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

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                                                         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

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                                      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 (»•»!)

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                      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

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                               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

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                            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.

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                                 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

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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.

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                                                    '--  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

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                              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

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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*.

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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.

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     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.

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     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,

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     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.

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                                                  76° 00'
Figure 3.  Locations of  topographic  quadrangles  in Virginia which were
           covered with  aerial photography  for SAV in 198U.

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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

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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.

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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

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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



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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

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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

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                           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.

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                  /-
                               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.

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          SECTION II




INTERACTIVE EFFECTS OF LIGHT,




    EPIPHYTES AND CRAZi-RS

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                                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

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                                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

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                              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

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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

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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

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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

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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.

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      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

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                  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

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     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

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     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

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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

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63

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64

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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

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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

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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

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     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

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                  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

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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

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                   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

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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

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I
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     cephalus), milkfish  (Chanos chanos).  and  the  ten-pounder  (Elops
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                                    78

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                      \
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                                   85

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                    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

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                                                               -
                                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

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-
                                                 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

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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

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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

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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

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(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

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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

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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.

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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.

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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.

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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

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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

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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

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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

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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

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  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

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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

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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

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                            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

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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

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Wilson, D. P.  1970.  The  larvae of Sabellaria spinulosa and their
     settlement behavior.  J. Mar. Biol. Ass. U.K. 50:33-52.
                                  107

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                 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

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                                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

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                                               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

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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

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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

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                                           60
113

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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

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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

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;                   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

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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

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                                                       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

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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

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                                                             - -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

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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

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                   1/1
                   o
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                   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

-------
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126

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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

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                                       MEPIl-M   HIGH
LOW

 SHADING LEVEL


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fi • S**v>* ' tf%'^-
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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

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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

-------
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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

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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

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                                     136

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