Aquatic Botany, 25 ( 1 9 8 6 ) 47 - -61 Elsevier Science Publ i shers B.V., A m s t e r d a m - - P r in ted in The N e t h e r l a n d s

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BIOMASS, PRODUCTION AND DECOMPOSITION OF A DEEP WATER SEAGRASS, HALOPHILA DECIPIENS OSTENF.

M I C H A E L J O S S E L Y N

Tiburon Center for Environmental Studies, San Francisco State University, PO Box 855, Tiburon, CA 94920 (U.S.A.)

M A R K F O N S E C A 1

Department of Environmental Sciences, University of Virginia, Charlottesville, VA 22903 (U.S.A.)

T H O M A S NIESEN and R A L P H L A R S O N

Department of Biological Sciences, San Francisco State University, San Francisco, CA 94132 (U.S.A.)

(Accep t ed for pub l i c a t i on 11 Apri l 1986)

A B S T R A C T

Josse lyn , M., Fonseca , M., Niesen, T. and Larson, R., 1986. Biomass, p r o d u c t i o n and d e c o m p o s i t i o n of a deep wa te r seagrass, Halophila decipiens Ostenf . Aquat. Bot., 25: 47- -61 .

Beds of Halophila decipiens Ostenfe ld , a t d e p t h s b e t w e e n 15 and 27 m, were s tud ied using a s a t u r a t i o n diving faci l i ty ( N U L S - I : H y d r o l a b ) in the Salt River s u b m a r i n e c a n y o n of f St. Croix, US Virgin Islands. D i s t r ibu t ion , b iomass , p r o d u c t i o n and d e c o m p o s i t i o n of t he seagrass were s tud ied dur ing two miss ions in J u n e 1983 and July 1984. Biomass of H. decipiens ranged f rom 5 to 12 g m -2 dur ing s u m m e r m o n t h s . Due to the rapid t u r n o v e r of H. decipiens, biomass d i s t r i bu t i on was closely re la ted to c o n c u r r e n t l y measu red g rowth rates. P r o d u c t i o n es t imates using oxygen p r o d u c t i o n t e c h n i q u e s or r h i z o m e e longa t ion were similar ranging b e t w e e n 100 and 500 mg C m -2 day -1. D e c o m p o s i t i o n of H. decipiens occur red rapidly , losing over 50% of its or iginal weight in a p p r o x i m a t e l y 3 days. U n d e r m o s t cond i t ions , weight loss f rom l i t te r bags occur red more rapidly t h a n n i t rogen loss. H. decipiens exh ib i t s a n u m b e r of a d a p t a t i o n s to a low a m b i e n t l ight e n v i r o n m e n t , inc luding a high ra t io of leaf t issue to n o n - p h o t o s y n t h e t i c t issue, low leaf area index to reduce se l f - shad ing , high t u r n o v e r leaf mater ia l and the abi l i ty to rapid ly co lonize sandy b o t t o m s w h e n l ight c o n d i t i o n s are sui table .

I N T R O D U C T I O N

Most of the work on seagrass communit ies has been focused on wide- spread, shallow water systems (den Hartog, 1977). These include Zostera

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beds in temperate waters, Posidonia meadows of the Mediterranean and the Thalassia and Halodule beds of the tropics and subtropics (McRoy and Helfferich, 1977). Frequently, the studies are conducted in waters less than 10 m deep. However, in clear waters, seagrasses can extend to depths of 85 m or more (den Hartog, 1970). In the tropics, Halophila decipiens Ostenfeld is often the dominant macrophyte in either shallow, turbid water or relatively deep water. Along with other members of the genus, it is considered a colonizer species and characteristic of disturbed environments (Birch and Birch, 1984). A few studies have been completed on related species (Williams and McRoy, 1982; Wahbeh, 1983, 1984), but relatively little is known about the ecology of H. decipiens, especially in depths below 10 m.

Our s tudy utilized the US National Oceanic and Atmospheric Admin- istration underwater habitat system (NULS-1) located in the Salt River submarine canyon off the island of St. Croix, US Virgin Islands (Fig. 1). The canyon extends from a shallow embayment and barrier reef on the north shore of St. Croix to depths over 3500 m. In the area of the study, the canyon floor is approximately 100--150 m wide and is surrounded by well-developed coral reefs on either side. The canyon floor itself is relatively flat and largely composed of medium-grained sand to silt. The H. decipiens beds are located between 8 and 40 m. During the summer months, H. decipiens is the dominant macrophyte on the canyon

4 Salt River Bay <~> A

~ ~~..ii!~ ' ~,.. rj,

Fig. 1. Map of St. Croix (A) and the Salt River Bay and Submarine Canyon (B). Shaded area indicates study site.

49

floor and it contributes significantly to down-canyon export of detritus (Josselyn et al., 1983). The objectives of the overall s tudy were to determine the production and decomposit ion cycles within the seagrass beds, the utilization of these unique, deepwater seagrass beds by invertebrates and fishes in this coral reef/seagrass complex, and the role of physical and biological disturbance on the longevity and distribution of H. decipiens. This report covers the growth, biomass and decomposit ion of H. decipiens as measured during two saturation diving missions (23--29 June 1983 and 26 July--1 August 1984).

METHODS

Environmen tal measurements

An in-situ monitoring station was established during the first mission (1983) approximately 30 m from the NULS-1 Habitat (Hydrolab) at a depth of 15 m. The station held a spherical quantum meter, temperature thermister, conductivity cell, dissolved oxygen probe and a pH electrode which were monitored by instruments within the habitat. Readings were taken at regular intervals throughout the mission and the probes calibrated on the first and fourth day. On the second mission (1984), irradiance was the only variable monitored on a diel basis. Instead of an in-situ station, irradiance measurements were taken from the surface to determine var- iability at various locations in the canyon. Sediment samples were col- lected by divers in the seagrass beds and in adjacent barren areas for lab- oratory analyses to determine silt--clay fraction, mean particle size and percent organic matter.

Biomass and morphometrics

Collections of above- and below-ground biomass were made in both 1983 and 1984 using a stratified sampling method. A 100-m 2 sampling stratum was established at each of three depths (15, 21 and 27 m). This stratum size was chosen since it was empirically observed to cover the range of sea- grass densities. The sampling strata were arbitrarily located on the canyon floor away from the guidelines used by divers for orientation. Randomly- chosen coordinates were used to locate ten 100-cm 2 plots within the sam- pling strata. All plant material was harvested from within the plots and sorted into two fractions: leaves (above-ground matter) and roots and rhizomes (below-ground matter), washed in dilute HC1 to remove any carbonate encrustation, and dried at 100°C for 24 h. Morphometric meas- urements (number of leaf pairs, size of leaves, length of branches and rhi- zome, number of fruits) were taken on 6 rhizomes from each stratum. Regression equations were developed to describe the distribution of biomass by component (leaf, root, rhizome) relative to distance from the rhizome

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apical meristem. The leaf area index was calculated from average leaf density times surface area of an individual leaf.

Photosynthetic rate, growth and production

Growth was determined from increases in rhizome length of tagged plants over a 4--6 day period during both missions. One hundred individual rhizomes at 15, 21 and 27 m were tagged with numbered aluminium tape placed behind the terminal leaf pair of each rhizome. Rhizomes wire tagged in the order encountered. Initial and final length measurements were record- ed.

Production was estimated from growth measurements, terminal bud density and morphometric relationships. Rhizome elongation was entered into the regression equations developed from morphometric measurements to provide an estimate of biomass increase for individual rhizomes during the obser- vation period. The biomass increase was multiplied by the terminal bud density and divided by the number of days in the observation period to determine daily productivity per area.

Measurements of oxygen production within 1-1 plastic containers (domes) inverted over H. decipiens were used to determine photosynthet ic rates. Domes were equipped with stirring bars and sampling vents. Intact plants (including roots and loosely-attached sediment) were removed from the bed and placed in domes that were sealed on the bot tom with plastic discs. The discs eliminated oxygen product ion by benthic diatoms which quickly developed on the sand when covered by a dome. Respiration was measured in two opaque domes. Two transparent domes containing no plant material were used to correct for respiration in the water column. Water samples were collected from the domes every 90--120 min using a 10-ml syringe. During sample removal, replacement water was allowed to enter from an opposite vent. Samples were immediately returned to the habitat and were kept submerged until measured. Within 30 min of collection, oxygen concentration was determined in a sealed 7-ml chamber using a tightly- fitting oxygen probe. The chamber contained a stirring bar and all meas- urements were taken at ambient temperature. The oxygen meter was cali- brated daily by ti tration methods.

Photosynthet ic rates measured by oxygen production were computed on a dry weight basis and then multiplied by areal biomass to give an estimate of daily production per unit area of canyon floor. Mean daily net oxygen production attributable to the H. decipiens was calculated from the net increase within the dome divided by the dry weight of the enclosed plant material and by the time of the incubation. Appropriate corrections were applied if clear domes wi thout H. decipiens showed either an increase or decrease in oxygen due to either phytoplankton productivity or bacterial and faunal respiration, respectively. Biomass estimates from the sampling described above were used to estimate net oxygen production on an areal basis.

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The biomass of attached epiphytes on H. decipiens leaves was estimated from pigment extractions of successive leaf pairs on individual runners or rhizomes. The primary epiphyte on H. decipiens is a red alga, Wrangelia bicuspidata B¢rg. Because of their small size, they are difficult to separate from the leaves, and accurate weights of the two components were not determined, Pigment analysis was used to separate the abundance of each component for various leaf sizes. While chlorophyll would be associated with both the seagrass and the epiphyte, phycobilins are found only in red algae. Successive leaf pairs were removed from rhizomes collected at 15 and 27 m. The size of leaves was recorded and one leaf of a pair was placed in 90% acetone and the other in water. Chlorophyll was extracted in acetone by grinding and phycobilins in water by alternate freezing and thawing. For phycobilin determination, leaf pairs of equivalent age from different runners were combined to provide a sufficient quanti ty of pigment for measurement. Samples were centrifuged and absorbances at 665 nm for chlorophyll and 565 nm for phycobilins were corrected for turbidity using absorbance at 750 nm. Using an empirical relationship between leaf length and dry weight, a relative pigment content based on weight was determined for each leaf pair for the two pigments.

Decomposition

During the 1984 mission, live plant material was harvested from 21-m depth and was sorted into leaves, and roots and rhizomes. These components were weighed and placed in mesh bags with 1.1-mm openings. The bags were placed at 21 m under two t reatment conditions; either buried beneath 5 cm of sand or attached to a line lying loose on the bot tom. Decomposition was examined under these treatments to mimic the disturbance pathways which H. decipiens commonly encounters in Salt River: burial and up- rooting. The seagrass was separated into above- and below-ground com- ponents to examine the relative reaction of each part to the decomposit ion process. Triplicate samples were harvested after 0, 3, 7 and 31 days, dried at 50°C, and the remaining dry weight compared to estimated initial weight using a wet :dry weight ratio. Ash content was determined from combustion and total carbon and nitrogen measured using a Carlo-Erba model 1106 elemental analyzer. Data were compiled as percent original dry weight (weight loss) and percent original N on an ash-free dry weight basis.

RESULTS

Environmental conditions

During the June 1983 mission, temperature and conductivity remained stable at 28°C and 583 × 103 pS (350/00), respectively. The pH varied slightly and ranged between 8.29 and 8.47 with no consistent diel pattern. Irradiance

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. o

10C

~a . . . . 2:3 25 27 29 26 28 30

June 1983 July 1984

Fig. 2. Ixradiance (circles) and dissolved oxygen (triangles)measured at 15 m in the Salt River Submarine Canyon for both missions. Dissolved oxygen was not measured in July 1984.

and dissolved oxygen both exhibited diurnal maxima (Fig. 2). On days with clear skies, irradiance at 15 m usually exceeded 450 ~E m -2 s -I at solar noon, but cloudy weather or turbid water sometimes reduced irra- diance to below 100/~E m -2 s -I. Increases in dissolved oxygen lagged slightly behind maximal irradiance. Lowest dissolved oxygen concentrations oc- curred just before dawn and maximum levels I h past solar noon. Daily dissolved oxygen increases were usually I ppm.

In July 1984, diel irradiance on the bottom was determined for three locations in the submarine canyon: at the head (15 m), middle (18 m) and near the lowest limit of the H. decipiens growth (27 m). In general, turbidity was greatest at the head and diminished towards the deeper portion of the canyon. Total daily irradiance for both sampling periods indicated marked differences between days due to cloudy weather and water tur- bidity (Fig. 3). On 26, 27 and 30 July, turbidity reduced irradiance at 15 m to values close to or less than observed at 18 m.

Sediments on the canyon bottom were composed primarily of calcareous sand with a mean size ranging from 0.30 to 0.43 ram. Organic matter in

15m

2 1 17 18rn • 27m

"111 1 cl~J£ 10. &

24 26 28 I 26 27 June 1983 I

28 29 30 31 July 1984

Fig. 3. Total daily irradiance in the Salt River Submarine Canyon. Measurements taken at 3 depths during the July 1984 mission.

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the s ed imen t s was b e t w e e n 3 and 5% of the d r y weight . In general , m e a n par t ic le size increased w i th d e p t h (a m e a n of 0 . 3 3 - - 0 . 5 3 ram) as did organic m a t t e r c o n t e n t (a m e a n of 3 .7- -5 .0%). Organic m a t t e r c o n t e n t wi th in sea- grass beds was sl ightly higher t h a n in bare sand areas (a m e a n of 4.7 vs. 3.9%).

Biomass and morphometrics

Biomass var ied wi th d e p t h and b e t w e e n years (Table I). A l t hough sig- n i f i can t d i f fe rences were obse rved , no cons i s t en t p a t t e r n wi th d e p t h or y e a r was a p p a r e n t . All b iomass - re la ted measures decreased wi th d e p t h in 1983 , b u t were r educed at 15 m in 1984 , and were s o m e w h a t higher at 21 and 27 m. F ru i t p r o d u c t i o n was m u c h lower in 1984. The ra t io of above- (leaves) to b e l o w - g r o u n d ( roo t s and rh i zomes ) t issue averaged 1.06 +- 0 .24 (S.D.) .

Leaves were b o r n e o p p o s i t e l y at each node and were near ly ident ical in shape. Leaves were m i n u t e at the end o f the r h i z o m e and reached a b o u t 2.5 c m in length w h e n m a t u r e . Average leaf surface area ( fo r b o t h sides of a single leaf) and s tandard dev ia t ion was 1.86 -+ 1.12 c m 2. L ike b iomass , the dens i ty of leaf pairs and leaf area index decl ined wi th d e p t h in 1983. Bo th decl ined (like b iomass ) at 15 m in 1984 , bu t were similar in b o t h years at 21 and 27 m.

F e w e r frui ts were obse rved in Ju ly of 1984 than J u n e 1983 indicat ing

TABLE I

Biomass and population data for Halophila decipiens in the Salt River Canyon during June 1983 and July 1984. Mean and standard deviation are given.

Depth (m)

15 21 27

Biomass (mg dry wt 100 cm -2) 1983 105 (46) 58 (39) 47 (26) 1984 50 (66) 120 (97) 73 (83)

Number of leaf pairs (100 cm -~) 1983 46 (18) 27 (19) 18 ( 9 ) 1984 19 (17) 33 (22) 21 (14)

Leaf area index 1983 1.72 1.02 0.68 1984 0.70 1.22 0.78

Fruits (100 cm -2) 1983 10.4 (6.5) 9.3 (8.0) 1984 1.0 (1.1) 1.4 (1.7)

7.1 (4.2) 1.5 (1.7)

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TABLE II

Relationships between length of plant rhizome and accumulative dry weight for various tissues in Halophila decipiens. Dependent variable is accumulative weight in mg for plant tissue specified and independent variable is length in cm. Relationships given for plant material excluding lateral branches and including lateral branches

Independent variable ~ r 2 Best fit equation

Rhizomes w/o branches 0.955 Y = -0.2 + 0.2X (a) with branches 0.952 Y = -0.2 + 0.3X (b)

Roots w/o branches 0.936 Y = 0.1 + 0.3X (c) with branches 0.914 Y = -0.06 + 0.4X (d)

Leaves w/o branches 0.817 Y = 0.4 + 0.3X (e) with branches 0.762 Y = 0.2 + 0.4X (f)

Total w/o branches 0.962 Y = 0.3 + 0.SX (g) with branches 0.956 Y = -0.1 + 1.0X (h)

1 w/o = without.

tha t e i ther frui t dehiscence m a y occur by the end of June or frui t pro- duc t ion was low in 1984. F r o m samples col lected in June 1983, the average n u m b e r o f seeds p r o d u c e d per fruit and the s tandard devia t ion was 35.3 -+ 12.3.

The m o r p h o m e t r i c relat ionships be tween mass o f d i f ferent p lant parts and rh i zome length all showed high corre la t ions (Table II).

This indicates a high degree o f u n i f o r m i t y in the g rowth pa t te rn o f these plants, even at d i f ferent depths . Using these regressions, g rowth in mass was calculated f rom the increase in length o f rh izome de te rmined f rom the tagging m e t h o d .

Growth measurements and oxygen production

During the first mission, 50 rh izomes were tagged at each dep th , bu t faunal a t tacks on the metall ic tags and rapid degrada t ion o f s tored samples l imited final sample numbers to less than 15 at each dep th . A to ta l o f 300 rh izomes were tagged in the second mission and preservat ion o f samples in cold, fresh water until measu remen t , resulted in a five-fold increase in observat ions. R h i z o m e e longat ion rates at 21 and 27 m did no t di f fer sig- n i f icant ly be tween years (Table III) . G r o w t h decl ined greatly at 15 m in 1984, so tha t it was comparab le to g rowth at 21 and 27 m dur ing tha t same year. This relat ionship was cons is tent wi th the more f r equen t per iods o f tu rb id i ty observed at the head o f the c a n y o n in 1984. On some days, to ta l daily irradiance was higher at 21 than at 15 m {Fig. 2). The mean

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TABLE III

Rhizome elongation rates for tagged Halophila decipiens in Salt River canyon at three depths. Mean and standard deviation are given

Year Depth N Duration Tot~ increase Dailyincrease (m) (days) (cm) (cm day-')

1983 15 11 4 4.52(2.35) 1.13(0.59) 21 14 4 1.13 (0.84) 0.28 (0.21) 27 10 4 1.70 (0.81) 0.43 (0.20)

1984 15 62 4 1.58 (1.13) 0.40 (0.28) 21 67 4 1.43 (0.83) 0.28 (0.16) 27 53 5 1.89 (1.07) 0.38 (0.21)

TABLE IV

Net oxygen production rates for Halophila decipiens placed beneath plastic domes, corrected for respiration by enclosed water. Reported mean (standard deviation) over 9-h period during daylight

Date Depth Net 02 production (m102 g-' h -1)

27 June 83 15 2.60 (0.74) 28 June 83 15 5.18 (1.89)

27 3.24 (2.08 29 June 83 15 8.26 (1.08) 29 July 84 15 0.45 (0.33) 30 July 84 15 1.20 (0.93)

dai ly r h i z o m e e longa t ion ra te (weighted for uneven rep l ica t ion) for all d e p t h s in 1983 was 0 .59 c m d a y - ' and fo r 1984 was 0 .33 cm day -1.

Ne t o x y g e n p r o d u c t i o n ranged f r o m 2 .60 to 8 .26 ml 02 g d ry we igh t - ' h -1 in 1983 and 0 .45 to 1 .20 ml 02 g d r y we igh t -~ h - ' in 1984 (Table IV). T h e lower values o b t a i n e d in 1984 c o r r e s p o n d wi th lower r h i z o m e elon- ga t ion ra tes at 15 m. P h o t o s y n t h e t i c o x y g e n p r o d u c t i o n was lowes t on days w h e n m a x i m u m ir radiance was be low 300 pE m -2 s -~ due to c l oudy skies or w a t e r t u rb id i ty . No ne t o x y g e n p r o d u c t i o n was obse rved dur ing pe r iods o f t he d a y w h e n i r radiance was less t h a n 100 pE m -2 s -~.

C h l o r o p h y l l c o n t e n t o f leaves on a we igh t basis showed an initial increase wi th the age o f the leaf at b o t h 12 and 27 m (Fig. 4). C h l o r o p h y l l c o n t e n t decreased a f t e r the e ighth leaf pair at 12 m and a f t e r the f o u r t h leaf pair a t 27 m. Signif icant d i f f e rences in leaf c h l o r o p h y l l c o n t e n t b e t w e e n d e p t h s did n o t o c c u r unt i l a f t e r the s ixth leaf pair , w i th d e e p e r w a t e r p lan t s showing a m o r e rap id decl ine in p igmen t . Red algal p i g m e n t ( p h y c o e r y t h r i n ) c o n t e n t in e p i p h y t e s on leaves also increased wi th successive leaf pairs, bu t did n o t show a decl ine wi th leaf age as did ch lo rophy l l . In general ,

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J 6E " ,12m T , A----.27rn t I ~ . ~ t

° r -- "x\ 1~ ~ 4C E /'r• ~r ~- chlorophyll (27m1 "K . ~ z ~ ~ . ~phycobilin (27m,

sc TX f ' [" er ~ 2C / / ~ J / / ~ phycobilin (12m)

lC ~ ~ ~A~-- - -

Loaf pair

Fig. 4. Ch lo rophy l ] and phycoe ry th r i n levels fo r sequent ia l leaf pairs a long H. decipiens runner. Plants were f r o m 12 and 27 m.

epiphyte development (as measured by phycobilin content) in shallow water occurred simultaneously with leaf pigment increase, whereas in deeper water epiphyte development came after the peak in leaf pigment content.

Decomposition

Decomposition of plant components in mesh bags varied by component (leaf vs. root and rhizome) type as well as with burial. Leaf material dem- onstrated a decrease over time in both the nitrogen content and dry weight (ash-free) initially present (Fig. 5A). Within 2--3 days, all components lost half their initial weight. All material under buried conditions exhibited a slightly greater weight loss. Roots and rhizomes on the surface regained some weight after 3 days.

¢A) ( B ) (C)roots & rhizomes 100 ~combined L & RR leaves ~ R R A

.~ .~ LA z

5C - ! .E

- -=LB a~ 1C LBI

= . . . . . . . . . . . . . . . . . . . . . . . 0 3 7 0 3 7 0 3 7

time (days)

Fig. 5. (A) Percent weight loss of plant material held in litter bags. RRA: roots and rhizomes above sediment surface; LA: leaf material above sediment surface; RRB: roots and rhizomes buried; LB: leaf material buried. (B) Percent loss of original nitrogen based on ash-free dry weight from litter bags for leaf material placed above and below the sediment surface. (C) Percent loss of original nitrogen based on ash-free dry weight from litter bags for root and rhizome material placed above and below the sediment surface.

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Using both dry weight loss from the litter bag and the nitrogen content of the remaining litter, the net loss or gain of nitrogen from the litter bags can be determined (Fig. 5B and C). Leaves under buried conditions ex- hibited a more cont inuous and greater net loss of nitrogen than those held at the surface. Buried leaves lost 75% of their original nitrogen in 3 days and remained at this level to Day 7. Leaves held on the surface lost only 35% of their original nitrogen after 7 days. In contrast, roots and rhizomes under both surface and buried conditions showed a 40% decline in net nitrogen after 3 days. The loss was largely regained by Day 7 {Fig. 5B and C).

DISCUSSION

Irradiance on the b o t t o m of the Salt River canyon is influenced by weather condit ions and water mass movement from the Salt River em- bayment . In the shallower port ions of the canyon, irradiance generally reaches between 400 and 700 ~E m -~ s -1 on clear days. Cloudy weather can reduce total daily irradiance by over half that of sunny days. This is especially critical below 27 m where light levels generally do not exceed 350 gE m -2 s -1 even on clear days. Cloudy weather can reduce maximum irradiance to less than 150 ~E m -2 s -1 at 27 m. In addition, when strong onshore winds occur, b o t t o m currents carry turbid water from the Salt River embayment to the canyon (Josselyn et al., 1983) and result in a gradient of high turbidi ty near the head of the canyon, clearing towards deeper water as the nearshore water is diluted by oceanic water. During the 1984 mission, b o t t o m irradiance was frequently greater in the middle of the canyon than in the shallower depths towards the shore.

Halophila decipiens exhibits a number of morphological and structural adaptations to the variable and low light environment. Microscopic ex- amination of leaves showed several features related to maximizing light- harvesting capacity, including thin cell walls, densely packed chloroplasts and simple leaf anatomy of only two cell layers. Another adaptation is the reduced biomass allocated to non-photosynthet ic tissue. The ratio of above- to below-ground biomass for H. decipiens is 1.06. This is higher than that generally reported for other seagrasses such as Zostera and Thalassia which have extensive below-ground tissue (Zieman and Wetzel, 1980), but less than that reported for another deep water seagrass, H. stipulacea (Forssk.) Aschers. (Lipkin, 1979}. The structure of the seagrass communi ty can also be an adaptation to low light. Leaf area index (LAD is a measure of the surface area of photosynthet ic tissue to bo t tom area. A low LAI reduces self-shading. Among seagrass communit ies studied, H. decipiens has the lowest LAI (McRoy and McMillan, 1977; Lipkin, 1979).

Growth of epiphytes on seagrass leaves also contr ibutes to shading and reduces photosynthet ic rates of the seagrass. Wrangelia bicuspidata was the major epiphyte observed on H. decipiens during this study. Microscopic observation of leaves showed that the epiphyte spores were germinating

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by the second pair of leaves. In shallow water (15 m), epiphyte abundance increased rapidly as the leaf aged, but had little apparent effect on the chlorophyll levels in the leaf, perhaps due to greater light availability. In deeper water (27 m) chlorophyll levels in the leaves decreased at the same time as epiphyte abundance increased, suggesting that shading by epiphytes may influence senescence of seagrass blades. From growth measurements of tagged shoots, approximately 4 new leaf pairs were produced over 5 days at 15 m and 3 leaf pairs over 5 days at 27 m. Therefore, the age at which leaf senescence (start of chlorophyll loss) began was similar at the two depths: 6--7 days. Johnstone (1979) observed a similar response in Enhalus acoroides (L.f.) Royle in which the photosynthetically useful life of a blade was between 10 and 25 days due to epiphyte shading. In H. decipiens, the high turnover rates for photosynthet ic tissue result in less oppor tuni ty for epiphytes to develop and maximize light availability to the seagrass.

Biomass, productivity, and decomposit ion patterns of H. decipiens are generally similar to those of other Halophila species. The differences which do occur are related to its morphology and deep water habitat. The biomass of H. decipiens reported for Salt River canyon is slightly less than that re- ported by Lipkin (1979) for Halophila stipulacea for the Red Sea. However, it is several orders of magnitude below the biomass reported for other seagrass communities in shallow water (McRoy and McMillan, 1977). The difference between deep and shallow water communities is primarily due to the reduced accumulation of biomass in perennating rhizomes, low LAI index and high turnover rate.

Production by H. decipiens in the Salt River canyon is low compared to other tropical seagrass beds, but similar to those of shallow, temperate regions (McRoy and McMillan, 1977). The difference appears to be due primarily to the low biomass per area as the photosynthet ic rates are within the range observed for other species. The overall mean for H. decipiens at 15 m under a range of light conditions was 3.54 ml 02 g-1 h-1 Buesa (1975) determined a photosynthet ic rate of 11.55 ± 6.28 ml O: g-1 h-1 for H. decipiens, the highest of several seagrasses he studied. Using C-14 methods, Williams and McRoy (1982) found that the uptake of C-14 by H. engelmanni Aschers. was 2--4 times greater than by either Thalassia testudinum Banks ex K6nig or Syringodium filiforme Kiitz. Although the application of oxygen production methods to seagrasses has been crit- icized (McRoy and McMillan, 1977; Zieman and Wetzel, 1980), they may be useful for small species such as H. decipiens. Halophila leaves are only two cell layers thick and although a lacunar system is present (Roberts and McComb, 1984), storage of oxygen produced during photosynthesis is reportedly minimal (Wahbeh, 1983). Our method placed the entire plant within the chamber, utilized a relatively large chamber volume, and was stirred at sampling times. All of these factors would contribute to a greater diffusion of oxygen from the seagrass into the water column. The

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TABLE V

Estimates of areal productivity based on oxygen production measurements and growth measurements

Year Estimate using oxygen production data

(1) (2) (3) (4) Mean 02 Production Average Biomass Areal O: Production a Productivity b ( m l O : g - ' h - ' ) ( g d r y w t l O O c m -~) (mlO:m-2day - ' ) (gCm-~day - ')

1983 4.82 .070 303 0.520 1984 0.83 .081 60.5 0.103

Year Estimate using growth elongation measurements

(5) (6) (7) Terminal shoot Areal growth c Productivity d (cm shoot-' day- ') (cm 100cm -2 day- ') (gC m-: day- ')

1983 0.59 4.63 0.238 1984 0.35 2.75 0.144

aCol. 1 x Col. 2 × 9 h daylength (duration of dome experiments). bUsing a photosynthetic quotient of 1.2. CCol. 5 multiplied by average terminal shoot density: 7.85. dUse value of Col. 6 in regression equation (h) Table II and multiply by carbon content of 52.5%.

s imi lar i ty b e t w e e n p r o d u c t i v i t y e s t ima tes based on r h i z o m e e longa t ion ra tes and o x y g e n p r o d u c t i o n suggest t h a t o x y g e n s torage in the lacunal sy s t em is m i n i m a l in this species (Table V).

G r o w t h of H. decipiens is d i rec ted t o w a r d rapid spread ing over the bot - t o m , n o t in the a c c u m u l a t i o n o f b iomass . R h i z o m e e longa t ion ra tes range b e t w e e n 0.3 and 1.1 cm d a y -1. With an average o f 8 t e rmina l shoo t s per 100 cm -2, an individual p l an t can rap id ly cove r areas d i s tu rbed b y animals or s to rms . T h e t u r n o v e r t i m e (b iomass divided by p r o d u c t i v i t y ) for H. decipiens ranges b e t w e e n 10 and 30 days which is cons ide rab ly fas te r t han the 65 days e s t ima ted fo r H. stipulacea (Wahbeh , 1984) . Rap id t u r n o v e r t ime is a charac te r i s t ic o f o t h e r co lon iz ing seagrass species (Virns te in , 1982) .

T h e d e c o m p o s i t i o n of H. decipiens in l i t ter bags had a pa t t e rn similar t o t h a t obse rved fo r o t h e r seagrasses (Fenche l , 1977; Klug, 1980) , bu t the ra te o f d e c o m p o s i t i o n was fas te r t han fo r any o the r seagrass s tudied. The we igh t loss d a t a fo r H. decipiens (Fig. 5b) had a s imilar p a t t e r n to t ha t f o u n d by b o t h Wahbeh and Mahasneh (1985) and K e n w o r t h y and T h a y e r (1984) e x c e p t t ha t the losses occur red wi th in 3--7 versus 4 0 - - 3 0 0 days . A d i rec t c o m p a r i s o n wi th the d e c o m p o s i t i o n da t a on H. stipulacea is d i f f icul t due to the subs tan t ia l ly d i f f e ren t p r e - t r e a t m e n t used b y Wahbeh and Mahasneh (1985) . T h e y co l lec ted a l ready dead and d e t a c h e d blades and dried t h e m at 105°C pr io r to p l a c e m e n t in l i t ter bags. This wou ld resul t in cons iderab le

60

pre-leaching of soluble carbohydrates and result in a slower percent de- crease in original weight.

Buried leaves lost nitrogen from the litter bag at a similar rate to weight loss. However, leaves on the surface and root and rhizomes under surface and buried conditions showed a conservation of nitrogen relative to the loss of carbon-containing organic matter. This suggests that either microbial enrichment or nitrogen fixation was occurring. The root and rhizome mass balance data were similar to the pat tern exhibited by Zostera marina L. buried in high organic matter sediment (Kenworthy and Thayer, 1984).

H. decipiens extends deeper into the ocean than most other vascular plants. Its adaptations to this environment include maximizing leaf tissue to non-photosynthet ic tissue, low leaf area index which reduces self-shading, high turnover of leaf material conducive to reducing epiphyte shading, and the ability to rapidly colonize sandy bo t toms when light conditions are suitable. Although its biomass is relatively low compared to other sea- grass communities, H. decipiens constitutes a unique communi ty at these depths. Turnover of plant material is rapid, bo th in terms of biomass pro- duct ion and decomposi t ion rates. During summer months, H. decipiens is one of the major sources of organic matter to the depths below 30 m (Josselyn et al., 1983). In an otherwise barren sandy substratum H. decipiens provides both a potential food source and a habitat structure for small invertebrates and fish.

ACKNOWLEDGMENTS

The authors greatly appreciated the field assistance of Susan Danek, William Pence, James Kusz of San Francisco State University and the sup- por t staff at the HYDROLAB mission base in St. Croix, USVI. The West Indies Labora tory of Fairleigh Dickinson University provided access to laboratory instrumentation. Jud Kenwor thy and Kathleen Cheap of the National Marine Fisheries Service, Beaufort , NC provided laboratory and data reduction assistance. Critical reviews by Mr. Kenwor thy and Dr. Susan Williams, Science Director of the HYDROLAB facility in St. Croix greatly improved an earlier draft of the paper. This research was supported by a contract from the US Depar tment of Commerce, NOAA Undersea Research Office for NULS-1 missions 83-8 and 84-9. This is contr ibut ion no. 8 from National Underseas Research Program, U.S. Dept. of Commerce. Additional support was provided by San Francisco State University.

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