p>0.05).
22. 3
11.1
6.6
Test 4. Rapid Salinity Reduction
No . of Metamorphosed Ind.
Test
Salinity
°/oo
Number
por
Bowl
ABC
Total
Number Mean No. and S.D.
0
0
0
0
0
0
16
0
0
5.0 +_ 4.6
0 +_ 0
0 + 0
Test 5. Gradual Salinity Reduction
No. of Metamorphosed Ind.
Test
Salinity
°/oo
22
16
11
9
6
.3
.3
.1
.5
.6
A
3
3
0
0
0
B
2
9
0
0
0
Number
per
Bowl
C
15
13
0
0
0
D
2
2
0
0
0
E
10
4
0
0
0
F
25
6
0
0
0
Total
Number
57
37
0
0
0
Mean No.
9.5 +
6.2 *_
0 +
0 +
0 +
and S.D.
9.2
4.2
0
0
0
101
-------
i although some were still actively swimming. However, after only
• 24 hours at this salinity, live larvae were no longer present.
DISCUSSION
Based on results of sampling the Bittium varium population at
Vaucluse Shores in 1982 as well as results from previous studies
(Marsh, 1973, 1976; Diaz et al., 1982), the life span of JJ. varium is
estimated to be approximately 14 to 18 months. JJ. varium generally
reproduces in June, with a new year class appearing in early July.
Adults either die after spawning or live for only several months
thereafter. By October-November, adults were not found in the Vacluse
Shore grassbed. The new year class overwinters in the sediments,
continues to grow in the spring and early summer and spawns in late
June to complete the life cycle.
' Newly hatched, free-swimming veliger larvae emerge from egg cases
1 laid on Zostera marina leaves. They apparently are not released as
pediveligers or crawling juveniles. Swimming veliger larvae were
observed for periods as long as 18 days in our experimental tests.
However, the length of the larval life may actually be much shorter
* under natural conditions because the presence of Z. marina leaves may
induce faster settlement of the larvae. This phenomenon has been
observed with planktonic larvae of many other invertebrate species
where either the presence of adults of that species or certain
sedimentological properties hastens settlement (Wilson, 1948, 1952,
1953, 1954, 1955, 1960, 1968, 1970; Knight-Jones, 1951, 1953;
Sheltema, 1961; Bayne, 1965; Thorson, 1966, 1975; Carriker, 1967).
; The results of laboratory salinity tests showed that salinities
I lower than 10 °/oo are stressful for adult Bittium varium. When
exposed to rapid salinity reductions, JJ. varium did not survive 6 °/oo
salinity (test 1 and 2). Although there was significant survival at 9
- and 10 °/oo salinity, anectdotal notes taken during the tests
I indicated that there were qualitative differences in the behavior of
* some of the snails in these levels. Snails moved along the bowls much
more slowly and their bodies were less extended from the shells than
snails at the 11 and 21 °/oo levels. When dislodged from feeding
surfaces, some snails at the 9 and 10 °/oo reattached more slowly than
at the higher salinity levels. Some snails at the 9 °/oo level in
test 2 appeared to equilibrate to that level and become more active as
several had even deposited egg cases in their bowls.
* Although in the gradient salinity test (test 3), adults survived
I at 6.9 °/oo, anectodotal observations indicated that their behavior
* was distinctly different from those in the higher salinities. Snails
were barely extended from their shells and moved very slowly. Feeding
presumably did not occur initially since fecal pellets were not
observed. Although movement was still quite slow after 120 hours in
6.9 °/oo water, some snails began to feed and egg cases were noted in
two o* the bowls. However, when placed in 3.4 °/oo water, the snails
102
-------
experienced rapid mortality and the few remaining at the end of the
experiment showed almost no movement.
The results of the tests using the veliger larvae indicated that
larvae were more susceptible to salinity stress than adults. Live
metamorphosed juveniles were not observed for extended periods in
treatments with salinities less than 11 °/oo. Observations of larvae
in the gradual salinity reduction experiment (test 5) indicated that
larvae survived and some development occurred at salinities lower than
16 °/oo and that several had metamorphosed, although eventually, both
larvae and metamorphosed individuals died.
Interpretation of data from salinity tolerance tests using both
adult and larval Bi11i urn varium suggests that the reduced salinities
following Agnes could have affected B. varium populations by causing
larval mortalities. The timing of the passage of Agnes may have been
the most critical factor in its offeet on the eelgrass fauna,
especially JB. vavium. Assuming that _B_. varium was reproductive at the
tine of Agnes, it is likely that the very low salinities in the lower
Bay tributaries could have detrimentally affected the recruitment of
the new year class. At the mouth of the York River (Sandy Point along
the north side), the salinity after Agnes was as low as 9 °/oo and did
not rise above 13 °/oo until August S, almost 45 days after Agnes.
Normally salinities in the area ranged between 15 and 20 °/oo for the
same period during previous years. Adults were present after Agnes at
this site but the juveniles were not observed in samples collected in
August (Orth, pers. obs.). Some recruitment and survival of juveniles
must have occurred because J5. varium were present in samples collected
in 1973 at several sites in the York River, but their abundances were
lower than levels recorded before Agnes (Orth, 1977).
It is also possible that Bittium varium adults at the Zostera
marina beds further upriver suffered greater mortality than downstream
populations since salinities were 6 to 6 °/oo or even lower for at
least a week after Agnes. Surviving individuals could have postponed
reproduction until a normal salinity level returned. The f.w
experimental snails which survived exposure to 6 °/oo salinities in
Test 5 were observed laying egg cases after being returned to York
River water (22 °/oo).
In sunmary, although detailed information on biological changes
in Zostera marina beds in the lower Bay immediately following Agnes is
limited, our data suggest that the dramatic reduction in Bittium
varium populations along the western shore of the Bay may be
attributable to larval mortality caused by extreme salinity
reductions. Bittium varium larvae appear to be more susceptible to
mortality by reduced salinities than adults and therefore the very low
salinities recorded after Agnes coincidental with the time JJ. varium
reproduces, may have seriously interefered with subsequent
recruitment. Since JK varium only reproduces once in the summer and
adult mortality occurs shortly after spawning, the population dynamics
of this species could seriously be altered by extremely low
103
-------
salinities. A significant reduction of J^. varium, an important member
of the Z_. marina epifaunal community could subsequently result in a
very different epiphyte community structure. If the role of ]5. varium
is significant in reducing epiphytic growth thereby ultimately
enhancing plant vigor, the loss of JJ. varium following Agnes could
have reduced the vigor of Z_. marina and encouraged the decline of Z.
marina in 1973, one year after Agnes.
104
-------
LITERATURE CITED
Bayne, B. L. 1965. Growth and delay of metamorphosis of larvae of
Mytilus edulus (L.). Ophelia 2:1-7.
Carriker, M. R. 1967. Ecology of estuarine benthic invertebrate :
a perspective, pp. 442-487 in_ George H. Lauf (ed.), Estuaries.
A.A.A. Publ. #83, Horn-Shafer Co., Baltimore.
Davis, J. and B. Laird. 1977. The effects of Tropical Storm Agnes
on the Chesapeake Bay estuarine systems. Chesapeake Research
Consortium Pub. No. 54. 639 pp.
Diaz, R. J. and T. Fredette. 1932. Secondary production of some
dominant macroinvertebrate :pecies inhabiting a bed of submerged
aquatic vegetation in the !^»rer Chesapeake Bay. pp. 95-123 in R.
J. Orth and J. van Montfrans (eds.), Interaction of resident
consumers in a temperate, estuarine seagrass community: Vaucluse
Shores, Virginia, U.S.A. VIMS SRAMSOE No. 267, and U.S. E.P.A.
Final Report. Grant No. R8G5974. 238 pp.
Knight-Jones, E. W. 1951. Gregariousness and some other aspects of
setting behavior of Spirorbis. J. Mar. Biol. Ass. U.K.
30:201-222.
Knight-Jones, E. W. 1953. Decreased discrimination during setting
after prolonged planktonic life in larvae of Spirolbis borealis
(Serpulidae). J. Mar. Biol. Ass. U.K. 32:337-345.
Marsh, G. A. 1973. The Zostera epifaunal community in the York
River, Virginia. Chesapeake Sci. 14:87-97.
Marsh, G. A. 1976. Ecology of the gastropod epifauna of eelgrass in
Virginia estuary. Chesapeake Sci. 17:182-187.
Orth, R. J. 1976. The demise and recovery of eelgrass, Zostera
marina, in the Chesapeake Bay, Virginia. Aquat. Bot. 2:141-159.
Orth, R. J. 1977. The effect of Hurricane Agnes on the benthic
fauna of eelgrass, Zostera marina, in the lower Chesapeake Bay.
In: J. Davis and B. Laird (coordinators). The Effects of
Tropical Storm Agnes on the Chesapeake Bay Estuarine System. The
Johns Hopkins University Press, Baltimore, Mariland. pp.
566-583.
105
-------
Orth, R. J. and K. A. Moore. 1962. Distribution and abundance of
subnerged aquatic vegetation in the Chesapeake Bay: A scientific
perspective. Virginia Institute of Marine Science Special Report
Appl. Mar. Sci. & Ocean Eng. No. 259.
Orth, R. J., K. A. Moore and H. H. Gordon. 1979. The distribution
and abundance of submerged aquacic vegetation in the. lover
Chesapeake Bay, Virginia. Final Report EPA 600/8-79-029/SAV 1,
199 pp.
Sheltama, R. S. 1961. Metamorphosis of the veliger larvae of
Nassarlus obsoletus (Gastropoda) in response to bottom sediment.
Biol. Bull. 120:92-109.
Thorson, G. 1957. Bottom communities. Chapt. 17 in J. W. Hedgpeth
(ed.), Treatise on marine ecology and paleoecology. Vol. 1,
Ecology, Geol. Soc. Am. Mem. 67:1296.
Thorson, G. 1966. Some factors influencing the recruitment and
establishment of marine benthic communities. Netherlands J. Sea
Res. 3:267-293.
van Montfrans, J., R. J. Orth and S. Vay. (in press). Preliminary
studies of grazing by Birtium varium on eelgrass periphyton.
Aquat. Bot.
Wilson, D. P. 1948. The larval development of Ophelia bicornis
Savigny. J. Mar. Biol. Ass. U.K. 27:540-553.
Wilson, D. P. 1952. The influence of the nature of the substratum
on the metamorphosis of the larvae of marine animals esp. the
larvae of Ophelia bicornis Savigny. Ann. Inst. Oceanogr. Monoco.
27:49-156.
Wilson, D. P. 1953. The settlement of Ophelia bicjrnis Savigny. The
1951 experiment. J. Mar. Biol. Ass. U.K. 31:«*l3-438.
Wilson, D. P. 1954. The attractive factor in the settlement of
Ophelia bicornis Savigny. J. Mar. Biol. Ass. U.K. 33:361-380.
Wilson, D. P. 1955. The role of micro-organisms in the settlement
of Ophelia bicornis Savigny. J. Mar. Biol. Ass. U.K. 34:531-543.
Wilson, D. P. 1960. Some problems in larval ecology related to the
localized distribution of bottom animals, pp. 87-103 in
Perspectives in Marine Biology. U. of Calif. Press, Berkeley and
Los Angeles.
Wilson, D. P. 1968. The settlement behavior of the larvae ot
Sabfcllaria alveolata (L.). J. Mar. Biol. Ass. U.K.
48(2):387-435.
106
-------
Wilson, D. P. 1970. The larvae of Sabellaria spinulosa and their
settlement behavior. J. Mar. Biol. Ass. U.K. 50:33-52.
107
-------
CHAPTER 3
THE ROLE OF GRAZING ON EELGR*.3S PERIPHYTON:
IMPLICATIONS FOR PLANT VIGOR
Jacques van Montfrans
Robert J. Orth
and
Clifford H. Ryer
108
-------
ABSTRACT
Natural periphyton removal through grazing and subsequent effects
on the growth of transplanted eelgrass (Zostera marina) were
investigated in laboratory microcosms. Experimental treatments
contained herbivorous gastropods (Bittium variuin) which fed on the
periphyton growing on Z,. marina under three levels of shading (25, 47,
and 632 light reduction) for approximately 30 days. Control tanks
were similar but did not contain B. varium. Parameters measured at
the termination ol the experiment included number of shoots, leaf
weight, leaf area, periphyton dry weight and ash-free dry weight,
chlorophyll a, phaeophytin a and macroalgal standing crop.
Light attenuation in the three shade treatments was significantly
different between treatments. The effects of the presence of
£. varium in the tanks were clearly seen within a week after the
experiment was initiated. Leaves with J.. varium were relatively clean
while leaves without JL varium were thickly coated with periphyton.
At the end of the experiment, treatments with B. varium at the high
and low shading levels had significantly more shoots, greater leaf
area and a higher leaf weight than the comparable controls. There was
no significant difference in these three parameters across shade
levels for both the experimental treatments and the controls.
Periphyton and ashfree periphyton weights increased with increasing
shading in the absence of ]J. varium but decreased in the presence of
JJ. varium. Chlorophyll a_ and phaeophytin a_ concentrations showed
considerable variation at the end of the experiment and were no1:
significantly different among the treatments except at the high shade
Bittium treatment for chlorophyll a_. Values for phaeophytin a_ at each
shading level tended to be lower in the presence of j^. varium than
when j^. varium was absent.
The results of these experiments have important implications for
the growth of the Z. marina and other seagrasses. Production and
turnover estimates for marine angiosperms may be closely linked to the
degree of periphyton fouling and consequently on the presence or
absence of grazers which rely on periphyton as a food source. The
absence of B. varium in Z. marina^ beds along the western shore of the
Bay may, in part, be a factor in the decline of these grass beds in
1173.
109
-------
INTRODUCTION
A recent shift from descriptive to experimental approaches in
; seagrass studies has helped to elucidate the functional relationships
within these complex habitats. Understanding such relationships is
crucial to the interpretation of past and present events in localized
grassbeds and can also have predictive value. A dramatic decline of
Zostera marina, a dominant species of submerged aquatic vegetation
(SAV) in the more saline portions of the Chesapeake Bay, has occurred
since 1972 (Orth and Moore, 1982). Recent research efforts have
t focused on determining the cause for the decline of SAV species and on
I understanding th«s functional role of this important natural resource
; in the shallow waters of the Bay (Wetr.el et al. , 1981; Kemp et al.,
1981).
|
j The presence of Zosters marina adds to the complexity of an
i otherwise barren sandy bottom and provides food, refuge and substrate
; for a diverse assemblage of species. The loss or reduction of
; vegetation drastically reduces species diversity (Orth, 1977) and has
i even changed the foraging strategy of at least two species of
overwintering waterfowl (Munro and Perry, 1981). Many commercially or
recreationally exploited species rely either directly or indirectly on
seagrasses. Blue crabs (Callinectes sapidus) and trout (Cynoscion
spp.) utilize Zostera marina beds as nursery and feeding areas(Heck
and Orth, 1980T
Invertebrates inhabiting seagrass beds typically assimilate
seagrass-fixed carbon through a bacterially mediated detrital pathway
(Fenchel, 1977; Klug, 1980). The infauna and epifauna are in turn fed
upon by resident and transient consumers, thus providing a link
between the seagrasses and higher trophic levels which frequently
contain commercial species (Carr and Adams, 1973; Brook, 1975, 1977;
Adams, 1976; Stoner, 1979; Stoner and Livingston, 1980; Zimmerman et
al., 1979; Nilsson, 1969; Ryer and Boehlert, 1982; Orth and van
Montfrans, 1982; Brown, 1981; Lascara, 1981; Ryer, 1981). The demise
of SAV in the Chesapeake Bay may therefore have far reaching effects
on numerous local species.
Several factors have been implicated in the decline of seagrasses
in the Chesapeake Bay (Stevenson and Confer, 1978). Agricultural land
use patterns have resulted in more extensive applications of
herbicides and fertilizers, some of which enter the Bay through
runoff. Herbicide use has increased with little understanding of itu
effect on SAV. Nutrient enrichment from both fertilizer runoff and
sewage input are known to stimulate plankton productivity resulting in
L
110
-------
increased turbidity and greater light attenuation, thereby limiting
macrophyte growth (Walker, 1959, Rayan et al., 1972; Klausner et al.,
1974; Stolp and Penner, 1973). The productivity of both macro- and
microepiphytes of seagrasses is also enhanced by nutrient enricnment
and the resulting epiphytic proliferation can be a factor in the
demise of seagrass beds (Cambridge, '975; Sand-Jensen, 1977).
A diverse assemblage of epiphytes is typically associated with
seagrass blades (Harlin, 1980). Micro-epiphytes (periphyton) are a
major food source for many customers inhabiting SAV beds (Kikuchi and
Peres, 1977; Harlin, 1980; Ogden, 1980). Grazers of periphyton can
substantially reduce the biomass of macro-epiphytes (Hunter, 1980; van
Montfrans, et al., in press) thereby possibly mediating the effects of
nutrient enrichment on periphyton proliferation. In the absence of
grazers, periphyton may have the potential to rapidly overgrow and
shade the host plant thus reducing photr>synthetic activity (Sand-
Jensen, 1977). Borum and Wium-Anderson (1980) determined that heavily
fouled Zostera marina leaves received only 10% of the light available
for photosynthesis. The wavelength of light absorbed by periphyton
growing on Z. marina is identical to that utilized by the host (Caine,
1980). Encrusting diatoms on the leaves of "L_. marina therefore
utilize almost all of the available solar energy and considerably
reduce macrophyte photosynthesis by limmiting both light and
bicarbonate uptake (Sand-Jensen, 1977).
Shading experiments have demonstrated the negative effects of
light attenuation on plant growth (Backman and Barilotti, 1976;
Congdon and McComb, 1979). Because light attenuation is one factor
determining the lower depth limit of macrophyte growth, fouling by
epiphytes may also affect seagrass distribution (Burkholder and
Doheny, 1968; Phillips, 1972; Thayer et al., 1975; Jacobs, 1979; Makai
et al., 1980). SAV will decline throughout its depth range when
shading by epiphytes results in an inadequate amount of light for
photosynthetic maintenance of the host plant (Cambridge, 1975).
In the Chesapeake Bay, Bittium varium, a prosobranch gastropod,
is one of the dominant grazers on the periphyton associated with
Zostera marina (Marsh, 1973, 1976). These small snails (less than
7 mm in shell length) have oeen shown to s>'gnif icantly reduce the
bioraass of periphyton associated with Z_. marina under laboratory
conditions (van Montfrans, et al., in press). The demise of Zostera
marina along the western shore of the lower Bay following the drastic
decline of Bittium varium in the same area during 1972 (Orth, 1977)
led to the hypothesis that the presence of periphyton grazers can
indirectly affect the vigor of the host plant by preventing periphyton
proliferation to potentially harmful levels. The objective of this
project was to examine how the growth of Zostera marine was affected
by the presence or absence of Bittium varium in laboratory
experiments.
Ill
-------
r
L
METHOD? ANI- MATERIALS
Experimental Design
Six large fiberglass tanks (3 x 2 x 0.5 m) each containing nine
polypropylene trays (60 cm long x 30 cm wide x 25 cm high) filled to a
depth of 14 cm with grassbed sediments were employed in the experiment
(Fig. 1). Sediment devoid of vegetation was collected from a Guinea
Marsh grassbed at the mouth of the York River one week prior to
transplanting the vegetation. Plugs of Zostera marina were collected
from the same grassbed on 22 May 1981. A cylindrical 30 CIP long
plexiglass coring tube measuring 9.4 cm in diameter (0.069 m2 area)
was carefully placed around several shoots and pushed into the
sediment to a depth of 14 cm. Each plug consisting of eelgrass
leaves, roots, rhizomes and attached sediments was placed in a plastic
bag after decanting the surplus water and transported to the
laboratory in large coolers to prevent desiccation. Six plugs of
vegetation were transplanted into each polypropylene tray by removing
sediment with the plexiglass core and replacing it with a vegetated
plug-
After transplanting the plugs, the fiberglass tanks were filled
to 40 cm with ambient seawater from the York River. Thus, the
sediment surface in the plastic trays was 26 cm from the air-water
interface. York River water was continuously pumped through each tank
at the rate of 960 1/hr resulting in a complete turnover every hour.
Tanks were randomly assigned an experimental treatment to test
for the effects of three degrees of shading in the presence and
absence of Bittium varium on plant growth (Table 1). Pairs of tanks
were covered with shades reported to reduce ambient light by 25, 47
and 632 (Chicopee brand luraite woven polypropylene shades, style
5187909, 5183809 and 5184009, respectively). The low shade treatment
(25Z reduction) was chosen to simulate the observed mean light level
reaching plants in the Guinea Marsh grassbed during 1979. Medium (472
reduction) and high shade (632 reduction) treatments were designed to
reflect further light reductions such as that caused by phytoplankton
blooms or increased suspended sediments. A randomly chosen experi-
mental tank under each level of shading .as innoculated with Bittium
varium to Lest the effects of periphyton grazing on plant growth. The
second tank of each pair was designated as the control tank.
Bittium Innoculation
Bittium varium were collected from a large Zostera marina bed at
the mouth of Hungar's Creek on Virginia's Eastern Shore using a
0.5 meter D-ring epibenthic sled. A standard volume of JJ. varium
(1/2 dram " approx. 340 individuals) was introduced to each
experimental plug of grass. This was accomplished by lowering the
water level in all tanks to 4 cm above the sediment surface, and
gently placing the JJ. varium on the Zostera marina leaves in the
112
-------
60
113
-------
TABLE 1. ARRANGEMENT OF TANK EXPERIMENT UTILIZING BITT1UM VARIUM
UNDER DIFFERENT INTENSITIES OF SHADE.
Tank 1
Tank 2
Tank 3
Tank 4
Tank 5
Tank 6
Shading
25%
632
252
472
472
632
Biciium
Yes
No
No
No
Yes
Yes
114
-------
experimental tanks only. The water in all t.Tnks was then raised to
th^ original level. Snails w e first introduced to the plugs on
May 22, 1981. Subsequently, we observed th.it snails soon dispersed to
thf sides of the tanks and polypropylene boxes wht-n periphyton on
grass blades became scarce. Additional snails were therefore placed
on experimental plugs on June 4 and June 16.
Tank Cleaning Procedures
All tanks were cleaned on a weekly basis r.o minimize the rapid
fouling of nonliving surfaces. Cleaning was accomplished by lowering
the water level in each tank and gently scouring the sides of the tank
and polypropylene boxes with a plastic household scouring p.-: 1 . All
algae, barnacles, other encrusting organisms and accumulated sediments
were removed by this process. Care was taken not to disturb the
transplanted plugs during the 45 minute cleaning procedure for each
tank. However, prior to lowering the water level, the water over each
plug was agitated uniformly by hand to simulate the wave action that
slants frequently experience under field conditions. This was done to
remove any loosely adhering participate material (mostly sediments)
that accumulated on the blades due to Che reduced turbulence in rhe
experimental tanks.
Sampling Procedure
Sampling was conducted from June 29 through July 3, 1981
approximately one month after initiating the experiment. Three trays
with six plugs each wero randomly selected from each tank (treatment).
While still underwater, choots of each plug were gently groomed to
remove unattached macroalgae and dead grass blades. Next, the shoots
of each plug were clipped off at the sediment surface and carefully
transferred Co an enamel pan filled with seawater. Observations on
the number of living shoots, general appearance, and condition of the
blades were recorded concurrently. The base of each shoot was thei
separated from rhe blades at the leaf node and dried in Cared aluminum
envelopes for ary weight determinations. The blades were mechanically
stripped of all attached periphyton and sediment by being repeatedly
drawn through closed forceps. All materials removed in this way
remained in the water-filled enamel pans. The stripped blades were
saved for leaf area and dry weight determinations.
rj varium, if present, were removed from the enamel trays,
counted, and preserved in 102 formalin. The remaining contents of Che
trays were sieved through a 0.5 mm screen and rinsed to force all
suspended sediment and microalgae (periphyton) through the screen.
The filtrate was collected and storad at 5*C for 16 hrs in 32 oz. jars
to allow suspended materials to settle. Excess water was decanted and
the conCenCs (i.e. periphyCon and sediment) were transferred to 4 oz.
jars and frozen for later examination. All materials retained by the
sieve were examined under a dissecting microscope to remove all
epibioia and Zostera marina fragments, leaving only the macroalgae.
115
-------
; The toacroalgae were then placed in tared aluminum pans for dry weight
I determination.
i
- Leaf Area Measurements
i
i Blades from each plug were blotted dry and sandwiched in a flat
i non-overlapping arrangement between two layers of Saran brand plastic
(wrap. Grass blade area estimates were then determined using a LI-COR
Model LI13100/1+1 Leaf Area Meter. Three area estimates were taken
[ for each plug and from these the mean value was calculated to be the
i leaf area for that plug.
Chlorophyll a and Pheophytin a Determination
Chlorophyll a determinations were made using a modified method
developed by Whitney and Darley (1979). This method employs a phase
separation te-hnique in which buffered aqueous-acetone extracts are
partitioned with hexane to separate interferring chlorophylls and
phaeophytin a_ from chlorophyll a_. The concentration of chlorophyll a_
in the presence of phaeophytin a_ was then detemined from absorbencies
of acidified and non-acidified aliquots of the hexane hyperphase read
on a Bausch and Limb Model 21 specirophotometer at 663 and 750 run.
After pigment extraction of the periphyton samples, all particulates
were saved and deposited in tared aluminum pans for dry weight
determinations.
Dry Weight and Ashfree Dry Weight Determinations
Dry weights were measured for leaves, shoot bases, macroalgae and
periphyton. Materials were dried to constant weight (UC hrs at 50*C
in a drying oven), tiansferred to desiccators for cooling to ambient
temperature and weighed on a Met tier balance (Model H-51). After
weighing, periphyton samples were combusted in a muffle furnace at
475 *C for 4.5 hours, cooled in desiccators, art4 reweighed.
Light Readings
The actual quantity of light reaching the experimental plugs was
determined by taking periodic light measurements using a LI-COR, Inc.
Quantum/Radiometer/Photometer Model LI-185B. These were taken both
with the shades in place and with the shades removed, at a water depth
of 26 cm (the approximate depth of the sediment surface in the trays).
Ambient light was also concurrently recor^d. Since preliminary
analysis showed no significant difference (ANOVA, p<0.05) in light
attenuation between experimental and control tanks under the same
shading regime, subsequent readings were taken in only one of the two
tanks for each treatment after the third week.
Ambient light conditions varied from day to day because of
weather conditions and therefore all light data are reported as
extinction coefficients following the equation:
116
-------
where
Kj m extinction coefficient
£2 = light intensity at surface
EI * light intensity at 26 cm and
0.26 * depth from surface (in meters).
The data collected for each tank enabled us to test the assumption
that light attenuation due to water quality was the same for all
treatments, and that observed differences in light inte sity were
caused by the artificial shades only.
Statistical Analysis
Data gathered from the eighteen replicate Zostera marina plugs
from each experimental treatment included numbers of shoots, leaf
weight, and leaf area. These data were used as primary indicators of
plant vigor since they integrated the effects of grazing activity,
periphyton fouling and Z_. marina photosynthesis on plant growth.
Direct measurements of periphyton fouling (macroalgae vt., periphyton
dry wt. and ashfree wt., chlorophyll _a, and pheophytin a) w»re also
made and standardized as the ratio of the measured parameter to total
leaf area per plug.
Data for the sample period were log transformed and tested for
homogeniety of variance (Bartletts F-max). In cases where the
assumption of homogeneous variance were met, data were analyzed using
a combination of one way analysis of variance (ANOVA), Student-Newman-
Keuls multiple range testing, and T-test (Sokal and Rohlf, 1969). In
cases where variances were determined to be heterogeneous, nonpara-
metric tests were utilized (Kruskal-Wal1 is one way analysis of
variance and Mann-Whitney U-test). Light data were first tested for
homogeneity of variance using the Bartlett F-max test, and then
analyzed by one way analysis of variance (Sokal and Rohlf, 1969).
RESULTS
The mean quantity of ohotosynthetically available light
(470-560 ran) on sunny days, during the course of the study was
1511 microeinsteins (me). The mean values of light actually available
to the experimental plants was 857 me for low shade treatments, 643 me
for medium shade treatments, and 452 me for high shade treatments.
This represented i 43, 58, and 69% decrease in available light,
respectively.
Light attenuation in the three shade treatments (i.e. low, medium
and high shade) was significantly different (ANOVA), p<0.05) between
tr«afnw»nts (Fig. 2; Table 2). With the shades removed, however, no
significant difftrences (ANOVA, p>0.05) were observed between tanks
(Fig. 3; Table 3) indicating that light differences between treatments
were due to the shade covers only. Differences in light between
117
-------
J
Figure 2. Llcht a-tetmatlon (expressed as the extinction coefficient) in
the three pairs of experimental tanks with shades in place.
Initiallv, measurements were made in all six tanks but since
paired measurements were not significantly different (p^O.05),
light measurements after day 25 were taken in only one of each
nair of tanks.
118
-------
TABLE 2. ANALYSIS OF LIGHT ATTENUATION AMONG TREATMENTS (AS MEASURED
BY EXTINCTION COEFFICIENTS) DUE TO THE COMBINED EFFECTS OF
WATER TURBIDITY AND ARTIFICIAL SHADING.
Analysis of all
treatment-, trough
day 25 of experiment
Analysis of Variance (ANOVA)
significant at p *• 0.000
F * 50.579
Student-Newman-Keul (SNK) (p < 0.0\)
Treatment
Mean Value
L
1.83
LB
2.19
M MB
3.34 3.54
H HB
4.62 4.67
Analysis of treatments
1,2, and 3 (low shade
Bittiaro, high shade and
medium shade, respectively)
for entire experiment
Analysis of Variance (ANOVA)
significant at p • 0.000
F - 75.060
Student-Newman-Reul (SNK) (p < 0.05)
Treatment LB M H
Mean Value 2.19 3.34 4.62
L - Low shade treatment
M - Medium shade treatment
H - High shade treatment
LB - Low shade Bittium treatment
MB - Medium shade Bittium treatment
HB - High shade Bittium treatment
* - On day 25, preliminary analysis (ANOVA) showed the three shading
treatment types to be significantly different from one another.
However, T-tests demonstrated no significant differences between
shading replicates (i.e. Bittium vs. non Bi11ium). Therefore it
was decided to limit light measurements to one treatment of each
shading level for the remainder of the experiment.
119
-------
- -V V N
Figure 3. Light attenuation (expressed as the extinction coefficient)
in the three pairs of tanks with shades removed. Initially,
measurements were made in all six tanks but were not
significantly different (pN0.f>5) during the first 25 days and
subsequent light intensities were monitored in only one tank
under each level of shading.
120
-------
TABLE 3. ANALYSIS OF WATER TURBIDITY AMONG TREATMENTS (AS MEASURED BY
EXTINCTION COEFFICIENTS).
Analysis of all
treatments through
day 25 of experiment
Analysis of Variance (ANOVA)
significant at p = 0.25
F - 1.376
Stadent-Newman-Keul Multiple Ranges (SNK) (p < 0.05)
Treatment
Mean Value
L
0.57
M
0.1.9
H
0.77
Lb
0.91
MB
0.98
Analysis of treatments
1,2, and 3 (low shade
Bittium, high shade and
medium shade, respectively)
for entire experiment*
Analysis of Variance (ANOVA)
not significant at p " 0.46
F - 0.788
Student-Newman-Keul Multiple Ranges (SNK) (p < 0.05)
Treatment
Mean Value
M
0.70
H
0.77
LB
0.9i
L - Low shade treatment
M - Medium shade treatment
H - High shade treatment
LB - Low shade Bittium treatment
MB - Medium shade Bittium treatment
HB - High shade Bittium treatment
* - On day 25, preliminary analysis (ANOVA) showed the three shading
treatment types to be significantly different from one another.
However, T-tests demonstrated no significant differences between
shading replicates (i.e. Bittium vs. non Bittium). Therefore it
was decided to limit light measurements to one treatment of each
shading level for the remainder of the experiment.
121
-------
experimental (with J3. varium) and control (no 3. varium) tanks for
each of the three shading levels were also net significant (T - test;
p>0.05).
Plant Vigor: Shoots, Leaf Weight and Leaf Area
Numbers of shoots, leaf weight and leaf area per plug exhibited
the same general pattern among treatments (Fig. 4) with experimental
treatments being significantly higher for all three variables (ANOVA;
p<0.0b) and with SNK analysis dividing treatments into two respective
groups: IJ. varium present, and ji. varium absent (Table 4). Among the
two groups there were no significant differences (p<0.05) between
tanks with different levels of shading. At the high and low shading
'avels, T-tests (p<0.05) showed that treatments with jJ. varium had
consistently higher values for each parameter than did control tanks
without JJ. varium. However, at the medium shade level, T-tests showed
that for leaf area and leaf weight, differences were not significant
(p>0.05) between experimental and control tanks.
Periphyton, Pcriphyton Ashfree, and Ma.roalgae "eight
These parameters showed considerable range in their variances,
and were therefore analyzed using non-parametric ranking methods. For
periphyton and periphyton ashfree dry weights, Kruskal-Wallis one way
analysis of variance showed treatments to be significantly different
(p<0.05) when tested together, as well as when grouped into Bittium
and non Bittium categories (Table 5). Examination by the Mann-Whitney
U test, showed that control treatments (non Bitturn) had consistently
higher values when compared to experimental treatments (with Bittum).
Thus periphyton and ashfree periphyton weights increased with
increasing shading in the absence of Bi11i urn, but decreased in the
presence of Bittium (Fig. 5).
Wich respect to macroal^al weight, all treatments, with the
exception of high shading -.ith Bittium, were statistically similar.
The latter had a significantly low?r mean value (K-W-ANOVA, p<0.05)
than others.
Chlorophyll a and Phaeophytin a
The variation of chlorophyll £ and pheophytin £ levels were
considerable among treatments. Hence, nonparametric statistical
methods were used in data analysis. With respect to chlorophyll £,
all treatments were similar, except for the high shade Bittium
treatment, which had signifi-.antly lower levels of chlorophyll £
(K-W-ANOVA, p<0.05) (Table 6; Fig. 6). When the ANOVA tested only
Bittium treatments, a significant difference among treatments was also
observed, with cl lorophyll £ concentration being inversely related to
the level of shading. For phaeophytin, an analysis of variance
demonstrated a non-significant variation (p>0.05) among all
treatments, as well as among the non-Bittium treatment. The
Mann-Whitney U test detected a -jon-significant difference (p>0.05)
122
-------
1/1
o
o
A '*
ca BEIM *•&(.•«
LOW MEDIUM HIGH
SHADING LEVEL
Figure 4. Mean numbers of shoots, leaf weight and leaf area for experimental
and control tanks at the three levels of shading.
123
-------
5
o
w
en
H
U.
O
a
w
en
at
U
U]
H
O
U
z
UJ
1-1 H
H Z
U
u. z:
°s
V) U
1-1 a.
en X
>< u
0)
u
c
c
so
o
o
o
o
N
O.
u"i
O
O
O
£
en
C
o
z
01
•o
(0
£
0)
"8
M
• *4
X
124
-------
I! II II
t T -r
I I I
-------
a
Ul
3
Z
»4
(-,
z
8
>*^
~»
a
at
H
01
u
e
eg
u
• •4
U-4
••4
C
BO
• v4
C/J
00
.-4
W
£
a
c
<
A •Oin »ir, cs «— 1
X •
^
CN
00 •»
J •
CN
1
i |
— ! 1
x x ^r n in
z • • x • !
CN 1 CN CN j
=0 0)1 en 1
XPH ~-* t QQ *3 c^ 30 CN !
-j- • *o >o -; • t-M CM
«e c
O> eg
LI ai
H X
u u u
< < < ID CB m
> > > V 01 01
O^£ Ob£ O^& 4J4-I4J
Z Z Z Z Z z III
£
— i C 4j 3 -a 60
— . O ••< O O> — <
< Z aa J X X
ed
W
u
<
u-«
eg
OI
.
n
ao
3
CL
en
to
eg
u
ao
00
— •
u
o
U-l
0)
OI
3
CB
>
e
e«
01
•o *
31 '
B <
U 4J |
0 C 4.
u-i o< c
• B a
C 4J 1
eg 4j eg 4
U C 0)
4J 01 4J 14 |
4j E c " :
00 C w U ••
0 Oj «8 1 B 4
-* B 0) 4J 3 4
u L, eg -^ ..
i» eg 4J 01 *-* 0
L. CJ, U U
CO V. 41 4J ••* <
*-> -O CO 1
en eg ti e
oi oi £ -a v j
3 TJ » eg Tl <
— eg js -c f
> » 3 « :
•-4 £
eg A-a t>C 3 -t
4j o 01 ••» o <
« J Z X J 3
•o
» 1 1 1 1
•^
< J r * 3 §
j
i 4J
= C
J 0>
0 E
U U
^ eg
J OI
u
: u
3
* E
J 3
J •*•
-4 4J
3 4J
• M
U CO
3
g oi
: •«
o eg
j-S
•< £.
t.y
: x
i
gx
L
126
-------
TABLE 5. STATISTICAL ANALYSIS OF GRAVIMETRIC DATA FROM THE FOULING
COMMUNITY.
Variable
Treatment Groups
Macro Algae
Weight
Periphyton
Dry Weight
Pe* iphyton
Ashfree
Dry Weight
All
Non-Bitt ium
BittiuiB
Low shade
Med shade
High shade
All
Non-Bittiurn
Bittium
Low shade
Med shade
High shade
All
Non-Bittium
Bittium
Low shade
Med shad
High shade
Analysis
Significance
K-W X2-38.118 p=0.000
K-W X2=1.226 p=0.542
K-W X2=30.030 p-0.000
M-W U-116.0 p-0.1456
M-W U="123.0 p=0.2172
M-W U-24.0 p=0.0000
K-W X2*78.162 p-0.000
K-W X2"14.733 p-0.001
K-W X2-18.029 p-0.000
M-W U«58.0 p-0.0010
M-W U»4.0 p-0.0000
M-W U-0.0 p-0.0000
K-W X2-67.353 p-0.000
K-W X2»13.194 p-0.001
K-W X2«12.831 p-0.002
M-W U-71.0 p-0.0068
M-W U-9.0 p-0.0000
M-W U-18.0 p-0.0000
All data values are log transformed mean values for 18 grass plugs.
K-W - Kruskal-Wallis oneway ANOVA
M-W - Mann-Whitney U test
127
-------
a-
o
00
5
EBL
'-.;•;..-A t
.sa-
MEPIl-M HIGH
LOW
SHADING LEVEL
$'''$& ' $$
fi • S**v>* ' tf%'^-
•
Figure 5. Mean macroalgal weight, pertphyton dry weight and periphyton ash
free dry weight per leaf area for experimental and control tanks
at the three levels of shading.
128
-------
TABLE 6. STATISTICAL ANALYSIS OF PHYTOPIGMENT DATA FROM THE FOULING
PERIPHYTON COMMUNITY.
Variable
Treatment Groups
Analysis
Significance
All
Non-Bittium
Chlorophyll a_ B i 11 i urn
Low shade
Med shade
High shade
All
Non-Bittium
Phaeophytin _a Bittium
Low shade
Med shade
High shade
K-W X2-18.619 p-0.002
K-W X2-0.582 p-0.747
K-W X2=24.266 p-0.000
M-W 11=20.39 p-0.2821
M-W U-147.0 p=0.6351
M-W U-117.0 p-0.1545
K-W X2»lo.611 p-0.060
K-W X2«1.Q04 p-0.605
K-W X2-9.377 p-0.009
M-W U-118.0 p-0.1639
M-W U-117.0 p-0.1545
M-W U-1CO.O p«0.9495
All data values are log transformed mean valut. tor 18 grass plugs.
<-W - Kruskal-Wallis oneway ANOVA
M-W - Mann-Whitney U test
129
-------
-
0 000-
\/7,
%J
'^.
:^
'//A
-y/'s.
'///'/<
• ///A
f .' t .' I
Q"
J
>
o
0
-------
between Bitt ium and non-Bittiutn treatments of the same shading levels
(Table 6). There appears to be a trend towards a direct relationship
between the amount of phaeophytin a_ present and the degree of shading
(Fig. 6) although the observed differences were not statistically
different. At each shading level, phaeophytin ^ levels tended to be
lower in the presence of ]J. varium than when _B_. varium was absent.
DISCUSSION
Shading of marine angiosperms by epiphytes is a well known
phenomenon that has potentially harmful consequences for the host
plant (Sand-Jensen, 1977; Bcrura and Wium-Anderson, 1980). Although
some angiosperms possess chemical defenses against various fouling
species (Zapata and McMillan, 1979; Harrison and Chan, 1980) the role
of micrograzers may be equally or even more important in .uinimizing
fouling.
In our study, measurements of time integrated parameters (leaf
biomass, leaf area, and numbers of new shoots produced) provided a
clearer indication of periphyton-grazer effects on eelgrass growth
than did measurements which were more closely related to t'.ie fouling
community (periphyton pigment analyses, periphyton dry and ash free
dry weight, and raacroalgal weight). Experimental tanks (with _B_.
varium) exhibited an inverse relationship between chlorophyll £ (high
to low) and phaeophytin a_ (low to high) concentrations under
increasing levels of shade. These data imply chat under low levels of
light and in the presence of grazers, most of the periphyton biomass
is nonliving whereas under higher levels of 1'ght, the periphyton is
living and actively undergoing photosynthesis. T'.iese relationships
are less apparent in the absence of grazers (i.e. control tanks)
suggesting that grazing activity has some influence o.i the functioning
of the periphyton community.
The level of periphyton fouling (microalgae and associated
participates) as measured by dry weight and ash-free dry weight
appeared to be related to both the presence or absence of Bittium
varium and the level of shading. Periphyton weight is negatively
correlated with the level of shading in the presence of J5. varium
whereas in the absence of JJ. varium, periphyton weight and shading
level are positively correlated (see Fig. 3). Reasons for such
relationships remain unclear although it can be suggested that because
of the effects of one or both factors, the various treatments have
different epiphyte communities.
The level of raacroalgal fouling among treatments demonstrated no
identifiable relationship with control variables. The only treatment
showing significantly different values for this parameter was the high
shade Bittium treatments, the reason for which is also not apparent.
We have clearly demonstrated over a short period of time that Bittium
varium grazing can greatly improve plant vigor based on the time
integrated parameters which were measured. Not only did the total
Zostera marina biomass increase in the presence of grazers but the
fact that a greater number of shoots was produced by the experimental
131
-------
plants indicated that the vegetative reproductive capability of Z^.
marina was enhanced.
Results such as these have important implications for work being
conducted in seagrass habitats. Production and turnover estimates for
marine angiosperms may be closely linked to the degree of periphyton
fouling and consequently on the presence of absence of grazers which
rely on periphyton as a food source. Natural or human induced
perturbations which alter the structure and composition of micrograzer
populations might ultimately determine the distribution and abundance
of seagrass beds. Our findings support the contentions of Caine
(1980) who suggested that 2^. marina distribution along the west coast
VuSA) could be affected by the presence of periphyton grazing
arn phi pods. The elimination of Bittium varium from western Zosteta
marina beds in the Chesapeake Bay resulting from reduced salinities
during Hurricane Agnes probably contributed to the reduced aerial
coverage of eelgrass in the lower Bay.
This idea seems oven more plausible if the seasonality of grazer
activity, periphyton fouling and Z_. marina growth is considered.
Eelgrass is a perennial plant exhibiting distinct phases of seasonal
growth, presumably associated with environmental temperature
(Setchell, 1929). In the Chesapeake Bay, _Z. marina grows slowly
during the winter months when water temperatures remain below 6°C.
When water temperatures increase to above 10°C during the early spring
(March-May) Z_. marina grows rapidly until temperatures climb above
20°C early in the summer. Growth throughout the summer and early fall
months is minimal but is followed by a second, less dramatic period of
growth in the late fall (Oct.-Nov.) as temperatures drop. It is
during the spring growth peak that eelgrass produces seeds and
undergoes extensive vegetative growth. This is also the period of
increased epifaunal growth and activity. Bittium varium in
particular, which recruits late in the summer but remains relatively
inactive throughout the cold winter months, grows rapidly as
temperatures increase ir the spring (Marsh, 1976 and pc^o. c^s.). It
is during the important spring months and throughout the summer when
fouling and water turbidity are maximal that grazers such as _B. varium
could have their greatest impact on the si rvival and distribution of
eelgrass.
We have shown that under short term experimental conditions,
Zostera marina exhibits greater growth in the presence rather than
absence of the micrograzer, Bittium varium. Our results support the
hypothesis that recent declines of Zostera marina could be related in
part to the prior reduction of _B. varium populations in the lower
Chesapeake Bay. The fact that JJ. varium populations and Z. marina
beds on the eastern shore of the Bay did not experience severe
declines after the passing of Hurricane Agnes lends further support to
our hypothesis. Future research should focus both on long term
experiments to further substantiate our hypothesis and on examining
the role of other micrograzers in vegetated habitats.
132
-------
LITERATURE CITED
Adams, S. M. 1976. Feeding ecology of eelgrass fish communities.
Transactions of the American Fisheries Society 105:514-519.
Backraan, T. W. and Barilctti, D. C. IS,6. Irradiance reduction:
effects of standing crops of the eel^rass Zostera marina in a
coastal lagoon. Mar. Biol. 34:33-40.
Borom, J. and Wium-Anderson, S. 1980. Biotnass and production of
epiphytes on eelgrass (Zostera marina L.) in the (Jresund,
Denmark. Ophelia (Supplement) 1:57-64.
Brook, I. M. 1975. Some aspects of the trophic relationships among
higher consumers in a seagrass community (Thalassia testudinum
Konig.) in Card Sound, Florida. Ph.D. Dissertation, Univ. of
Miami, Coral Gables. 133 p.
Brook, I. M. 1977. Trophic relationships in a seagrass community
(Thalassia tesfjdinum), in Card Sound, Florida. Fish diets in
relation to macrobenthic and cryptic faunal abundance.
Transactions of the American Fisheries Society 106:219-229.
Brown, N. J. 1981. Reproductive biology and recreational fishing for
spotted seatrout, Cynoscion nebulosus, in the Chesapeake Bay
area. M.A. Thesis, William and Mary, Virginia. 120 p.
Burkholder, P. R. and Doheny, T. E. 1968. The biology of eelgrass.
Lament Geol. Observatory, Contribution 1227, 120 p.
Caine, E. A. 1980. Ecology of two littoral species of caprellid
amphipods (Crustacea) from Washington, USA. Mar. Biol.
56:327-335.
Cambridge, M. L. 1975. Seagrasses of southwestern Australia with
special reference to the ecology of Posidonia austral is Hook f.
in a polluted environment. Aquat. Bot. 1:149-161.
Carr, W. E. S. and Adams, C. A. 1973. Food habits of juvenile marine
fishes occupying seagrass beds in the estuarine zone near Crystal
River, Florida. Trans. Amer. Fish. Soc. 102:511-540.
Congdon, R. A. and McComb, A. J. 1979. Productivity of Ruppia;
seasonal changes and dependence on light in an Australian
estuary. Aquat. Bot. 6:121-132.
133
-------
Fer.chel , T. 1977. Aspects of Che decomposition of seagrasses. Hp.
123-145 ir± C. P. McRoy and C. Helfferich (.eds.), Seagrass
Ecosystems, A Scientific Perspective. Marine Science, Volume 4.
Marcel Dekker, Inc. New York and Basel.
Harlin, M. M. 1980. Seagrass epiphytes. Pp. 117-131 jjn R. C.
Phillips and C. P. McRoy (eds.), Handbook of S>>agrass Biology: An
Ecosystem Perspective. Garland STPM Press, New York and London.
Harrison, P. G. and Chan, A. T. 1980. Inhibition of the growth of
microalgae and bacteria by extracts of eelgrass (Zostera marina)
leaves. Mar. Biol. 61:21-26.
Heck, K. L. and Orth, R. J. 1980. Structural components of eelgrass
(Zostera marina) meadows in the lower Chesapeake Bay - decapod
crustaceans. Est. 3:289-295.
Hunter, R. D. 1980. Effects of grazing on the quantity and quality
of freshwater aufwuchs. Hydrobiol. 69:251-25V.
Jacobs, R. P. W. M. 1979. Distribution and aspects of the production
and bioioass of eelgrass, Zostera marina L. , at Roscoff, France.
Aquat. Bot. 7:151-172.
Kemp, W. M., Stevenson, J. C., Boynton, W. R., and Means, J. C.
(editors) 1981. Submerged aquatic vegetation in Chesapeake Bay:
its ecological role in Bay ecosystems and factors leading to its
decline. Final Report Chesapeake Bay Program, U.S. EPA,
Annapolis, MD.
Kikuchi, T. and Peres, J. M. 1977. Consumer ecology of seagrass
beds. Pp. 147-193 jji C. P. McRoy and C. Helfferich (eds.),
Seagrass Ecosystems, A Scientific Perspective. Marine Science,
Volume 4. Marcel Dekker, Inc., New York and Basel.
Klausner, S. D., Zwerman, P. J., and Ellis, D. F. 1974. Surface
runoff losses of soluble nitrogen and phosphorus under two
systems of soil management. J. Env. Qual. 3:42-46.
Klug, M. J. 1980. Detritus-decomposition relationships. Pp. 225-245
In: R. C. Phillips and C. P. McRoy (eds.), Handbook of Seagrass
TTology: An Ecosystem Perspective. Garland STPM Press, New York
and London.
Lascara, J. 1981. Fish predator-prey interactions in areas of
eelgrass (Zoscera marina). M.A. Thesis, William and Mary,
Virginia. 81 p.
Marsh, G. A. 1973. The Zostera epifaunal community in the York
River, Virginia. Chesapeake Sci. 14:87-97.
Marsh, G. A. 1976. Ecology of the gastropod epifauna of eelgrass in
a Virginia estuary. Chesapeake Sci. 17:182-187.
134
-------
Mukai, H., Aioi, K. and Ishida, Y. 1980. Distribution and biomass
of eelgrass (Zostera marina L.) and other seagrasses in Odawa
Bay, central Japan. Aquat. Bot. 8:337-342.
Munro, Robert E. and Perry, Math^w C. 1981. Distribution and
abundr.nce of waterfowl and submerged aquatic vegetation in
Chesapeake Bay. EPA Draft Report, Interagency Agreement Number
EPA-78-D-X0391. 177 p.
Nilsson, L. 1969. Food consumption of diving ducks wintering at
the coast of South Sweden in relation to food resources. Oikos
20:128-135.
Odgen, J. C. 1980. Faunal relationships in Caribbean seagrass beds.
Pp. 173-198 ir± R. C. Phillips and C. P. McRoy (eds.), Handbook of
Seagrass Biology: An Ecosystem Perspective. Garland STPM Press,
New York and London.
Orth, R. J. 1977. The effect of Hurricane Agnes on the benthic
fauna of eelgrass, Zostera marina, in the lower Chesapeake Bay.
In: J. Davis and B. Laird (coordinators). The Effects of
Tropical Storm Agnes on the Chesapeake Bay Estuarine System.
The Johns Hopkins University Press, Baltimore, MD, pp. 566-583.
Orth, R. J., and Moore, K. A. 1982. Distribution and aoundance of
submerged aquatic vegetation in the Chesapeake Bay: A scientific
summary. Special Report No. 259 in Applied Marine Science and
Ocean Engineering, Virginia Institute of Marine Science of the
College of William and Mary, Gloucester Point, VA, 42 p.
Orth, R. J. and J. van Montfrans. 1982. Interactions of resident
consumers in a temperate, estuarine seagrass community: Vaucluse
Shores, Virginia, U.S.A. Final Report. U.S. E.P.A. Grant No.
R805975 and VIMS S.R.A.M.S.O.E. No. 267, 238 p.
Phillips, R. C. 1972. Ecological life history of Zostera marina L.
(eelgrass) in Puget Sound, Washington. Ph.D. Thesis, 1972,
University of Washington, Seattle, Washington, 153 p.
Ryan, J. B., Riemer, D. N., and Toth, S. J. 1972. Effects of
fertilization on aquatic plants, water and bottom sediments.
Weed Sci. 20:482-486.
Ryer, C. H. 1981. The feeding ecology and trophic role of the
northern pipefish, Sygnathus fuscus, in a lower Chesapeake Bay
seagrass community. M.S. Thesis, 1981, William and Mary, VA.
Ryer, C. H. and Boehlert, G. W. (in press). Feeding periodicity,
daily ration, and the effects of temperature upon gastric
evacuation in the pipefish, Syngnathus fuscus. Env. Biol.
Fishes.
Sand-Jensen, K. 1977. Effects of epiphytes on eelgrass
photosynthesis. Aquat. Bot. 3:55-63.
135
-------
Setchell, W. A. 1929. Morphological and phenological notes of
Zostera marina L. Univ. Calif. Pub. Bot. 18:389-452.
Sokal, Robert R., and F. J. Rohlf. 1969. Biometry. The
principles and practice of statistics in biological research. W.
H. Freeman and Company, San Francisco.
Stolp, C. F., and Penner, D. 1973. Enhanced phytotoxicity of
atrazine-phosphate combinations. Weed Sci. 21:37-40.
Stoner, A. W. 1979. Species-specific predation on amphipod
Crustacea by the pinfish Lagodon rhomboides: mediation by
macrophyte standing crop. Mar. Bot. 55:201-207.
Stoner, A. W., and Livingston, R. J. 1980. Distributional ecoL .nd
food habits of the banded blenny Parachries fasciatus (Clini> 'e):
a resident in a mobile habitat. Mar. Biol. 56:239-2'»6.
Stevenson, J. C., and Confer, N. M. 1978. Summary of available
information on Chesapeake Bay submerged vegetation. U.S. Fish
and Wildlife Service, Office of Biological Services.
FWS/OBS-78/66. 335 p.
Thayer, G. W., Wolfe, D. A., and Williams, R. B. 1975. The impact of
man on seagrass systems. Araer. Scient. 63:288-296.
van Montfrans, J., Crth, R. J., and Vay, S. A. (in press)
Preliminary studies of grazing by Bittium varium on eelgrass
periphyton. Aquat. Bot.
Walker, C. R. 1959. Control of certain aquatic iA=eds in Missouri
farm ponds. Weeds 7:310-316.
Wetzel, R. L., Penhale, P. A., Webb, K. L., Orth, R. J., Merriner, J.
V., and Boehlert, G. W. (eds.), 1981. Functional ecology of
submerged aquatic vegetation in the lower Chesapeake Bay. Final
Report, U.S. EPA, Chesapeake Bay Program, Annapolis, MD.
Whitney, D. E. and Darley, W. M. 1979. A method for the
determination of chlorophyll a_ in samples containing degradation
products. Lirnnol. Oceanogr. 24:183-186.
Zapata, 0., and McMillan, C. 1979. Phenolic acids in seagrasses.
Aquat. Bot. 7:307-317.
Zimmerman, R., Gibson, R., and Harrington, J. 1979. Herbivory and
detritivory among gammaridean amphipods from a Florida seagrass
community. Mar. Biol. 54:41-47.
136
------- |