FAU Institutional Repository

http://purl.fcla.edu/fau/fauir

This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute.

Notice: ©1985 Elsevier. The final published version of this manuscript is available at www.elsevier.com/locate/ecss and may be cited as: Short, F. T., Davis, M. W., Gibson, R. A., & Zimmermann, C. F. (1985). Evidence for phosphorus limitation in carbonate sediments of the seagrass Syringodium filiforme. Estuarine, Coastal and Shelf Science, 20(4), 419‐430. doi:10.1016/0272‐7714(85)90086‐1 Evidence for Phosphorus Limitation in Carbonate Sediments ofthe Seagrass Syringodiurnfiliforrne

F. T. Short", M. W. Davis", R. A. Gibson" and C. F. Zimmermann" "Jackson Estuarine Laboratory , UNH, RFD no. 2, Adams Pi, Durham, N H 03824, bMarine S cience Center, OSU, Newport, OR 97365 and

Keywords: ph osphorus; seagrasses; nutrients; limitation; carbonate sediments; geochemistry; Syringodium fi lifo rme; Bahamas

The seagrass Sy ringodium filiforme was examined in an ecological analysis of plant nutrient requirements and nutrient resource availability. Assessment of the sediment geochemistry in a San Sal vador Island seagrass bed indicated that phosphorus was not readily accessible. to the plants. Ammonium regeneration in the fine-grained carbonate sediments was high, and interstitial con centra tions averaged ca. 100 11M while phosphate replenishment to interstitial water was low, and concentrations were generally less than 2 11M . Analysis of the seagra ss leaf tissue content (C: N : P = 1390 : 47 : 1, atomic wt) suggested that nitrogen and ph osphorus were both depleted relative to carbon . However, this high N : P for S. fi lifo rme and th e low concentration of phosphate available in th e interstitial water established the likelihood that plant acquisition of phos ph orus was limited. The finding ofhigh root biomass relative to leaf biomass in th ese seagrass beds corroborates this evidence by depicting a method of plant adaptation that increases nutrient absorptive root surface area.

Introduction

Seagrasses comprise a group of submerged marine angiosperms found worldwide in shallow tropical and temperate oceans (D en Hartog, 1970). Three seagrass species, Th aIassir: testudinum Banks ex K on ig, Syringodium fil iforme Kiitzing, and Halodule wrightii Ascherson, dominate the tropical western North Atlantic and the Caribbean coastal envi ronments. The ecology of S. fi liforme, manatee grass, has received little attention although it is the dominant seagrass in some regions (Phillips, 1960; Thompson, 1978) and may be the preferred food source for herbivorous fish (T ribble, 1981) and turtles (Fenchel et al ., 1979). Early studies of seagrass distribution outlined the descriptive ecology of S. filiforme along the Florida coast (Phillips, 1960; Strawn, 1961). The metabolic acti vity and light-controlled primary production of S. fiIiforme have been examined (Buesa, 1975; Will iams & McRoy, 1982), as have salinity and temperature tolerances (M cM ahan, 1968; McMillan, 1979). However, no att ention has

been given to the nutrients important for plant growth or to nutrient cycling in S. filiforme beds, particularly in the carbonate sediment environment. Research on nutrient resource availability in both tropical and temperate seagrasses has established a notion that considerable reserves of phosphorus are available in seagrass sediments (Patriquin, 1972; McRoy & McMillan, 1977; Entsch et al., 1983). Recently, studies of seagrass nutrient cycling have emphasized the importance of nitro gen (Capone & Taylor, 1977; Iizumi et al., 1980, 1982; Kenworthy et al., 1982; Short, 1983a, b). Phosphorus has been given only secondary consideration and until now has not been examined as a limited resource. The geochemistry of phosphate in carbonate sediments indicates that mineral regeneration is rapid although phosphate does not accumulate in the interstitial water (Rosenfeld, 1979). Low concentrations of phosphate, relative to ammonium, have been observed in a number of studies of carbonate sedimentary interstitial water (Rosenfeld, 1979; Gaudette & Lyons, 1980; Hines & Lyons, 1982). These low dissolved phosphate concentrations may be a result of adsorption of phosphorus on carbonate sediment grains, diagenetic formation of apatite, or replacement of calcium carbonate with a phosphate-rich phase (Bern er, 1974; DeKanel & Morse, 1978; Gaudette & Lyons, 1980). Interstitial water samples from carbonate sediments of seagrass beds also con tained low phosphate concentrations, although additional phosphate was extractable from the sediment particles (Patriquin, 1972). The present study investigated aspects ofsediment geochemistry and the ecology ofS. filiforme in the carbonate sediments of an oligotrophic lagoon. This analysis assessed seagrass biomass, plant chemical constituents, plant growth rates, nutrient resource availability, and regeneration ofnutrients in the sediments ofthe seagrass bed.

Site description and methods

A seagrass bed of Syringodium filiforme was sampled in Graham's Harbor, a shallow semi-enclosed lagoon at the north end of San Salvador Island, Bahamas (F igure 1). This lagoon averages 1-2 m in depth and is protected from oceanic swells and storms by fring ing islands and coral reefs , a configuration that allows extensive flushing of the seagrass bed with oligotrophic Atlantic Ocean water while dissipating most ofthe wave energy. A S. filiforme bed located on the west side of Cut Cay was selected for study because it represented a monospecific stand of seagrass in an area of uniform environmental conditions i.e., constant water depth, relatively uniform current flow, and fine-grained carbonate mud. Seagrass plant samples were collected in triplicate with a 16 em diameter plexiglass core sampler to a depth of30 cm in th e sediment and by clipping within a 1/16 m 2 frame. Shoot density was determined from the number of shoots per sample. Shoot height was measured on 10 of the longest shoots representing the top of the leaf canopy in each sample. Rhizome length measurements were made of the total length of horizontal rhizome in each core sample. Root size was measured on selected roots attached to the rhozome and having an intact root tip . Leaf, rhizome, and root portions of the plant samples were separated, washed in fresh water, and dried to constant wt at 80 °C for 24 h to determine plant biomass. The weight ratios for carbon and nitrogen in plant tissue were mea sured on dry plant samples using a Perkin Elmer elemental analyzer. Total phosphorus was determined after persulfate oxidation (M enzel & Corwin, 1975).

. ).,". N " SOl mp,mg Site .".... '.:." • c. '. ..,Cu t Coy

"~ ' .

o 2 Mil es

I 74° 30" W Figure 1. San Salvador Island, Bahamas, showing the location of the study site west of Cut Cay in Graham's Harbor.

Interstitial nutrient depth profiles were determined from duplicate 4·7 ern diameter core sam ples collected by hand, sectioned into 50 ml pol ystyrene centrifuge tubes, capped, and centrifuged for 10 min at 1500 rpm. The interstitial water was removed through the cap with a syringe, injected directly into a Vacutainer, and frozen for NH~, PO~ -, analysis of and Si04 on a Technicon AutoAnalyzer (Zimmerman et al., 1977). Interstitial water samples were also collected using an in situ 'sediment sipper' , These samplers were constructed of hollow PVC stakes having a porous Teflon collar (Zimmermann et al., 1978; Montgomery et al., 1979) located at the required sampling depth (F igur e 2). The stakes were sealed except for a sampling tube extending into the bottom of the stake and a gas port at the top. The sippers were inserted into the sediment to the appropriate depth, argon gas at a very low pressure was used to force all water out through the sampling tube, suction was applied to the gas port with a hand pump to evacuate the sampler, and the interstitial water from around the porous collar slowl y seeped into the hollow stake. The interstitial water sample was removed using argon gas pressure to force the water out the sampling tube where it was collected directly into a Vacutainer. These samples were stored in the dark and transported back to the laboratory where sub-samples were removed with a syringe for immediate analysis of platinum electrode potential (Eh) on an Orion Eh probe, and of pH on a Fi sher combi nation pH electrode. The remaining interstitial water sample was frozen for further chemical analysis as described above. The sediment sippers were left in place in the sedime nt for subs equent sampling ofinterstitial water.

'. . ' · '1 i I !, i I i I I !

. i1 !

F igure 2. Photo of two 'sediment sippers' used to repeatedly collect sediment inter stitial wate r from a specific study site . The sampling method is de scribed in th e text. Not shown is a 1·9 mm ' 0 ' ring that seals the cap to the stake.

Nutrient regeneration rates were determined in jar exp eriments by measuring daily formation ofammonium, phosphate and silicate in isolated samples from three sediment depths (Aller & Yingst, 1980). Carbonate mud was obtained using a 16 ern diameter core sampler,S cm depth sections were placed in plastic bags and quickly sealed to avoid excessive contact with air. The mud was homogenized, packed into 50 ml polystyrene centrifuge tubes, and incubated under anoxic conditions in a mud-filled plastic bag at in situ temperatures. The rates of ammonium, phosphate and silicate production were determined by removing three tubes from each depth interval each day, separating interstitial water by centrifugation and extracting samples with a syringe through a hole punched in the plastic lid to avoid air contamination. The amount of adsorbed ammonium and phosphorus in the sediments was determined by extraction. Ammonium was extracted with 4 ml of 2 M KCl for 15 min on approximatel y 15 g ofsediment (Blackburn , 1979). Phosphate was extracted with filtered deoxygenated ocean wat er using 40 ml of water and 109 of sediment (Patriquin, 1972;

j K rom & Berner, 1980). Nutrients were anal yzed on the T echnicon AutoAnalyzer. -; Sediment samples were collected and determination of sediment water content was made by measuring wet w t and subtracting dry wt determined after 24 h at 80 °C. Organic content of th e sediment was calculated by measuring the dry wt and subtracting ash dry wt determined after combustion for 24 hat 500 °C. Water column samples were collected on four separate days and immediately frozen for later nutrient anal ysis.

::. ..'- . :.. ~.,

Phosphorus limitation in carbonate sediments 423

T ABL E 1. Sy ringodium fi lifo rme abundance at Cut Cay, San Salvador Island, Baham as. Samples were collected with a 1/16m2 frame (21 October) and 16cm diam eter core sampler (24 October)

Shoo t Rh izom e Rh izom e Sh oot density Leafbioma ss biomass Root biomass length height Sampl e date (no. m - 2) (g dr y wt m - 2 ) (g dr y wt m - 2 ) (g dr y wt m - 2) (m m - 2) (em)

21 October 1982 9020 151 ND ND ND 19 21 October 1982 10824 191 ND ND ND 18 24 October 1982 7905 130 376 460 220 15 24 October 1982 12444 171 426 214 261 20 24 October 1982 8568 154 260 234 233 18 Average 9752 159 354 303 238 18

ND-indicate s no data .

A seagrass growth experiment was conducted between 24 and 29 October 1983, to estimate S. filiforme leaf growth rate during thi s season. Seagrass leave s were clipped initially to a known height above the plant meristem, reclipped after 5 days, and the new gro wth mater ial was collected. Length of leaf growth was measured for 100 shoots and the combined dry wt was measured to obtain a weight-to -len gth ratio.

Results Seagrasses are extremely abundant in the shallow waters around San Salvador Island in the Bahamas (F igure 1). The seagrass bed at Cut Cay was nearly devoid of epiphytes, a condition that appeared related to the large congregations of grazing snails, Cerithium litteratum (M ikkelsen, personal communication), that mo ved in groups around the seagrass bed. The density of S. filiforme shoots in the Cut Cay seagrass bed was high, 2 2 averaging 9752 shoots m - (T able 1). Leaf biomass, 159 g dry m - , was lower than the below ground biomass of 657 g dry m - 2, and leaves had a relatively low canopy height (shoot height of 18 ern), The root biomass and rhizome biomass (T able 1) were equally large with an extensive rhizome network 3-4 cm below the sediment surface and extremely large diameter (1 mm) roots extending 20-30 cm into the sediment. S. filiforme leaf regrowth rate was measured as an indicator of plant production rate. Leaf regrowth ranged from 0·5 to 1·4 ern shoot- 1 d - 1 and the dry weight-to-length ratio for the se leaves was O·65 mg ern - I. The mean ± 95 % CI for leaf growth was I 0·95 ± 0·25 em shoot - 1 d -I. The average shoot growth rate was 0·62 mg dry shoot - I d - or, given th e observed shoot density from Table 1 and % C from T able 2, the growth rate is 2·0 gC m - 2 d -I . Si fi liforme plant tissue from the Cut Cay seagra ss bed contained sma ll percentages of nitrogen and phosphorus relative to carbon (T able 2). In comparing plant parts, leaves were found to be high est in nitrogen and phosphorus, while rhizomes were highest in carbon. The N: P was relatively contant for all S . fi lifo rme plant parts (T able 2). Nutrient concentrations in the overlying water were N~ < 1·0 11M, NO; < 0·1 11M and PO~ - undetectable ( < 0·08 11M). Nutrient resources in the seagrass bed sediments (13% organic content, including root and rhizome material) generally showed a pattern ofdecreased concentrati on with depth into the sediment (F igure 3). The maximum ammonium concentration in the sed iment -j 424 F . T . Short et al.

I I TABLE 2.Chemical nutrient tissue compos ition and nutrient ratios for Sy ringodium ! filiforme from San Salvador Island C:N :P C :N :P C N P Seagrass" (% dry wt) (% dry wt) (% dry wt ) Wt ratio Atom ic ratio

L eaves 32·8 1·29 0·061 538 :21 : 1 1390 :47:1 Rh izomes 37· 1 0·59 0·027 1374 : 22: 1 3550: 49 : 1 Roots 32·2 0·78 0·040 805: 20 : 1 2080 : 44 : 1

"Maxim um coefficient ofvariation for leave s is 0,05, for rhizome is 0'11 , and for roots is 0·09 (N= 4).

Core Cor e 2

Insl. HOH (°10 ) Insl. HOH (Olo )

0 40 8 0 0 40 80 I , I I I I I :~ I I :~I I

P04 - P (I'M) P04 - P (I'M)

0 '0 2 ·0 4'0 0'0 2'0 4 '0 :~ r I 1 ~ t=J I I E I 15 ~

.I: ..Do 0 NH 4-N {I'M} NH 4 -N (I'M)

0 100 200 0 100 200 , I I I I I I~[; II~ I 15 I

NH 4 (nmol ml-' ) NH 4 (nmol ml-')

o 80 16 0 o 80 160 :~I w,~ , :~II---~~ I F igure 3. Sediment profiles in a Sy ringodium fili/orme bed in San Salvad or , Bahamas. Depth profile s for two sedi ment core sam ples showing th e 0-5,5-10, 10-1 5 em depths for percent interstiti al water, interstitial phosphate and ammonium concentrations, and the am ount of dissolved (open bar s) and ad sorbed ammonium (hatched bars) per cubic cent imeter of sediment.

interstitial water was 100 11M for two core samples in the Si filiforme bed. Phosphate con centration in the interstitial water was low, gen erally less th an 2·0 11M. The N : P for ammonium and phosphate in the interstitial water averaged 60 : 1. Time course samples of interstitial water using the sediment sippers th rough a 5-day period showed a .. .. ;

Ph osphoru s limitation in carbonate sediments 425

7·5

7·4 I n 7·3

7·2

- 2 25

:;- -275 E .-;..::: ..- s: ..~ ~ ...... : .J w -325

- 375

. ", ;"E ::I.. 50 z I + v 25 I Z a

2·0

:::E ~ 1·5 a. 1 0 1·0 , . a. . . -: . 0 ·5 3 4 Days Figure 4. Five da y time course of changes in sedim ent interstitial water samples col lected from three replicate in situ sediment sippers at a sedim ent depth of 5-10 cm (mean ± SE).

relatively con stant platinum electrode potential (Eh) and pH, and decreasing NH~ and PO~ - (F igure 4). The higher nutrient concentrations measured by the coring method may be a result of disruption of roots that stimulated rapid regeneration in the sediment samples. Additional nitrogen available to the seagrass as ammonium adsorbed onto sediment particles was shown to be nearly equal to the amount of interstitial ammonium (inter stitial = 1'1 x ad sorbed, Figure 3 and Table 3). Adsorbed phosphorus removable by two extractions averaged greater than 5 times the interstitial phosphate (T able 3). In jar exp eriments the regeneration of nutrients in carbonate sediment interstitial water was highest in the upper 5 ern and decreased with depth (T able 4). Ammonium production rates had a strong linear relationship with time (correlation coefficient, r > 0'85) at all three sediment depths. The proportion ofad sorbed ammonium on the car bonate sediments was similar in both the initial samples and the samples incubated for three days (T able 3). Phosphate concentration changes in the incubation experiment

..... I i 426 F. T . Short et al. 1 I -.J I I TABLE 3. Interstitial and extractable phosphate and ammonium for 3 depth sections in I core samples of carbonate sediment fro m a San Salvador Island seagrass be d and in I sediment sam p les at th e end of a time course incubation. Values expressed on a j sed iment volume basis ! i ! PO~ NH~ i - (nmol em - 3) (nmol em - 3) I I Sediment depth Interstitial Seawater Seawater Interstitial KCI I (em) water extraction 1 extraction 2 water extraction i -,! Initial samples ! Core 1 o-S 2·1 3·S 2·2 37·3 38 ·4 ::"< 5-10 1·1 3·1 2·1 27 ·3 40 ·3 1001S O'S 1·7 I·S 27·S 26·4 Core 2 o-S 1·2 2·1 I ·S 79·7 72-3 5-10 2·2 8·S 4·8 98·9 90·9 1001S 4·9 10·0 S·2 162·6 13S·2

Samples after 3 days in incubation experiment Core 1 o-S 2·2 11·9 S·8 1401 3068 5-10 0·8 6·S 3·3 444 34S 1001S 1·7 6·3 2·S 426 228 Core 2 o-S 2·S 11·7 S·9 3S41 3884 5-10 0·8 6·0 2·4 710 236 1001S O'S 4·6 2·6 290 247

TABLE 4. Rates ofnutrient regeneration as determined in 3 day incubation experiment. All rates are expressed as 11Md -1 . Correlation coefficients (r) indicate th e linearity of the nutrient accumulation over the incubation period

Sediment depth (ern) Ammonium Phosphate Silica

o-S 988 0·60 33· 1 (0'87) (0'70) (0'99) 5-10 479 0·08 12·6 (0'9S) (0'28 ) (0' 97)

; 1001S 387 0·2S 6·4 (0' 86) (0' S2) (0'99)

were small and tend ed to be less linear (Table 4). The correlation coefficients for the deeper samples were not significant and the actual amounts of phosphate in th e inter stitial water were not different betw een th e initial and final samples during the incuba tion experiment (Table 3). The amount of seawater-extractable phospha te in two sets of samples showed more than double the amo unt ofadsorbed phosphate after th ree days of incubation. T he silicate regeneration rates decreased with depth . The silicate concentra tion change with time demonstrated a very strong linear relationship at all three sedi ment depths (T able 4). The mineral regeneration of silica is incl uded to indicate the homogeneity of the incubated sediment and th e integrity ofthe incubation experiment. Phosphorus limitation in carbonate sedim ents 427

TABLE 5. Comparative C : N : P ato mic ratios for seagrass es from around the world

C :N :P" Seagr ass atomic ratio Referenc e"

L eaves Enhalus acoroides (Palau) 1000 : 48:1 Sy ringodium fi liforme (Bahamas) 1390 :47 :1 This stu dy Zostera marina (Virginia) 584 : 4 1 : 1 Posidonia oceanica (Corsica) 956 : 39 : 1 Thala ssia testudinum (Barbados) : 32: 1 Posidonia ostenfeldia (W . Au stralia) 1070: 29 : 1

' , ' Thalassia hemprichii (N. Queensland) 599 : 27 : 1 Phyllospadix scouleri (Californ ia) 509 : 24 : 1 A mphib olisgriffithii (W . Au stralia) 535 : 20: 1 Cymo docea serrulatat (N . Queensland) : 19 : 1 Birch (1975) Halodule univervis (N. Queensland) 623 : 18 : 1 Sy ringodium isoetifo lium (N . Queensland) : 17 : 1 Birch (1975) Z ostera capricorni (N. Queensland) : 17 : 1 Birch (1975) Posidonia sinuosa (W . Au stral ia) 512 :16 :1 Cymodocea nodosa (Corsica) 408 : 15 : 1 Rhiz ome Syringodium filiforme (Bahamas) 3550 : 49: 1 This study Posidonia oceanica (Corsica) 1749: 40 : 1 Thalassia testidinum (Barbados) : 20 : 1 Enhalus acoroides (Palau) 659: 16 : I Halodule univ ervis (N. Queensland) 388 : 14 : I Cy modocea serrulata (N . Qu een sland) 872: 13 : I Syringodium isoetifolium (N. Queensland) : 10 : 1 Birch (1975) Z ostera capricorni (N. Queensland) : 8 : 1 Birch (1975) Roots Posidonia oceanica (Corsica) 3550 : 61 : 1 Syringodium fi liforme (Bahamas) 2080 : 44 : 1 This study Posidonia sinuosa (W. Au stralia) 809 : 18 : 1

"H ighest reponed N : P known for each seagrass species. bValues from Atkinson & Smith (1983) unless otherwise noted .

Discussion Abundant S. filiforme was found in a pure stand having average total biomass of 816 g dry m - 2 and a relatively high leaf growth rate (2'0 gem- 2 d - I ) for late October. This is

..•.. in the range of other reported rates for this species and comparable to production rates for other seagrasses (Zieman & Wetzel, 1980; Fry, 1983) although this is only a portion of the whole plant growth. From the measured gro wth rate, biomass, and tissue content, both the nutrient requirements and existingnutrient pool sizes can be calculated. Plant biomass represents a pool of0·10 g P m - 2 and 2·05 g N m - 2 in the leaves, 0·10 g P m - 2 and 2·09 g N m - 2 in the roots, producing a total seagrass pool of0·32 g P m - 2 and 6·50 g 2 .', N m- or aN: P of20: 1. Root biomass in this S .filiforme bed accounts for more than one-third of the total plant biomass (T able 1). The large portion of nitrogen and phos phorus in these roots (T able 2) is not typical for seagrasses (Birch, 1975; Aioi & Mukai, 1980; Atkinson & Smith, 1983). Similarly, the C: N : P for S ifiliforme rhizome is greater than that reported for other seagrasses (T able 5). The high leaf N : P is alm ost three times the atomic ratio reported for Syringodium from Australia (T able 5). Additionally, the atomic ratio for leaves (N:P = 47) is higher than any values reported for marine or -;

; 428 F. T. S hort et aI. I I • I

I fre shwater spermatophytes which range from 5 to 41 except for one value of 48 for ! Enh alus acoroides from Palau (Raven, 1981; Atkinson & Smith, 1983). Phosphorus depletion is not considered the typical situation in marine systems where the atomic -I ratio, C: N : P, for marine plankton was established as 106: 16: :1 (Redfield et al., 1963). i :! The equivalent ratio for the photosynthetic portion of many seagrass species averages 507 : 21: 1 (Atkinson & Smith, 1983). Comparison to the ratio for S. filiforme leaves, C : N : P= 1390 : 47 : 1, suggests depletion of both phosphorus and nitrogen relative to carbon. The low nitrogen and phosphorus content of these plants indicates that the plant system has adapted to conditions ofscarce primary nutrient resources. The average N:P of 47 for Si filiforme tissue content in San Salvador is similar to the 60 ratio for the inter stitial water from core samples, although the sediment sippers indicate the N : P in the seagrass root zone may actually be lower. The nitrogen available for plant growth is acquired from three major sources: (1) the low concentration present in the water column; (2) fixation of nitrogen in the plant phyllosphere and rhizosphere (Capone, 1983); (3) decomposition oforganic matter in the carbonate sediments, regenerating ammonium into the interstitial water. The measure ment of ammonium production in these carbonate sediments (T able 4), includingboth fixat ion and decomposition, indicates that a substan tial amount of ammonium can be generated in the sediments. These rates, 387-988 JlM d - 1, are much greater than rates reported for non-vegetated carbonate sediments (Rosenfeld, 1979). These three nitrogen sources in the seagrass bed must supply the nitrogen necessary for leaf, rhizome and root growth. Phosphate originates from two primary sources in the San Salvador seagrass beds: (1) low concentrations in the oligotrophic waters; (2) regenerated phosphorus from organic or inorganic material in the sediments. Phosphate concentrations in the water '; : ... column at San Salvador Island were low, typical ofopen ocean water. The net regenera tion rate of inorganic phosphorus in these carbonate sediments is relatively low com pared to non-carbonate sediments (0'6 JlM d - 1 vs. 3 JlM d - 1, respectively; Table 4 and Short et al., in preparation). An apparent low rate of regeneration in the carbonate sedi ments also observed in non-seagrass sediments (H ines & Lyons, 1982) suggests a phos phate removal mechanism in the sediments. The availability of phosphorus in carbonate sediments is limited by rapid adsorption onto carbonate (Patriquin, 1972; Berner, 1974). This process establishes an equilibrium with interstitial phosphate at concentrations of 0,5-2,5 JlM in these sediments (F igu re 3). Thus, the large proportion of phosphate adsorbed on carbonate sediments relative to ad sorbed ammonium is not reflected in the interstitial water concentrations even though this bound phosphorus is extractable in

" . J seawater. This phosphate equilibrium at low concentration and the N:P ratio of plant .. '; tissue suggest that the large amount of adsorbed phosphorus in the sediment is not readily available to seagrass plants. Since the uptake of phosphate by roots of the temperate seagrass Zostera marina is concentration dependent (Penhale & Thayer, 1980), it is expected that the rate ofnutri ent uptake by tropical seagrass roots in sediment of low phosphate concentration will be slow . This slow phosphate uptake rate appears to be the major obstacle to the accumu lation of phosphate in S.filtforme tissue. In contrast, the ammonium concentration in the sediment interstitial water provides a large supply of nitrogen to th e seagrass roots. The rate-limiting step ofphosphate uptake by S . filiforme roots ma y explain th e inordinately high root biomass obse rved for these sediments. Increasing the root surface area is an . " "'" ' ~ ' <. ~ - ' .. .

Ph osph oru s lim itation in carbona te sediments 429

effective morphological mechanism for increasing nutrient uptake at low concentrations (Short, 1983a). Thus the acquisition of phosphate by S . filiforme is limited by both the sparse supply in the water column and the plants' inability to rapidly take up phosphate from the sediments. Additional experimental research is required to determine to what extent the inacces sible phosphorus resources limit seagrass production . In the Bahamas, the leaf growth rate of S. filiforme and a high plant biomass indicate th at th e nutrient dynamics in th is system are tightly coupled. Phosphate, although abundant in the sediments, occurs at low concentrations in th e interstitial water thus limiting the rate of phosphorus uptake. The inability to rapidly accumulate phosphorus from the sediments appears to be the primary factor resulting in phosphorus depleted plant tissue. However, S. filiforme can ma intain substantial primary production even th ough sediment geochemical processes produce nutrient stress.

" '. ". Acknowledgements We are grateful to th ose assisting in th e field program including Don Gera ce, Paul J.ensen and th e crew of the R!V Johnson . We also thank John Ryther, Dennis Hanisak, Berry Lyons, Mark Hines, Peter McRoy and Catherine Short for criticism on the manuscript. This work was supported by Harbor Branch Foundation (C.N. 375), the CCFL Bahamian Field Station (C.N . V-ll5), and the Center for Marine Biotechnolog y, H arbor Branch. Jackson Estuarine Laboratory, UNH C.N. 168.

References Aioi, K . & Mukai, H . 1980 On the distribution oforgan ic contents in a plant ofeelgrass (Zostera marina L.). JapaneseJ ournal ofEcology 30,189-1 92. Aller , R. C. & Yingst, J. Y. 1980 Relation sh ip between micro bial di stribution and th e an aer obi c decompo sition of organic m atter in surfce sediments of Long Island Sound, U. S.A. Marine Biology 56, 29-42. Atkinson , M . J. & Sm ith, S. V. 1983 C : N : P ra tios of benthic marine plants. Limnology and Oceanography 28, 568-574 . Berner, R.A. 1974 K inetic mod els for th e earl y diagenesis of nitrogen, sulfur, ph osphoru s, an d silicon in anoxic marine sediments. In The Sea Vol. 5 (G oldberg, E. D ., ed .). John Wi ley, N ew York. pp . 427-450. Bir ch, W .R. 1975 Som e che mical and calorific prop ert ies of trop ical marine an giospe rms compared with th ose ofoth er plants. J oum al of Applied Ecology 12, 201-212. Blackburn , T .H . 1979 M eth od for measurem en t rates of NIr,; turnover in anoxic marine sediments, using IS N-NIr,; dilution techniqu e. Applied Environmental Microbiology 33(4),760--765. . './ Buesa, R. J. 1975 Pop ulation biom ass and metabolic rates of marine angiosperms on the northern Cuban she lf. Aquatic B otany 1, 11-23.

Capo ne, D. G . 1983 N 2 fixation in seagrass communities. Marine Technical Society J ournal 17, 32-37. Capo ne, D . G. & T aylor, B. F . 1977 Nitrogen fixation (acetylene reduction ) in th e phyllosphere of Thalassia testudinum , M arine Biology 40, 19-28. ..:: D eKanel, J. & M orse, J. W . 1978 The chemis try of ortho phospha te uptake from seawater on to calcite and arago ni te. Geochimica et Cosmochimica Acta 42, 1335- 1340. D en H artog, C. 1970 The Seagrasses of the Wor ld. North H olland Publish ing Co mpa ny, Amsterd am . 275 pp. En tsch , B., Boto, K. G ., Sim, R . G. & We lling ton, J. T . 1983 Phosph orus and nitrogen in coral reef sediments. Limnology Oceanography 28, 465-476. Fen chel, T . M., M cRoy, C. P., Og den, J. c., Parker, P. & Rainey, W . E. 1979 Symbio tic cellulose degrada tion in green tu rtles, Chelonia my das L. A pplied Env ironmenta l Microbiology 37, 348-350. F ry, B. D . 1983 Leaf growth in th e seagrass Syringodium fi liforme, Kiitz. Aquatic B otany 16, 36 1-368. Gaudette, H . E. & L yon s, W . B. 1980 Ph osphate geochemis try in nearshore carbo na te sedime nts : sugges tion of apa tite formation . In Ma rine Phosphorites-Geochemistry , Occurrence, Genesis (Bentor, Y. K ., ed .) SEMP Special Publication 29. Tulsa, Oklahoma. pp . 215-225. G ilbert, S. & Clark, K. B. 1981 Seasonal varia tion in standing cro p ofth e seag rass Syringodium filiforme and associated macrophy tes in the Northern Indian River , Fl orida. Estuaries 4, 223-225. -~ .

- "' _~_ ·'·'''':-:':'';'': A

430 F . T . Short et al.

" " H ines, M. E . & L yon s, W . B. 1982 Biogeochemi stry of nearshore Bermuda sedime nts. I. Su lfat e reduction rate s and nutrient generatio n . M arin e Ecology Progress Series 8, 87-94. Iizumi, H ., H attori , A. & M cR oy, C. P. 1980 Nitrate and nitrite in inters titial waters of eelgr ass beds in relatio n to th e rh izosphere. J ournal ofExp erimental M arine B iology and Ecology 48, 191-201. Iizumi, H., H attori , A. & M cR oy, C. P . 1982 Ammonium regenerati on and assimilation in eelgrass (Z ostera marina) bed s. M arine B iology 66, 59-65. K enworthy, W . 1., Ziem an, 1. C . & Thayer, G . W . 1982 Evidence for th e influence of seag rass es on the ben thi c nitrogen cycle in a coasta l plain estuary near Beaufort, N orth Carolina (U .S.A.). Oecologia 54, 152-158. . Krom , M . D. & Berner, R. A. 1980 Ad sorption of phosphate in anoxic marine sediments. Limnology and Oceanography 25, 797-806. McMahan , C. A. 1968 Biomass and salinity tolerance of shoalgrass and manateegrass in lower L aguna ., M adre, Texas. J ournal of W ildlife Management 32, 501-506. McMillan , C. 1979 Differ entiation in response to chilling temperatures am ong population s of three marine spe rrnatophy tes, T . testudinum, S.filiforme and H . wrightii. American J ournal of B otany 66, 810-819. McRoy, C . P . & M cMillan , C . 1977 Production ecology and physiology of seagrass . In Seagrass Ecosystems (M cRoy, C. P. & H elfferich, c., eds). Marcel Dekker In corporated, New York. pp. 53-87. M enzel, D . W. & Co rw in, N . 1965 The me asurem ent of total phosphorus in seawater based on the liberation of orga nically bound fraction by persul fate oxidatio n . Limnology and Oceanography 10, 280-282. M ontgomery, 1. K , Zimmermann, C . F . & Price, M . T. 1979 The collection, ana lysis and varia tion of nutrients in estuarine pore water. Estuarine and Coastal M arine S cience 9, 203-214. Patriquin, D . G . 1972 The origin of nitrogen and phosphorus for growth of th e marine angiosperm Thalassia testudinum. Marine Biology 15, 35-46. Penhale, P . A. & T hayer, G. W . 1980 Uptake and transfer of carbon and phosphorus by eelgrass (Z ostera marina L. ) and its epiphy tes. J ournal ofExperimental Marine Biology and Ecology 42, 113-123. Philips, K C. 1960 Observati on s on th e ecology and distribution of the Flor ida seagrasses. Fl or ida St ate Board of Conservation M arine L aboratory, St Petersburg, Florida. Prof essional Papers Series 10,1-10. Raven, 1. A. 1981 Nutrition al strategies of subme rged benthic plants: the acquis itio n of C, Nand P by rhizophytes and haptophyte s, New Phytologist 88, 1-30. Redfield , A. c., Ketchum, B. H. & Rich ards, F . A. 1963 The influence of or ganisms on the composition of sea-water. In The S ea, Vol. 2 (H ill, M . N ., ed .) Iohn W iley, New York. pp. 26-77. Rosenfeld , 1. K . 1979 Interstitial water and sedi ment chemistry of two cores from Florida Bay. J ournal of S edimentary Petrology 49, 989-994. Sh ort, F. T . 1983a The seagrass, Z ostera marina L.: plant morphology and bed structure in relation to sedi ment ammon ium in Izembek Lagoon , Alaska. Aquatic B otany 16, 149-161. Sh ort, F . T . 1983b The re spon se of interstitial ammonium in eelgrass (Z ostera marina L.) beds to env ironmental perturbati ons.J ournal of Experimental M arine B iology and Ecology 68, 195-208. Sh ort, F. T ., M ontgomery, 1. R . & Zimmermann, C. F . 1985 Sea sonal Seagrass Abundance and Nutrient D ynamics of a Syringodium filiforme Klitz. bed in th e Indian River L agoon , Florida, U .S.A.(in preparation). Strawn, K . 1961 F actor s influencing the zona tion of submerged monocotyledons at Cedar Key, Florida. J ournal of Wildlife Management 25, 176-189. Thompson , M . 1. 1978 Species composition and distribution of seagrass beds in the Indian River lagoon, Fl orida. Florida Scientist 4, 90-96. . " . ~ : Tribble, G . W . 1981 Reef-based herbivores and the distribution of two seagrasses (S . filiforme and T . testudinum ) in the San BIas Islands (W estern Caribbean ). M arine Biology 65, 277-28 1. Will iam s, S. L. & M cR oy, C. P . 1982 Seagrass productivity: the effect of light on carbon uptake. Aquatic B otany 12, 321- 344. Zieman , 1. C. & We tze l, R. C. 1980 Productivity in seagrasses: methods and rates. In Handb ook of S eagrass Biology , an Ecosystem Perspective (P hilips, R. C. & M cR oy, C. P., eds ) Garland STPM Press, New York . pp. 87-116. Zimmermann, C. F ., Price, M . T . & M ontgom ery , 1. R. 1977 Operati on s, method s and qualit y control of T echnicon AutoAna lyzer II systems for nutrient determination s in seaw ater. R eport N o. 11. Harbor Bran ch Foundation , In c., Fort Pierce, Flor ida. Zimmermann, C. F ., Pri ce, M. T . & M ontgom ery, 1. R. 1978 A compari son of ceramic and teflon in situ samplers for nu tr ient por e water determination s. Estua rine and Coastal Marine Sci ence 7, 93-97. .1;,....