Estuaries and Coasts
Vol. 30, No. 3, p. 482~490
June 2007
Lucinid Clam Influence on the Biogeochemistry of the Seagrass
Thalassia testudinum Sediments
LAURA 1C REYNOLDS*,
PETER BERG,
and JOSEPH C. Z[E~L~N
U:,dversit7 ~f Vir~inia, Dqmrtme'nt q[Environmental Sciences, Clark Hall, 29t "UcCarmick Road, P. O.
Box 400123, Chartottesvg~, Virginia 22904-4123
ABSTRACT:
Luci~fid bivalves domhaate 1he infatma of tropical sea~'ass sedkaaents. While the effecI of sea~m'ass on lucinids
has been studied, the reverse effect has laa'gely been i.#aored. Lucinids can alter porewater ehenfisWy (i.e., incre~e porewater
nutrients by s-uspension feeding mad decrease porewater sttlfides by oxygen inia'odtlcfion mad bacterial oxidation}, which can
potenfi',dly change seagn'ass productivity and growth morphology. To obsma'e correlations betx~,een porewater ehenfi~taT mad
incixxid w e s e n e e , a field smwey and laboratory microcosm expeliment were conducted. Sun-ey smnpling sites with IllCi*,ids
had shgnificmatly lower sulfide and higher ammonimn concentrations than snmpling sites ~,ithout ludxfids. There ~aas no
difference in phosphate eoneent*ation among sampling sites. Both lucinid species ,tsed in the microcosm experiment (Ctena
orbieulata and Lueinesea nassula} significantly lowered mdfide eoncent*-ations in the sediment porm~'aler. Miel~oeosm and field
san'roy *~esults were ineorporaled into a sulfide budget. In seagrass sediments, luelnids remove 2-16% of the total sulfide
produced. Sulfide is a major stressor to both plants and animals in Florida Bay sediments; this removM may be important to
maintaining seagrass producltivily and health. Oxygen introduction into sediments by C. o,~i~/ata was estimated in a dye
experiment. C. orbic~lata were added to small tubes containing sieved m u d and incubated in a bath of seawater with
a R_hodamine WT. Rhodamine WT accumulation in the sediment was measured. A first order estimate showed that oxygen
introduction can account for less than 5% of C. orbicu/ata sulfide removal.
Introduction
lucinid bivalves are confined to the g a m m a subdivision of Protobaeteria (Durand a n d Gros 1996;
D u r a n d et al. 1996). These bacteria enzymatically
oxidize sulfides, which are t b u n d in a b u n d a n c e in
the sediment, to provide energy that is used to fLx
dissolved carbon dioxide into sugars. Lucinids have
a r e d u c e d tittering capacity and a r e d u c e d digestive
system, so these sugars are an i m p o r t a n t t o o d source
tor not only the bacteria but also for the bivalve
(Diste[ a n d Felbeck 1987; Cary et al. 1989; Le
P e n n e c et at. 1995; Talyor and Glover 2000).
T h e positive influence of seagrass on lucinid
bivalves is often credited ~ t l l tile close association
of the two (Jackson 1972, 1973; B,etsky 1976, 1978;
Barnes 199(3). Seagrasses prmdde m~ ideal habitat tbr
K~cinid bivalves. T h e dense root and rhizome mat
created by the grass protects fl~e bivalves f l o m
e n c o u n t e r i n g predators (Barnes 1996; Barnes and
H i c k m a n 1999; Jackson I972). For most relatively
immobile moE:~sks, seagrass sediments are harsh
em~ronments, because they are relatively reduced
and rich in sIfifide, which is toxic to most animals
( H e m m i n g a m~d Duarte 2001 ). Lucinids, unlike most
animals, thrive in sulfide rich sediments, so competition t)om other bivalves is reduced (Cavanaugh
1983; Barnes 1996; Barnes a n d H i e k m a n 1999). T h e
goal of this investigation is to demonstrate that not
only do seagrasses positively afteet lueinids, but these
bivalves can potentially positively affect seagrasses by
altering porewater biogeoehemistry.
Bivalves b e l o n g i n g to the family Lucinidae are the
most a b u n d a n t a n d diverse of the int~mnal mollusks
living within the sediments of tropical seagrass
meadows. These sediments are also the primary
habitat for shallow water lucinid bivalves (Moore
1968; Barnes 1996; J a c k s o n 1972, 1973). T h e
association between lucinid bivalves a n d seagrasses
is strong e n o u g h that the shells of dead lucinid
bivalves are used to age seagrass meadows a n d to
locate relic seagrass meadows (Barnes 1996;Jackson
1972, 1973; Bretsky 1976, 1978).
Lucinids are u n i q u e bivalves. C o m p a r e d to o t h e r
bivalves, they have unusual gills, mantile placations,
reduced labial palps, and lack an inhalant siphon.
They fiber the water collxmn b y building hollow
tubes to the sediment-water inteKace and ~tsing
ciliary currents to bring the water into their bodies
(Allen I 958; Jackson 1972; Taylor and Glover 2000).
Lucinids also have a symbiosis. AI1 species of
lucinids analyzed to date h a r b o r c h e m o a n t o t r o phic-endos?anbiotic bacteria living within their gills.
While e a c h lucinid species h a r b o r s only o n e
bacterial species, there is a diversity of bacterial
species a m o n g lueinids. All b a c t e r i a t b u n d in
*Corresponding author; current address: Romberg Tiburon
Center for Environmental Studies, San Francisco State University,
3152 Paradise Drive, Tibnron, California 94920; tele: 415/4357120; fax: 415/435-7120; e-mail: LKReynolds@alumni.vitginia.edu
9 2007 Estuarine Research Federation
482
Lucinid Clam Influence on Seagrass Sediments
Seagrass vegetated sediments typically have high
sulfide c o n c e a t r a t i o n s . Sulfides a c c u m u l a t e as
a standing stock in seagrass vegetated sediments as
an e n d p r o d u c t o f m i c r o b i a l d e c o m p o s i t i o n
(Fenchel and Riedel 1970; Fenchel et al. 1998)
and exit the system by reaction with oxygen to form
sultate ions, by b o n d i n g to hydrogen ions and
diffusing into the water c o l u m n as a gas, or b)
adsorbing to hea D metals such as iron or manga~
nese. The latter reaction is not significant because
tropical carbonate sediments, such as those in
Florida Bay, tend to be very low in these heavy
metals (Carlson et a[. 1994; Duarte et al. 1995;
Ersklne and Koch 2000; Chambers et al. 2001).
Lucinids cat, further increase the rate of sulfide
removal by two methods: bacterial oxidation .and
oxygen introduction. Since the bacteria liviag
within the gills of the bivalve enzymatically oxidize
sulfide to elemental sulfur or to sulfate in order to
create sugars (Distel and Feldbeck 1987), they
remove a finite a m o u n t of the available sulfide.
Lucinids can also reduce sulfide levels loy oxygen
introduction. Sultldes and oxygen cannot coexist
for very long. Oxygen wilI spontaneously react s~4tt~
sulfide to p r o d u c e sulfate until o n e of ihose
reactants is no longer available. Paradoxically, these
bivalves require both oxygen and sulfides to sur~4ve.
Lucinids obtain oxygen fi-om the water colmm~
using ciliary- currents to transport water t h r o u g h
hollow tubes (AJlen 1958; Jackson 1972). Not all
oxygen b r o u g h t into the tubes reaches the bivalves'
body. Bacterial symbionts c o n s u m e oxygen for
sulfide oxidation (Duplessis et al. 2004), and some
oxygen will naturally diftuse t h r o u g h the tube walls
into the sediments, where it may e n c o u n t e r and
react with sulfide. Oxygen introduced by bivalve
activity can also be c o n s u m e d in reactions such as
mineralization or nkritication.
T h e process of bringing water c o l u m n water into
the lucinid's b o d y is also used as a feedit~g
mechanism. White the bivalves get sugars from their
endosymbiotic bacteria, they still require o t h e r
nutrition, which they obtain ti-om organic material
suspended in the water column (i.e., suspension
tieeding; Distel and Felbeck 1987). O t h e r suspen
sion feeders living in seagrass meadows have been
shown to increase nntrients in the interstitial water
of the sediments (Reusch et al. 1994; Peterson and
Heck 1999, 2001a,b). Suspension feeding bivalves
transfer planktonic production in the water co]utah
to the sediments by means of fecal and pseudofecaI
production. Nutrient pools in the sedimen~ can be
increased by means of bivalve activity.
These biochemical changes (i.e., increased nutrients and decreased sulfides) have the potential to
increase seagrass productivity. Seagrasses tend to be
nutrient limited, and in Florida Bay, p h o s p h o r o u s is
483
typically the limiting nutrient (Fourqurean et al.
1992). Thalassia test'udi.~urn, the most a b u n d a n t
seagrass in Florida Bay, is more efficient at gaining
nutrients ti~om the sediment porewater as o p p o s e d
to the water column (Zieman 1982; McGlathery
2001). An addition of these nutrients or a transter
of these nutrients from the water c o l u m n to the
sediments should stimulate seagrass productivity.
This increase should allow the seagrasses to allocate
more resources to a b o v e g r o u n d as opposed to
b e l o w g r o u n d p r o d u c t i o n , increasing the aboveg r o u n d to belowground bhJmass ( H e m m i n g a and
Duarte 2001).
Sulfide is toxic to seagrasses and other plants
(Carlson et al. 1994; Koch and Erskine 2001; Borum
et al. 2005). Seagrasses have m e c h a n i s m s for
surviving in sulfide rich marine sediments. An e n d
p r o d u c t of photosynthesis is oxygen gas, which can
diffuse from the leaves t h r o u g h lacunae to the
roots. Some of that oxygen escapes t h r o u g h the
roots into the sediments where it reacts with and
reduces the a m o u n t of toxic sulfide in close
proximity to the seagrass tissue (Pederson et al.
1998). Although seagrasses have this mechanism,
sulfide at high but natural levels, can reduce
photosynthetic capacity a~d even induce die-off
( G o o d m a n et al, 1995; Koch and Erskine 2001;
Pederson et al. 2003). Reducing the ambient sulfide
levels further by means of bivalve activity reduces
this toxic stress o n the seagrasses. Lower sulfide
levels also allow the seagrass to allocate m o r e
resources to a b o v e g r o u n d as opposed to belowg r o u n d biomass, since they do not n e e d excess
b e l o w g r o u n d surtace areas lu
which to introduce
oxygen (Fig. 1).
STUDY SITE
Florida Bay is a shallow, triangular el-nba}aT,ent of
approximately 2,000 kin< It is b o r d e r e d by the
southern tip of the Florida peninsula on the north,
by the Florida Keys on the south and east, and is
o p e n to the Gulf of Mexico on the west. The bay
contains n u m e r o u s mangrove islands and meandering m u d banks subdividing the bay into many
distinct basins. The sediment typically consists of
carbonate muds. The most c o m m o n benthic cover
is seagrass. Three species of seagrasses are t b u n d in
Florida Bay-: Halodu~ w~vTghtii, &ringodium filiforme,
a n d T. testudinum. T. test udir~um is the most
a b u n d a n t (Zieman 1982).
Sunset Cove is located in the northeastern part of
Florida Bay very close to the main line of the keys,
adjacent to Key Largo (25~163
80~
Maximum water depth is no more than 2 m. Sunset
Cove is characterized by patches of hard b o t t o m and
patches of relatively- dense T, testudinum (742 shoots
m ~) with low densities of H. wrightii (95 shoots
484
L.K. Reynolds et al.
Fig. 1. Conceptual model describing the interactions in
seagrass vegetated sediments. The rectangular boxes describe
processes. The ovals describe standing stocks. Pluses and minuses
describe increases or decreases, respectively, in the standing
stocks symbol following. The model describes the following
interactions: the presence of seagrass increases lucinid survival,
which increases porewater nutrients and decreases porewater
sulfides. Both increased nutrients and decreased sulfides increase
the standing stock of seagrass. The following is an example of how
to read this diagram using the outside connection between
lucinids and porewater sulfides. Lucinid bivalvescreate burrows,
which increase the sediment water interface. The increase
sediment water interface allowsfor a greater diffusion and a larger
introduction of dissolved oxygen into the sediments. Dissolved
oxygen will react with porewater sulfides and decrease the
ambient pool. DO - dissolved oxygen; SWI - sediment
water interface.
m 2) in a very t h i n s e d i m e n t layer (10-50 cm;
R e y n o l d s u n p u b l i s h e d data).
R a b b i t Key Basin is l o c a t e d w i t h i n the w e s t e r n
c e n t r a l p o r t i o n o f F l o r i d a Bay ( 2 4 ~
8 0 % 0 ' 3 6 " W ) . It is f u r t h e r f r o m i n h a b i t e d l a n d
i n f l u e n c e t h a n S u n s e t Cove. M a x i m u m water d e p t h
is a g a i n n o m o r e t h a n 2 m. T h e b o t t o m is c a r p e t e d
by d e n s e T. testudinum (1146 shoots m 2; Reynolds
u n p u b l i s h e d data).
Methods
SURVEY
A p p r o x i m a t e l y biweekly, d u r i n g the s p r i n g a n d
s u m m e r o f 2003 (March u n t i l A u g u s t ) , at b o t h
S u n s e t Cove a n d R a b b i t Key Basin, twelve 20-ml
p o r e w a t e r samples were collected at a d e p t h of
15 c m u s i n g a s a m p l i n g p r o b e (Berg a n d McGlathery 2001). Each p o r e w a t e r s a m p l i n g site was m a r k e d
with a n u m b e r e d flag. T h e s a m p l e was filtered
t h r o u g h a 0.45-btm Millipore filter, a n d o n e 5-ml
s u b s a m p l e was fixed with 5-ml zinc acetate for
sulfide analysis. Samples were t r a n s p o r t e d o n ice to
l a b o r a t o r y facilities w h e r e they were analyzed for
sulfide, a m m o n i u m , a n d p h o s p h a t e c o n c e n t r a t i o n s .
S u l f i d e c o n c e n t r a t i o n was a n a l y z e d u s i n g t h e
m e t h o d o f C l i n e (1969). Sulfides were c o n v e r t e d
to zinc sulfide with zinc acetate. T h e zinc sulfide
t h e n r e a c t e d with a d i m e t h y l s o l u t i o n p r o d u c i n g
a b l u e color, which was analyzed s p e c t r o p h o t o m e t rically. A m m o n i u m c o n c e n t r a t i o n was also determined spectrophotometrically using a method
b a s e d o n the f o r m a t i o n of a b l u e color ( i n d o p h e n o l ) by the r e a c t i o n o f h y p o c h l o r i t e a n d p h e n o l i n
the p r e s e n c e of a m m o n i u m (Strickland a n d P a r s o n s
1972). P h o s p h a t e was d e t e r m i n e d s p e c t r o p h o t o m e t rically by r e a c t i n g a c o m p o s i t e r e a g e n t c o n t a i n i n g
m o l y b d i c acid a n d ascorbic acid, a n d t r i v a l e n t
a n t i m o n y reacts with p h o s p h a t e to p r o d u c e a b l u e
color ( S t a i n t o n et al. 1974). Directly a r o u n d each
f l a g - m a r k e d p o r e w a t e r s a m p l i n g site, o n e core
( d i a m e t e r = 7.6 cm, d e p t h = b e d r o c k or 50 cm
m a x i m u m ) was taken. T h e 12 cores were sieved i n 5cm s e g m e n t s t h r o u g h a 1-mm m e s h . All seagrass
tissue was discarded, b u t all live bivalves were kept,
identified, and measured.
O n c e d u r i n g the s a m p l i n g p e r i o d , t h r e e smaller
s e d i m e n t cores were t a k e n with a 60 cc syringe.
T h e s e s e d i m e n t samples were weighed, t h e n d r i e d
at 60~
a n d reweighed. T h e s e data were u s e d to
calculate s e d i m e n t water c o n t e n t . T h e water c o n t e n t
o f the s e d i m e n t was d e t e r m i n e d as the mass o f water
lost by d r y i n g divided by the mass o f the total wet
sample.
SULFIDE MICROCOSM EXPERIMENT
F i f t e e n t u b e s ( d i a m e t e r = 3.8 cm, d e p t h =
10 cm, c a p p e d at o n e e n d ) were filled with coarsely
sieved (1 cm) s e d i m e n t f r o m R a b b i t Key Basin.
T h e s e t u b e s were p l a c e d i n t o a t a n k of seawater
c o n t i n u o u s l y b u b b l e d with air a n d m a i n t a i n e d at
a t e m p e r a t u r e of a p p r o x i m a t e l y 28~ u s i n g aquari u m heaters. A l t e r a settling p e r i o d of at least 24 h,
the t u b e s were carefully r e m o v e d f r o m the water
bath, a n d a 2-ml s a m p l e o f the p o r e w a t e r was t a k e n
f r o m a d e p t h of 10 cm u s i n g a s a m p l i n g p r o b e
(Berg a n d M c G l a t h e r y 2000). R e m o v i n g the t u b e s
a s s u r e d t h a t water c o l u m n water was n o t i n t r o d u c e d
i n t o the sample. I n the lab, samples were filtered
t h r o u g h a 0.45-btm Millipore filter a n d analyzed for
sulfides u s i n g the m e t h o d of C l i n e (1969). Following initial sampling, the tubes were carefully
r e t u r n e d to the seawater bath. T h e t u b e s were
r a n d o m l y a s s i g n e d to o n e o f t h r e e t r e a t m e n t
groups: c o n t r o l , Ctena orbiculata, or Lucinesca nassula. C o n t r o l t u b e s were n o t m a n i p u l a t e d . O n e live
C. orbiculata or o n e live L. nassula was a d d e d to t h e i r
respective t u b e s a n d allowed to burrow. A l t e r a n
i n c u b a t i o n p e r i o d of 3 d, p o r e w a t e r was s a m p l e d
a n d analyzed for sulfide c o n c e n t r a t i o n u s i n g the
m e t h o d d e s c r i b e d previously. T h e s e d i m e n t u s e d i n
the e x p e r i m e n t was analyzed for water c o n t e n t .
Lucinid Clam Influence on Seagrass Sediments
Clams (%)
10
20
30
40
50
-5
E
vr
-10
121.
-15
ID
._E -20
O0
-25
/
J
J
J
-30
Fig. 9. Lucinid d e p t h distribution, The X axis describes the
p e r c e n t a g e of lueinids (Cte~a or&'cuhz~a and L'acir~esca r~as-~la)
found at the s e d i m e n t d e p t h represented on the y axis. n = 75.
T h e change in sulfide concentration was calculated as the initial sulfide concentration of each tube
subtracted fi-om the final concentration, The mean
rate of concentration change was calculated as the
quotient of the mean change and the incubation
period. The actual c o n s u m p t i o n rate of each lucinid
bivalve was d e t e r m i n e d by subtracting the mean
sulEcle ciaange in the control tubes {?ore the mean
change in the lneinid experiment tubes.
The ettect of the bivalves on a 1 • 1 X 0 . 1 5 m
block of natural sediment was estimated for the two
surveyed basins: Rabbit Key Basin and Sunset Cove.
The d e p t h of 15 cm was chosen because 90% of the
lucinids f o u n d were at that depth or shallower
(Fig. 21. This estimate was based on several assumptions. Sulfide p r o d u c t i o n was assumed to be spatially
h o m o g e n o u s . Lucinid c o n s u m p t i o n rates of sulfide
were assumed to be constant with time and with
various c o n d i t i o n s (i.e., various water c o l u m n
nutrient levels, various porewater sulfide levels)
and similar to those consumption rates measured
in the microcosm experiment. To put these rates in
perspective they were c o m p a r e d with published
rates of sulfide p r o d u c t i o n t h r o u g h sulta_te reduction (Pollard a n d Moriarty 1991; Holrner a n d
Nielson 1997).
OXYGEN TRANSPORT DYE F.XPERIMENT
Eight tubes (dimneter - 2.5 cm, depth - 15 cm,
c a p p e d at one end} were filled with coarsely sieved
(1 cm) sediment. These robes were placed in a m b
containing seawater continuously bubbled with air
and maintained at a temperature o~~approximately
28"C using aquarium heaters. Atler a settling period
of approximately 24 h, the tubes were randomly
assigned to one of two treatment gioups: control or
C. orbicu&ta. Controls were not manipulated. In the
485
C, orbicugata tubes, one live C. or~iculata was placed
o n the surface and allowed to burrow and acclimate
f o r 94 h. C o n c e n t r a t e d R h o d a m i n e WT dye
(200 inl) was addect to file water column, resuhing
in a water c o l u m n with a concentration of 3%
Rhodamine \gs
Alter 5 d of incubation, the tubes were removed,
covered with para_filrn, and fi-ozen. Once completely
f r o z e n , the tubes were s e g m e n t e d into 2-cm
sections. The sediment ti-om each section was
allowed to thaw and placed into a centriihge tube
and centrifuged o n the highest setting for 10 min.
T h e resulting s u p e r n a t a n t was pulled off with
a syringe, filtered t h r o u g h a 0.45-pro Millipore filter,
a n d anal)led spectrophotometricaliy tbr Rhodamine W2" concentration.
The a m o u n t of Rhodamine %rI" introduced to the
sediment by one (2 orbicutata was d e t e r m i n e d by
subtracting the bulk a m o u n t of R h o d a m i n e WT
f o u n d in the control tubes fi-om the bulk a m o u n t of
R h o d a m i n e WT f o u n d in the lucinid tubes. The
bulk a m o u n t of Rhodamine WT was calculated by
multiplying the measured porewater concentration
of dye by the volume of porewater present. The
a m o u n t of water c o l u m n intrusion due to the
bivalve activity was d e t e r m i n e d by dividing the
a m o u n t of Rhodamine WT added to the sediments
by the experimental water column concentrauon.
Results were depth integrated to estimate a total
a m o u n t of introduced water due to one bivalve.
Using the assumption that lucinids react similarlyin the natural environment, the results were scaled
u p to a ]-m ~ area within a natural basin (Sunset
Cove) ia Florida Bay. D e p t h of influence was
estimated to 15 cm. This assumption was supported
by the field survey data as well as the dye experiment
data. The total water c o l u m n intrusion was determined by multiplying the water c o l u m n intrusion
of one experimental C. ~)rbic~data by the density o~ C.
orbicMata in Sunset Cove determined in the ~ield
survey. The a m o u n t of oxygen introduction was
d e t e r m i n e d by multiplying the average water colu m n dissolved oxygen concentration by the volume
of water column water introduced, it was assumed
that all of this oxygen chemically reacted with the
sulfide in the sediment, and the a m o u n t of sulfide
used in this reaction was d e t e r m i n e d stoichiometrically. Since the sediment characteristics of Sunset
Cove are known, a concentration change was also
determined.
Results
SURVEY
In Sunset Cove, the lucinid population is dominated by C. orbic~tata (80 m -2 SE
13, n = 83). In
Rabbit Key Basin, two species of lucinid bivalves
486
L.K.
Reynolds
et al.
80
160
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120
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E
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o
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Published
Production
25
~a
rO
20
u
15
'e
10
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<
0
6
::t.
~-
Ctena
Lucinesca
orbiculata nassula
Fig. 4. Lucinid influence on porewater sulKtde concentration:
Microcosm experiment results. The chart describes the sulKtde
change in small tubes incubated u n d e r one of the following
treatments: c o n t r o l +1 C'tena orbiculata, or +1 L u c m ~ c a nas~-ula.
The first bar represents published sulfide production rates for
Yhalas~ia te~tudinum sediments scaled down to d~e siee of the
experimental tubes, Decreases in both [ucinid robes are signiftcar~tiy different from the control increases, but the changes ir~ the
C ortdc~ulata and L. )zass'Ma tubes were not different from each
other. The error bars represent standard error The symbols
around the published so~ide production bar represent the range
of values.
O
E
E
Control
5
O
.~,
r-
4
l u c i n i d s as o p p o s e d to cores w i t h o u t l u c i n i d s
( S u n s e t Cove a n d Rabbit Key Basin p < 0.1), a n d
t h e r e was n o c o r r e l a t i o n b e t w e e n l u c i n i d bivalve
p r e s e n c e a n d p h o s p l l a t e c o n c e n t r a t i o n (Fig~. 3).
(D
=
3
O
L)
2
63
o_
9"1
1
a_
0
O
r-
L
Prese nce
SULFIDE MEgOCOSM EXPERIMENT
Absence
Fig. 3. Lucinid influence on pocewater: Survey results. The
bar" graphs display the results from a 2003 survey of two Florida
Bay basins: Rabbit Key Basin and Sunset Cove. The bars marked
presence reflect porewater concerUrafions in cores that contained
lucinids, and ~he bars marked absence reflect porewa~er
concentrations in cores without lucinids. Error bars represent
standard errors.
d o m i n a t e the p o p u l a t i o n : C. orbicutata (25 m -2 SE =
12, n - 56) a n d L. ~ass,~ga (30 m ~ SE - 10, n =
56). A t h i r d species, Anodontia alba, is f o u n d rarely.
All l u c i n i d bivalves were f o u n d b e t w e e n 0 a n d 25 c m
s e d i m e n t d e p t h , with m o s t individuals b u r r o w i n g to
a d e p t h of 5 to 10 cm (Fig. 2).
T h e d i f f e r e n c e in p o r e w a t e r sulfide, a m m o n i u m ,
a n d p h o s p h a t e c o n c e n t r a t i o n s b e t w e e n cores where
bivalves were f o u n d o r n o t f o u n d was a n a l y z e d u s i n g
a >test. Sulfide c o n c e n t r a t i o n was lower i n cores
with L u c i n i d s as o p p o s e d to cores w i t h o u t l u c i n i d s
( S u n s e t Cove p < 0.05; R a b b i t Key Basin p < 0.1).
A m m o n i u m c o n c e n t r a t i o n was h i g h e r i n cores with
Sulfide c o n c e n t r a t i o n i n c r e a s e d in t h e experim e n t a l c o n t r o l tubes, while t h e sulfide c o n c e n t r a t i o n i n e a c h o f t h e l u c i n i d t u b e s d e c r e a s e d (Fig. 4).
Decreases i n b o t h l u c i n i d tubes are significantly
d i f f e r e n t tYom c o n t r o l t u b e s (p < 0.05), b u t t h e
c h a n g e s i n the C. arbi~data a n d L. nassuh~ t u b e s
were n o t differen~ f~*om o n e a n o t h e r . T h e s e d i m e n t
v o l u m e o f the e x p e r i m e m a l t u b e s was ] ] 5 ml. U s i n g
a s e d i m e n t wet d e n s i t y of 1.4 g m l -~ ( T e e t e r 2002),
t h e weight of the s e d i m e n t was calculated to b e
215 g, a n d u s i n g t h e water c o n t e n t of t h e s e d i m e n t
(70%, SE - 0.5, n - 4), the weight o f t h e p o r e w a t e r
was 149 g. U s i n g a seawater d e n s i t y o f 1.02 g m l :,
t h e v o l u m e of the p o r e w a t e r in e a c h t u b e was
137 nil. Molar an-tount o f c h a n g e was d e t e r m i n e d by
m u l t i p l y i n g the c o n c e n t r a t i o n c h a n g e by the volu m e o~ porewater. C o n s u m p t i o n rate was c a l c u l a t e d
as t h e increase in c o n t r o l t u b e s s u b t r a c t e d i r o m t h e
decrease i n the C orbiculata a n d the L. r~assuta
tubes. M e a n daily c o n s u m p t i o n of sulfide for o n e C
orbiculata was 23 pmol. M e a n daily c o n s m n p t i o n for
o n e L. nassuta was 18 gmol.
I n S u n s e t Cove (C. orbic/ulata density o f 80 m -2)
total l u c i n i d c o n s m n p t i o n is 1.9 m m o l m -~ d -a. I n
Lucinid Clam Influence on Seagrass Sediments
487
Discussion
-2
m
-
SURVEY
-
E
.9% -4
t-
"ID
r-O
1t4
-8
E
-10
Control
-12
t
J C. o r b i c u l a t a
-14
0,0
0,5
1.0
1.5
2.0
2.5
Rhodamine Concentration (%)
Fig. 5. Porewater and water co/umo interactions via Ctena
orbiculata: Dye e x p e r i m e n t results The chart describes the
R h o d a m i n e WT concentration change of tubes containing either
0 or 1 C. orbiculata. All tubes were incubated for 5 d in a b a t h of
seawater with a 3% R h o d a m i n e WT concentration. At a d e p t h of
9 cm, the difference between the corttro[ and C orbiculata tubes
b e c o m e s insignificant. Error bars repcesent standard error.
Rabbit Key Basin ( C. orbicutata density 96 m ~ and L.
nassula density 28 m -~) total lucinid consunlption is
1,1 mmol m -2 d-L The range of" sulfate reduction,
d e t e r m i n e d f r o m a literature review, was 1260 m m o l
m -~ d-: (Pollard and Moriarty 1991; Holmer and Nielson 1997). These sulfide p r o d u c t i o n
rates were used for both Sunset Cove and Rabbit
Key Basin (ambient sultide concentration 102 and
104 gM, respectively) and resulted in an estimate of
11-59 m m o l m ~ d : of sult]de that is removed
f i o m the system. That means that sulfide removal
due to lucinid activity-is between 2% and 16% of the
total sulfide removal in both systems.
OXYGEN TRANSPORT DYE E ~ E R I M E N T
In the experiment, o n e C c~rb,culata introduced
0.7 gl of R h o d a m i n e WT per day-. Since the
R h o d a m i n e WT concentration in tile water column
was 2.8%, bivalves introduced water at a rate of
2.5 ml d -~ (Fig. 5).
In a 1 • 1 X 0.12 m Mock of Sunset Cove
sediment (C c/rbiculata density = 80 individuals
m ~), bivalves introduce 180 ml of water into the
sediments. Assuming an average dissoh'ed oxygen
c o n c e n t r a t i o n of 6.0 mg 1 ~, lucinid activity in
Sunset Cove can add an increase in dissolved
oxygen of 35 ~m~oI d L Using natural Sunset Cove
sediment characteristics, that results in an 0.21-FM
increase in sediment dissolved oxygen per day-.
Assuming that all of the introduced oxygen reacts
with sulfide a n d converts it to sulfate, sulfide
concentration will decrease 0.1 ] btM d -s,
Sediment sulfide concentration was lower in areas
that were in close proxhnity to ludnids, suggesting
that bivalve activity reduces porewater sulfides.
There are problems affecting the observation of
sulfide removal. Sulfide is a very transien~ molecule.
Measuring tile ambient pool might not accura.tely
depict alterations made by Iucinids. Accurately
measuring sulfide oxidation would reveal a better
u n d e r s t a n d i n g o f lucinid eftect on p o r e w a t e r
sulfide. Measuring suH]de pools is much easier
and less time consuming than measuring sulfide
oxidation. Despite the complications with these
measurements and the problems associated with
surveying a complex system, it is apparent that the
presence and activity of lncinids is correlated to
some extent with decreased sulfide concentrations
in the sediment (Fig. 3). 3dtering the sulfide levels
even to a small degree in the systems has many
implications for the seagrasses in these sediments.
In both systems, the presence of lncinids was
weakly associated with increased a m m o n i u m concentrations in the sediment (Fig. 3). The alterations
in porewater a m m o n i u m c o n c e n t r a t i o n appear
somewhat less than the increases f o u n d with mussels
in seagrass beds (Reusch et al. 1994; Peterson and
Heck 2001a,b). A possible explanation for this
discrepancy is that lucinids rely to some degree on
the bacteria living in their gills fbr food and have
a r e d u c e d filtering capacity (Cary et al. 1989; Le
P e n n e c et al. 1995). The small changes can still be
detected since a m m o n i u m is relatively labile in the
sediments of Florida Bay. Florida Bay- is typically
considered p h o s p h o r o u s limited (Fourqnrean et al.
1992), so nitrogen additions are not taken up
quickly. Lucinids a n d seagrass exist in other systems
that are not p h o s p h o r o u s limited, and in other
areas of the world, this interaction between lucinids
and sediment a m m o n i u m levels n i g h t be more
significant. This nitrogen addition might be underestimated. Nitrogen a d d k t o n is occurring in close
proximity to oxygen introduction (via diffusion
t h r o u g h hollow tubes). Some of the a m m o n i u m
m i g h t be nitrified to nitrate. Nitrate was n o t
measured in this survey, since nitrate is typically
considered below the detection level in Florida Bay
sediments.
While this study f o u n d no evidence of hlcinid
influence on sediment porewater phosphate concentradons, in p h o s p h o r o u s limited systems, an
addition of phosphate will be immediately taken up
by plants a n d bacteria in the sediments. The
carbonate muds of these systems are able to sorb
p h o s p h a t e and remove it {rum the porewater pool.
It is not u n e x p e c t e d that slight phosphate additions
4.88
L.K. Reynolds et al.
to the sediment due to suspension feeding are
difficult to detect, especially since lucinid suspension feeders have a reduced filtering capacity and
presumably introduce only a small a m o u n t of
p h o s p h o r o u s to the sediments.
3O
'7,
25
-o 20
r
SULFIDE MESOCOSM EXPERIMENT
The microcosm experiment data show that the
bivalves C. or&culata and L. "nassula do have the
potential to considerably alter the sulfide concentration of sediment porewater in controlled conditions (Fig. 4). Scaling these results up assumes that
lucinids act similarly in the manipulated sediment
conditions of the microcosms and in the natural
environment. These are bold assumptions, but the
results of the smwey support and help to validate the
results of the microcosm experiment.
~qfile lucinid activity is certainly not the only
m e t h o d for r e m o v i n g toxic sulfide f r o m the
environment, it does appear to be important. These
bivah,es may be more important to total sulfide
removal than the 2-16% calculated, since sulfide
p r o d u c t i o n was most likely overestimated. This
overestimate is supported by the controls from the
microcosm experiment. Without bivalves, sulfide
accumulated at a rate of 2 m m o l m 2 d ~. \4Chile
acknowledging that this is a conservative estimate of
sulfide production, using this value as the sulfide
p r o d u c t i o n rate, bivalves remove a liberal estimate
of 16-32% of the total sulfide removed fi-om the
system.
W i t h o u t sulfide removal by lucinid bivah.'es,
sulfide would either accumulate or be removed by
another process. The latter appears unlikely to
compensate for lucinid sulfide removal since in the
laboratory microcosm experiment, sulfide accumulated in the sediments. High sulfide accumulation
has been linked to seagrass decline (Carlson et al.
1994; Koch and Erskine 2001; Borum et al. 2005).
Removal by bivalves potentially has a positive effect
on seagrass productMty and health.
These bivalves are not only important in reducing
the total a m o u n t of sulfide; the specific location of
these two species makes them even more beneficial
to seagrasses. The average depth of these bivalves is
7-9 cm. This d e p t h is above the bulk of the
rhizosphere, closer to the basal meristem area of
T. testudi~zum where sulfide intrusion into the tissues
is most detrimental and most likely to initially
induce die-off (Borum et al. 2005).
OXkGEN TRANSPORT DXE EXPERIMENT
The depth integrated bulk calculation estimates
that one C. orbiculata introduces 0.4 pmol O 2 d
into the sediment (Fig. 6). The microcosm experiment showed that one C. orbiculata can remove
-6 15
E
E
00
"ZD
2D
~,,
5
Oxygen Introduction
Bacterial Activity
O
~3
0
Bulk Calculation Sulfide Demand
Fig. 6. Oxygen introduction estimates. TEe figure sEows tee
estimates of oxygen introduction via Ctena orbiculata burrows. The
second bar shows the a m o u n t of introduced oxygen needed to
remove 13.6 ~tmol of sulfide. This value was estimated as potential
sulfide removal due to lucinid activity using a microcosm
experiment. The pie chart displays the percentage of sulfide
removal due to bacterial activity in the lucinid's gills as opposed to
oxygen introduction via burrows.
14 btmol of sulfide per day. If all of that sulfide was
removed by oxygen, one C. orbiculata indMdual
would need to add 28 ,umol 0 2 d a in addition to
the oxygen that it introduces far its own respiration
and that oxygen which is c o n s u m e d by bacterial
endosymbionts. The estimate of C. orbiculata oxygen
introduction projects a much smaller oxygen introduction. This estimate of oxygen introduction
suggest that oxygen introduction can only remove
about 1.5% of the sulfide removed by lucinid
activity. One must assume that most of the sulfide
removal is achieved by means of bacterial oxidation
or by another m e t h o d (Fig. 6).
The calculation is subject to some measurenlent
errors. The approach used R h o d a m i n e WT diffusion to approximate dissolved oxygen diffusion. The
dfffusivities of the two c o m p o u n d s are not equal.
R h o d a m i n e WT diffusivity is 2.3 X 10 6 cm2s
(Glud and Fenchel 1999), and oxygen diffusivity is
approximately 1.9 X 10 5 cm2s ~. Since the diffusivity of oxygen is over 8 times larger than the
diffusivity of R h o d a m i n e WT, oxygen diffusion
should be considerably larger than that of Rhodamine ~rF.
The sulfide removal achieved by lucinid burrows
might be underestimated for other reasons as well.
This study only addresses sulfide removal by oxygen
i n t r o d u c e d into the sediments. Sulfide will be
diffusing out of the sediments into the bivah'e tube
as well. From the bivalve tube, the sulfide can
diffuse into the water column. When the bivalve
tubes contain dissolved oxygen, that sulfide can also
react to form sulfate.
Lucinid Clam Influence on Seagrass Sediments
X~'~lile t h i s o x y g e n i n t r o d u c t i o n v i a l u c i n i d b u r rows is s m a l l a n d may- n o t b e t h e p r e d o m i n a n t
m e t h o d f o r s u l f i d e r e m o v a l , it m a y still b e important. O x y g e n t y p i c a l l y e n t e r s t h e s e d i m e n t b y m e a n s
of diftilsion fiom the overlying water column. That
o x y g e n is d e t?le~ed i n t h e t o p f e w m i l l i m e t e r s o f
sediment by bacterial respiration (Hemminga
and
D u a r t e 2 0 0 1 ) . C. or~ic~ulaga b u r r o w s t o a n a v e r a g e
d e p t h o f 7.5 e m (Fig. 2). T h e s e b i v a l v e s a r e introducing oxygen in small amounts to a deeper
depth. This creates or enhances a sediment complex that while mostly anoxic has small transient
patches of oxygenated sediment.
Small oxygenated zones can have a large effect on
the sediment
environment.
Microbes are much
more efficient decomposers when they use ox) gen
as o p p o s e d t o s u l f a t e as a t e r m i n a l e l e c t r o n a c c e p t o r
( A l o n g i 1 9 9 8 ) . M o r e energy- is p r o d u c e d , a n d m o r e
o f t h e a v a i l a b l e c a r b o n is a s s i m i l a t e d . W h i l e s e a g r a s s
meadows are some of the most productive systems
in the world, most of the production
is p a s s e d to
h i g h e r t r o p h i c levels o n l y via t h e d e t r i t a l f o o d w e b
(Zieman
1982). More efiicient assimilation
by
b a c t e r i a will r e s u l t i n m o r e e f f i c i e n t t r m a s f h r o~
energ T up the ii)od chain.
S u l f i d e d?a~amics i n s e a g r a s s s y s t e m s a r e h i g h l y
s t u d i e d ( C a r l s o n e t al. 1 9 9 4 ; K o c h a n d E r s k i n e 2 0 0 1 ;
B o r n m e t al. 2 0 0 5 ) , b u t m o s t s t u d i e s o f s u l f i d e
dynamics do not incorporate
l u c i n i d sult3de r e moval. This study demonstrates that these lucinids
r e m o v e a s i g n i f i c a n t a m o u n t o f s u l f i d e fi-om t h e s e
sediments, and in order to get the tull and accurate
understanding
of sulfide dynamics, the actixities of
these bivalves must be considered.
ACKNOWLEDGMENTS
We wonld like to acknowledge the field assistance of j. Burr, T.
Frankovich, A. Schwarzschild, and B. Wolfe, and to thank B.
Ha?den and K. McGiathery for their valuable cornments~ This
projee~ was f~mded by the Jot~es Everglades Research Fund at the
University e3fVirginia.
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Received, June 13, 2006
Revised, November 21, 2006
Accepted, January 11, 2007